Regional (14C) 2-deoxyglucose uptake during forelimb movements evoked by rat motor cortex...

THE JOURNAL OF COMPARATIVE NEUROLOGY 224259-285 (1984)

Regional (14C> 2-Deoxyglucose Uptake During Forelimb Movements Evoked by

Rat Motor Cortex Stimulation: Cortex, Diencephalon, Midbrain

FRANK R. SHARP Department of Neurosciences, University of California, San Diego, School of Medicine,

La Jolla, California 92093

ABSTRACT The caudal forelimb region of right “motor” cortex was repetitively

stimulated in normal, conscious rats. Left forelimb movements were produced and (I4C) 2-deoxyglucose (2DG) was injected. After sacrifice, regions of increased brain (14C) 2DG uptake were mapped autoradiographically.

Uptake of 2DG increased about the stimulating electrode in motor (MI) cortex. Columnar activation of primary (SI) and second (SII) somatosensory neocortex occurred. The rostra1 or second forelimb (MII) region of motor cortex was activated.

Many ipsilateral subcortical structures were also activated during forelimb MI stimulation (FLMIS). Rostra1 dorsolateral caudate-putamen (CP), central globus pallidus (GP), posterior entopeduncular nucleus (EPN), subthalamic nucleus (STN), zona incerta (ZI), and caudal, ventrolateral substantia nigra pars reticulata (SNr) were activated. Thalamic nuclei that increased (14C) 2DG uptake included anterior dorsolateral reticular (R), ventral and central ventrolateral (VL), lateral ventromedial (VM), ventral ventrobasal (VB), dorsolateral posteromedial (POm), and the parafascicular-centre median (Pf-CM) complex. Activated midbrain regions included ventromedial magnocellular red nucleus (RNm), posterior deep layers of the superior colliculus (SCsgp), lateral deep mesencephalic nucleus (DMN), nucleus tegmenti pedunculopontinus (NTPP), and anterior pretectal nucleus (NCU).

Monosynaptic connections from MI or SI to SII, MII, CP, STN, ZI, R, VL, VM, VB, POm, Pf-CM, RNm, SCsgp, SNr, and DMN can account for ipsilateral activation of these structures. GP and EPN must be activated polysynaptically, either from MI stimulation or sensory feedback, since there are no known monosynaptic connections from MI and SI to these structures. Most rat brain motor-sensory structures are somatotopically organized. However, the same regions of R, EPN, CM-Pf, DMN, and ZI are activated during FLMIS compared to VMIS (vibrissae MI stimulation). Since these structures are not somatopically organized, this suggests they are involved in motor-sensory processing independent of which body part is moving. VB, SII, and MI1 are activated during FLMIS but not during VMIS.

Key words: brain glucose, metabolism, motor pathways

Accepted September 28, 1983.

0 1984 ALAN R. LISS, INC.

260 F.R. SHARP

Studies of the physiology and anatomy of motor cortex (Asanuma, '75; Brooks and Stoney, '71; Evarts and Thach, '69; Kuypers and Tuerk '64; Kuypers and Lawrence, '67; Kuypers and Brinkman, '70; Phillips and Porter '77; Wool- sey, '58, '67, '81; Woolsey et al., '50, '75; Woolsey and van der Loos, '70), motor thalamus (Kunzle, '75, '76, '77, '78a,b; Kunzle and Akert, 77; Rispal-Padel and Massion, '70; Ris- pal-Padel and Grangetto, '77; Rispal-Padel et al., '73; Strick, '73, 75, 76; Strick and Preston, '82), basal ganglia (Beck- stead, '79; Carpenter, '76; Carpenter et al., '67, '76, '81a,b; Grofova, '79; Mehler, '71; Mehler and Nauta, '74; Nauta and Cole, '78; Van der Kooy, '79; Van der Kooy et al., '81; Van der Kooy and Hattori, '80; Van der Kooy and Carter %l), and midbrain structures (Brodal, '81; Brodal et a1.,'72; Veazey and Severin, '80a,b, '82; Edwards, '72, '75; Edwards et al., '72, '78, '79) have advanced our understanding of the complex motor-sensory systems involved in the production of voluntary and reflex movement. A somatotopic functional and anatomical organization has been proposed for many, but not all, subcortical motor-sensory structures. From the studies performed, however, it is often difficult to know whether some, or all, of the subcortical structures implicated in production or modulation of movement are actually activated during a particular movement or not and which region of each structure is involved.

To help answer such questions, we have recently described the regions of increased (*4C) 2-deoxyglucose (2DG) uptake in brains of rats that had repetitive vibrissae movements produced by repetitive electrical stimulation of "motor cortex." In the present and accompanying study we describe the regions of increased (I4C) 2DG uptake in brains of rats that have repetitive forelimb movements produced by repetitive electrical stimulation of motor cortex. The cortical and subcortical regions activated during forelimb movements are compared to the regions activated during vibrissae movements. Some subcortical structures are activated only during forelimb or only during vibrissae movements, but most are activated during both. Within a given structure activated during both forelimb and vibrissae movements, activated regions either overlap completely or partially or not at all. The presence or absence of overlap during forelimb, compared to vibrissae movements, implies functional differences between structures, which are dis- cussed.

METHODS This study autoradiographically maps increased (I4C) 2-

deoxyglucose (2DG) uptake in rat brain during cortex-stimulated forelimb movements using methods identical to those used to study vibrissae movements (Sharp and Evans, '82). The methods are based on those of Sokoloff ('79) and Soko- loff and his collaborators ('77). Twenty 300-400-gm female Sprague-Dawley rats were used. Food and water were pro- vided ad libitum until 24 hours prior to the experiment, when food was withheld.

Rats were anesthetized with ketamine (80 mgkg) and Rompun (8 mgkg). They were placed into a David Kopf stereotaxic apparatus with blunt ear bars. Care was taken not to rupture the ear drum as this affects cerebral glucose metabolism in auditory structures. The skin was incised over the skull and a burr hole was drilled 0.8 mm anterior and 3.0 mm lateral to bregma over right motor (MI) cortex. A coaxial electrode, with an inner contact diameter of 200 pm and an outer contact diameter of 500 pm with 500 pm between contacts (Rhodes Medical Instruments) was low-

ered into cortex avoiding large arteries and veins as much as possible. Only one cortex penetration was performed per animal because of possible cortex injury from multiple penetrations.

During anethesia, stimulation with a Grass Constant Voltage stimulator (sometimes with a constant current unit) or a Bak BPGl stimulator with constant current unit was begun at 5 trainskecond. The bipolar electrode was slowly lowered into primary motor cortex (MI; a complete abbre- viation list precedes Fig. 1) to the depth at which left-sided forelimb movements were obtained by lowest current. This depth was generally between 1.3 mm and 1.8 mm. All animals had isolated left forelimb movements under anesthesia. Stimulation was stopped and the electrodes ce- mented into place with methyl-methacrylate. Animals were removed from the stereotaxic apparatus, wound edges were infiltrated with xylocaine, and the animals were lightly taped onto animal boards and allowed to recover from anesthesia for 8-24 hours,

Cortex stimulation at 5 trainskecond was begun with the animal's forelimbs restrained when the animals were alert and fully recovered from anesthesia. Fifty-millisecond trains of 300 Hz, 0.5-msec biphasic pulses were delivered at a threshold voltage or current usually 20% to 60% less than that during anesthesia. Stimulation voltage or current was slowly increased above threshold until left, fairly stereo- typed 5/sec forelimb movements appeared; the voltage required was usually between 5 and 20 V and the measured current 30-120 pA. Within 5 minutes of stimulation movements of the left forelimb became less visible; from here on, stimulation was intermittently stopped and then restarted 10-15 seconds later to ensure that left forelimb movements were still produced by the trains of stimuli. Sometimes only one of the small digits of the left forelimb would contract at 5 times per second for the entire 45 minutes of stimulation. The animals showed no distress and sat very quietly during cortex stimulation. Only animals which had repetitive movements confined to the left forelimb were used. A dose of (I4C) 2-deoxy-D-glucose (Amersham, 57 mCi/mmole) was injected, via the tail vein, as a bolus of 16.7 pCi/lOO-gm body weight in 0.25 ml 0.9% saline and followed immediately by 0.25 cc 0.9% saline. Stimulation was continued at 5 trainskecond for a period of 45 minutes.

Forty-five minutes after injection of the (14C) 2DG, animals were sacrificed with pentobarbital. Without prior per- fusion, the brains were rapidly removed and frozen in 2- methyl butane cooled with dry ice, embedded in Lipshaw M1 embedding matrix, and sectioned at 20 pm on an Amer- ican Optical cryostat at -20°C. From one-third to two- thirds of the sections were saved in each case, picked up with coverslips, and dried on a hotplate at +70°C. Cover- slips were glued to cardboard; then Kodak SB5 x-ray film was placed on top of the brain sections in x-ray film cas- settes for 7 days with calibrated (14C) plastic standards. The film was developed in x-ray developer 5 minutes, washed 1 minute, fixed 5 minutes, washed 20 minutes, and dried (Sokoloff et al., '77; Sokoloff, '79). Selected brain sections which produced autoradiographs were stained with cresyl echt violet.

Optical densities on autoradiographs were measured on a MacBeth TD 502 LB densitometer with a 0.5-mm aperture. The densitometer was zeroed on the background of each x- ray film and the optical density (OD) for each structure was read on six different sections. As optical density was varia- ble within many structures, the highest optical density

2DG UPTAKE WITH MOTOR CORTEX STIMULATION 261

obtained for a gray matter structure was used, while the lowest optical density for a white matter structure was taken. Optical densities (OD) of each gray matter structure were averaged on each side of the brain and divided by the averaged optical density of the inferior cerebellar peduncle for each animal. These optical density ratios (OD gray matter/OD white matter) were then averaged for each structure on left and right sides of brain (Sharp et al., '83). Table 1 lists those structures for which there was a significant difference (P < 0.05) of the optical density ratios of left compared to right side of brain using the U test for ratios. Table 2 lists those structures for which there was not a significant left-right difference. Activated structures had L- R differences of greater than 0.20, and unactivated structures had L-R differences less than 0.10. In all illustrations, the right side corresponds to the side on which MI motor cortex was stimulated-i.e., the right side of the brain. More rostral sections of brain are pictured at the top, or top left, of each figure.

RESULTS Uptake of (14C) 2-deoxyglucose approximately doubled

throughout the thickness of a 2-mm-wide diameter region of cortex surrounding the track of the stimulating electrode (Table la; heavy arrows, Figs. ld,h,2a). The 2DG uptake increase about the electrode site was the largest of any activated brain region (Table 1, compare with next paper). Corpus callosum 2DG uptake increased posterior to the electrode site (Fig. 2c,g).

Anterior to the electrode site a right cortical region of increased 2DG uptake could be followed in the ventral layers of cortex just above forceps minor (Fig. lb,f,c,g). In very rostral portions of right cortex a diffuse increase of 2DG uptake occurred in the intermediate layers of cortex extending to superficial layers (Fig. la,e, Table 1). We labeled this the second forelimb region (MI11 in accordance

TABLE 1. Optical Density (OD) Ratios of Left (L) and Right (R) Sides of Brain Structures: Increased 2DG Uptake After Right Forelimb Motor

Cortex Stimulation'

TABLE 2. Optical Density (OD) Ratios of Left (L) and Right (R) Sides of Brain Structures in Which Right Forelimb Motor Cortex Stimulation Did

Not Increase 2DG Uptake on One Side of the Brain Compared to the Other'

OD Ratio OD Ratio L-R

Nucleus accumbens 2.29 2.27 0.02 Medial septal nucleus 1.59 1.61 0.02 Lateral septal nucleus 1.64 1.68 0.04 Preoptic n. hypothalamus 1.91 1.88 0.03 Ventromedial n. hypothalamus 1.61 1.61 0.00 Lateral hypothalamus 1.97 1.92 0.05 Dorsomedial n.hypothalamus 1.83 1.85 0.02 Piriform cortex 2.40 2.36 0.04 Hippocampus-molecular layer 1.75 1.74 0.01 Hippocampus-pyramidal layer 2.07 2.09 0.02

L R Difference

Nucleus of lateral olfactory tract 2.30 2.25 0.05 Paratenial n. thalamus 2.22 2.25 0.03 Anteroventral n. thalamus 2.67 2.62 0.05 Ventromedial n. thalamus 2.62 2.62 0.00 Zona incerta 2.61 2.65 0.04 Medial dorsal n. thalamus 2.48 2.40 0.08 Lateral habenula 2.80 2.79 0.01 Dorsal lateral geniculate 2.26 2.18 3.08 Basal amygdaloid nucleus 1.97 1.92 0.05 Posterior parietal cortex 2.36 2.30 0.06 Central gray 1.95 1.95 0.00 Substantia nigra compacta 2.00 1.96 0.04 Oculomotor nucleus 2.57 2.56 0.01 Occipital cortex 2.19 2.19 0.00 Cingulate cortex 2.33 2.33 0.00 Lateral pontine nuclei 1.90 1.91 0.01 Inferior colliculus 3.50 3.57 0.07 Nucleus reticularis tegmenti pontis 2.19 2.25 0.06 Dorsal tegmental nucleus 2.61 2.55 0.06 Locus coeruleus 2.26 2.24 0.02 Fastigial n. cerebellum 2.63 2.63 0.00 Cochlear nuclei-dorsal 2.67 2.60 0.07 Superior olive 2.85 2.85 0.00 Trapezoid body 2.85 2.88 0.03 Superior vestibular nucleus 2.90 2.93 0.03 Lateral vestibular nucleus 2.80 2.78 0.02 Spinal vestibular nucleus 2.94 2.96 0.02 Facial nucleus 1.99 1.94 0.05 Nucleus solitarius 2.07 2.11 0.04 Nucleus spinal tract of the

trigeminal nerve 2.25 2.21 0.04 Nucleus gracilis 1.96 1.94 0.02

'OD ratios = OD gray matter structurelOD cerebellar peduncles.

ODratio ODratio R-L Gray matter structure L R difference

a. 2DG uptake higher on right side of brain Motor cortex (MI)-stimulated site 2.82 5.12 2.30 Motor cortex (MII) 2.61 3.39 0.78 Somatosensory cortex (SI) 2.37 3.27 0.90 Somatosensory cortex (SII) 2.55 3.13 0.58 Anterior Caudate-putamen (CP) 2.45 3.13 0.22 Mid caudate-putamen 2.67 3.85 1.18 Posterior caudate-putamen 2.18 2.45 0.27 Globus pallidus (GP) 1.87 3.27 1.40 Entopeduncular n. (EPN) 1.74 2.27 0.53 Reticular n. thalamus (R) 2.27 2.72 0.45 Ventrolateral n. thalamus (VL) 2.47 3.47 1.00 Ventrobasal n. thalamus (VB) 2.38 3.13 0.75 Posteromedial n. thalamus (POm) 2.42 3.14 0.72 Parafascicular-CM n. thalamus (Pf-CM) 2.30 2.63 0.33 Subthalamic Nucleus (STN) 2.00 2.48 0.48 Deep mesencephalic nucleus (DMN) 2.64 3.04 0.40 Substantia nigra pars reticulata (SNr) 1.99 2.79 0.80 Red nucleus-pars magnocellularis (Rm) 2.45 2.70 0.25 Superior colliculus deep layers (SGsgp) 2.04 2.38 0.34 Nucleus tegmenti pedunculopontinus 2.04 2.38 0.34

Lateroposterior n. thalamus (LP) 2.51 2.28 0.23 Posterior n. thalamus (PO) 2.35 2.14 0.21

b. 2DG uptake higher on left side of brain

'Optical density (OD) ratios = OD gray matter structurelOD cerebellar peduncle.

with a recent physiological study (Neafsey and Sievert, '82). Uptake of 2DG also increased in right dorsolateral somatosensory cortex (Fig. 3a-f; Table 1). This probably corresponds to forelimb primary somatosensory cortex (SI), which overlaps with and is just posterior to forelimb motor cortex in the rat (Hall and Lindholm, '74). The broad region in forelimb motor cortex MI (Fig. 2a,b,e,f) merges into the more discrete, columnar increase of 2DG uptake in forelimb SI (Figs. 2c,d,g,h, 3a-f). Uptake of 2DG also increased in a separate region of somatosensory cortex on the lateral portion of the hemisphere not contiguous with MI or SI (Fig. 3). This region appears to coincide with the second somatosensory (SII) region of rat neocortex (Welker and Sinha, '72). The 2DG uptake increases that occurred in forelimb SI and SII somatosensory cortex were approximately 1.5 mm in diameter and extended through all of the layers of neocortex. There is a region of somatosensory cortex between SI and SII that was not activated (Fig. 3a-0.

2DG uptake increased in right dorsolateral caudate-putamen (CP) (Fig. 2a-h, Table 1) particularly in anterolateral portions (Figs. ld,h, 2a-c,e-g). Uptake of 2DG increased in dorsolateral and ventromedial portions of ex-

262

treme anterior CP (Fig. ld,h). In posterior CP there was patchy 2DG uptake adjacent to globus pallidus (Figs. 2d,h, 3a-f). There was a very small increase of 2DG uptake in left dorsolateral CP that mirrored that on the right side (Fig. 2c,g). However, the 2DG uptake increase in left CP occurred over a much smaller region than the right and did not extend as far anteriorly or posteriorly (Fig. 2a-h). Not infrequently, there was a distinct increase of 2DG uptake in a region of the right CP just adjacent to the lateral ventricle (Fig. 3b,e). This region may be analogous to the caudate in primates.

Uptake of 2DG increased dramatically in right globus pallidus (GP) during right MI stimulation (Table la). The increases occurred primarily in central portions of GP (Fig. 3), extending to the border of GP and CP. The most dorsal and ventral portions of GP were not activated (Figs. 3,4a,d), particularly anteriorly (Fig. 3a,d) and posteriorly (Fig. 4a,d). There was a small 2DG uptake increase in central portions of left GP as well (Fig. 3c,f). Uptake of 2DG increased in discrete portions of right internal capsule (CAI) adjacent to GP and R (reticular nucleus thalamus; Figs. 3c,f, 4a,d).

MI stimulation increased 2DG uptake in right entopeduncular nucleus (EPN; Fig. 5a-f, Table la). The activated portions of EPN occurred at the level of the middle and posterior ventrobasal nucleus WB) of thalamus (Fig. 5) .

F.R. SHARP

A AD AM AV C CA CAI cc CCA Ce CL CM CP cu DAO dmcc DMN EPN FLM FMI FR G GP gr HI HL iP LD LGd LGv LL LM LP MA0 MD med MG MI MI1 MV NCU

NF NI NL

Anterior portions of EPN were not significantly activated (Figs. 4b,c,e,f, 6a,d).

Reticular (R) nucleus of thalamus increased 2DG uptake (Table la) primarily in the dorsal, anterolateral portions of the nucIeus (Fig. 4). Ventral (Fig. 4) and posterior portions of R (Fig. 5) were not activated. The right ventrolateral WL) nucleus of thalamus also increased 2DG uptake during right MI stimulation (Table la). In anterior VL, 2DG uptake increased in central and lateral portions of the nucleus (Fig. 4c,D. In middle and posterior VL, 2DG uptake increased in ventral portions of VL (Fig. 5a,b,d,e).

A very large portion of the right ventrobasal WB) nucleus of thalamus was activated (Table la , Figs. 5 , 6). Uptake of 2DG increased in the ventral three-fourths of anterior and middle VB. The most dorsal portion of VB was not activated (Fig. 5a,b,d,e). In posterior VB the activated area decreased from the ventral half of the nucleus (Fig. 5c,f) to the ventral third of the nucleus (Fig. 6a,d) to a small crescent in ventrolateral VB (Fig. 6b,e).

Posteromedial nucleus (POm) of thalamus also increased 2DG uptake (Table la), particularly dorsolaterally (Fig. Ga,b,d,e). The activated regions of posterior POm continued uninterrupted posteriorly into activated portions of the parafascicular (Pf)-centre median (CM) complex of thalamus (Fig. 6c,f). The activated region occurs immediately adja-

Abbreuiations Accumbens n. Anterodorsal n. thalamus Anteromedial n. thalamus Anteroventral n. thalamus Caudate Anterior commissure Internal capsule Crus cerebri Corpus callosum Central medial n. thalamus Central lateral n. thalamus Centre median nucleus thalamus Caudate-putamen Cuneate nucleus Dorsal accessory olive Dorsomedial cell column inferior olive Deep mesencephalic n. Entopeduncular n. Medial longitudinal fasciculus Forceps minor Fasiculus retroflexus Gracilis n. Globus pallidus Granule cell layer of cerebellum Hippocampus Lateral habenula Interpeduncular n. Lateral dorsal n. thalamus Lateral geniculate-dorsal Lateral geniculate-ventral Lateral lemniscus Lemniscus medialis Lateroposterior n. thalamus Medial accessory olive Mediodorsal n. thalamus Medullary layer of cerebellum Medial geniculate Motor cortex primary Motor cortex secondary Medioventral n. thalamus Ventral deep mesencephalic n. (Anterior pretectal n.) Fastigial n. cerebellum Interpositus n. cerebellum Lateral n. (dentate) cerebellum

SL Sm sm SNc SNr SOL STN tsv VB VL VM VMb vm xcu ZI NTD NTPP NTV ntV nX nxI1 N 111 P pci PCM Pf Po PO POL POM POm POV R rh Rm RP RTP s c s g p

scsgs

SGC SI SII

Nucleus lateralis septi Submedial n. thalamus Striamedullaris thalamus Suhstantia nigra pars compacta Substantia nigra pars reticulata Nucleus solitarius Subtbalamic nucleus Spinal tract of the trigeniinal nerve Ventrobasal compiex thalamus Ventrolateral n. thalamus Ventromedial n. thalamus Ventromedial basal n. thalamus Medial vestibular n. External cuneate Zona incerta Dorsal tegmental nuclei Nucleus tegmenti pendunculopontinus Ventral tegmental nuclei Nucleus of spinal tract of trigeminal nerve Vagal n. Hypoglossal n. Nucleus of oculomotor nerve Corticospinal tract Inferior cerebellar peduncle Middle cerebellar peduncle Parafascicular n. thalamus Principle olive Posterior n. thalamus Lateral pontine nuclei Medial pontine nuclei Posterior complex media1 division thalamus Ventral pontine nuclei Reticular n. thalamus Nucleus rhomboideus Red n. magnocellularis Red n. parvocellularis Reticular tegmental n. of pons Superior colliculus stratum griseum profundum Superior colliculus stratum griseum superficialis Substantia grisea centralis Somatosensory cortex SI Somatosensory cortex SII


e

f

Fig. 1. In these (14C) 2-deoxyglucose (2DG) autoradiographs (a-d) and line drawings (e-h) right motor cortex stimulation (d) produced repetitive left forelimb movements. Uptake of 2DG increased in a large region about the

stimulating electrode in MI cortex (d,h). A small region of increased 2DG uptake was observed in right frontal cortex (a,e) far removed from where the electrode was located (heavy arrows, d and h).

Fig. 2. These (14C) 2DG autoradiographs show the site of electrical stimulation of right motor cortex (MI, a,e), and increased 2DG uptake in right (CP) caudate-putamen (a-h) and (SI) somatosensory cortex (d-h). The Nissl-stained section in e produced the 2DG autoradiograph in a.

2DG UPTAKE WITH MOTOR CORTEX STIMULATION

Fig. 3. Regional increases of (I4C) 2DG uptake occur in SI somatosensory cortex, SII somatosensory cortex, internal capsule (CAI), and central portions of globus pallidus (GP). The Nissl-stained section in f produced the adjacent 2DG autoradiograph in c. Note the patchy 2DG uptake increases in right posterior caudate-putamen (a-c).

265

266

Fig. 4. Right forelimb MI stimulation increased (“Ci 2DG uptake in anterodorsolateral reticular n. of thalamus (Rl, internal capsule (CAI), globus pallidus IGP), and ventrolateral n. thalamus (VLi. The Nissl-stained section in d produced the 2DG autoradiograph in a.

F.R. SHARP


Fig. 5. These (14C) 2DG autoradiographs (a-c) and line drawings (d-D show the anterior half of rat thalamus. 2DG Uptake increased in right ventral ventrolateral nucleus (VL), right ventrobasal nucleus (VB), right posteromedial nucleus (Porn), and a small amount in lateral parts of right ventromedial nucleus (VM) of thalamus. Uptake of ('4C) 2DG also increased in the right entopeduncular nucleus (EPN).

268 F.R. SHARP

Fig. 6. These (14C) 2DG autoradiographs (a-c) and line drawings (d-fl show the posterior half of rat thalamus. 2DG Uptake increased in right VB, POm, VM, and the parafascicular-centre median (Pf- CM) complex of thalamus. A punctate increase of 2DG uptake also occurred in right internal capsule (CAI) (b-0.

E


cent to the fasciculus retroflexus (FR) (Fig. 7a-d) but also extends fairly far laterally (Fig. 7). There was consistent activation of right Pf-CM (Table la).

In a number of animals, 2DG uptake was less in the right lateral dorsal (LD; Fig. 5b,e) and right lateral posterior (LP) nuclei of thalamus (Fig. 6a,b,d,e) than on the left side (Table lb). Uptake of 2DG in the right posterior nucleus of thalamus (PO) was also less than in left PO (Fig. 7a-c, Table lb). LD, LP, and PO were the only structures in thalamus or above the pons to have higher 2DG uptake on the left side of the brain compared to the right side during stimulation of right forelimb motor cortex. Uptake of 2DG increased slightly in the right zona inserta (ZI; Figs. 6b,e, 7b,d). Op- tical density measurements, however, did not reveal a consistent change of 2DG uptake in ZI (Table 2). Right ventromedial nucleus (VM) of thalamus might have increased 2DG uptake in a few animals (Fig. 6a,d) but optical density measurements did not reveal a consistent increase (Table 2).

Uptake of 2DG clearly increased in right subthalamic nucleus (STN) both autoradiographically (Fig. 7) and den- sitometrically (Table 1). Uptake of 2DG also increased in the internal capsule (CAI) just lateral to STN (Fig. 7).

Many regions of the midbrain were activated. The midbrain reticular formation, called the deep mesencephalic nucleus (DMN) in this study, increased 2DG uptake (Fig. 8,

Table la). In the most ventral part of DMN is a triangular collection of cells we have labeled NCU in this study and in our previous study (Sharp and Evans, '82). The dorsal portion of DMN merges with the deep layers of the superior colliculus (SC,,). Uptake of 2DG increased in NCU (Fig. 8b,c,e,f), DMN, and in the most posterior portions of SC,, (Fig. 9c,d,g,h).

Uptake of 2DG increased in substantia nigra (Table la) primarily in the central and ventral portions of the substantia nigra pars reticulata (SNr) (Fig. 9a-c,e-g). Dorsal and medial portions of SNr were not activated. The most anterior portions of SNr (Fig. 8a,d) and the most posterior portions of SNr (Fig. 9d,h) were only slightly activated. Substantia nigra pars compacta was only slightly activated (Figs. 8a,d, 9a,b,e,f).

Red nucleus pars magnocellularis (R,) increased 2DG uptake (Table la) in ventral portions of anterior R, (Fig. 8c,f) and middle R, (Fig. 9a,b,e,f). Uptake of 2DG increased in ventromedial portions of posterior R, (9c,d,g,h). The parvocellular regions of the red nucleus (Rp) did not increase 2DG uptake in anterior (Fig. 8a,b,d,e), middle (Figs. 8c,f, 9a,b,e,f), or posterior (Fig. 9c,d,g,h) portions of the nucleus.

The right nucleus tegmenti pedunculopontinus also increased 2DG uptake (Table la). The region of increased 2DG uptake occurred dorsal to the superior cerebellar pe-

Fig. 7. Uptake of (''0 2DG increased throughout the right Pf-CM complex of thalamus as well as right zona incerta (ZI), right subthalamic nucleus (STN), and rlght internal capsule (CAI).

270 F.R. SHARP

Figs. 8, 9. Right MI stimulation also increased 2DG uptake in the deep mesencephalic nucleus DMN @a-0, the ventral deep mesencephalic nucleus NCU @a-0, ventrolateral substantia nigva pars reticulata SNr (8c,f, ga-hl, magnocellular portions of the red nucleus RNm (8c,f, 9a-h), and deep layers of the posterior superior colliculus SCsgp (9c,d,g,h). The Nissl-stained section in 9e produced the (''(3 2DG autoradiograph in 9a.


Figure 9

2 72 F.R. SHARP

duncle, lateral to the central gray, and ventral to the most monosynaptic afferents to MI and SI, however, only account posterior portions of the deep layers of the superior collicu- for a few of the observed activated structures. lus (not pictured). Every animal showed a discrete increase It seems more likely that increased 2DG uptake in many of 2DG uptake in the right nucleus tegmenti pedunculopon- of the activated structures results from monosynaptic acti- tinus during forelimb MI stimulation (FLMIS). vation of MI efferents to SI, SII, ?ME, CP, R, VL, ?VM,

POm, central lateral n. thalamus (CL), Pf-CM, STN, SNr, DMN, NCU, SCsgp, RN, POM, POV, POL, reticular teg-

DISCUSSION mental n. of pons (RTP), 10, LR, and cervical spinal cord gray matter (Asanuma and Sakata, '67; Brooks and Stoney,

The region of rat neocortex electrically stimulated in this '71; Kunzle, '75, '76, '77, '78; Kuypers and Lawrence, '67; study has been termed "forelimb motor Cortex'' by Previous Phillips and Porter, '77). Regions of increased 2DG uptake investigators Woolsey et al., '50; Woolsey '58; Hall and may also result from monosynaptic activation of SI effer- Lindholm, '74). This region of neocortex, when electrically ents to MI, SII, VB, POm, Pf-CM, R, CL, CP, S C s s , ZI, stimulated, has the lowest threshold of any neocortical re- DMN-NCU, POM, lateral (POL) and ventral pontine nuclei gion for the production of forelimb movem(?nts. In Our ex- (POV), CU, and cervical spinal cord dorsal horn gray matter periments, stimulation of this region of forelimb motor (Jones and Powell, '69; Jones and Burton, '74; Kuypers and cortex" predictably produced movements of the contralat- n e r k , '64; Wise and Jones, '77a,b). Most of the efferents era1 forelimb in every animal. I t is possible that there was from MI and SI cortex are described in the cat or monkey. spread of the stimulus to nonforelimb areas of rat motor Only a few studies have described the efferents of rat MI or cortex. However, any spread was not sufficient to produce SI cortex and only a few of these have distinguished be- observable movements of any region of the body except the tween face, vibrissae, forelimb, or hindlimb regions of MI forelimb. In addition, cervical spinal cord was activated by or SI cortex (Wise and Jones, '77a,b; Donoghue et al., '79). the electrode stimulation whereas thoracic, lumbar, sacral It is apparent that most, but not all, structures activated spinal cord, and brainstem motor nuclei were not activated. are monosynaptic efferents of MI and/or SI. Retrograde Stimulation of "forelimb" motor cortex resulted in in- activation of MI and SI afferents may not play a significant creased 2DG uptake in nucleus cuneatus (cu) (see ComPan- role in increasing 2DG uptake in activated structures. This ion paper) but not in nucleus gracilis. This is compatible is based partly on observations of locus coeruleus. Locus with activation of forelimb dorsal column pathways through coeruleus projects to MI and SI, but MI and SI do not project nucleus cuneatus (Hand and Winkle, '771, whereas hind- to locus coeruleus. Electrically stimulating MI and SI should limb sensory pathways via nucleus gracilis were not acti- retrogradely activate locus coeruleus cellular perikarya. vated. In addition, the regions activated during electrical Table 2 shows that forelimb MI-SI stimulation does not stimulation of "vibrissae motor cortex" (Sharp and Evans, increase 2DG uptake in right compared to left locus coeru- '82) significantly differ from the regions activated during leus. In addition, sciatic nerve electrical stimulation only stimulation of "forelimb motor cortex" described in the slightly increases 2DG uptake in retrogradely stimulated present study. These arguments suggest that the electrode spinal cord ventral horn motor neurons (Kennedy et al., has stimulated primarily "forelimb" motor cortex. This area '75; Sharp, '76a,b). is termed motor cortex because it has the lowest threshold There are several structures that were activated by corti- for production of forelilmb motor movements, projects Mat- cal stimulation that have no known monosynaptic connec- erally to caudate-putamen, connects to cervical spinal cord tions to motor sensory neocortex, however. They include gray matter, and has reciprocal ~ ~ n n e c t i o n s with th: ven- the globus pallidus and entopeduncular nuclei. These struc- trolateral (VL) nucleus of thalamus (Donoghue et al., 79). tures must have been activated polysynaptically during MU

It is possible, however, that the bipolar electrode directly SI stimulation, or from sensory feedback from the moving stimulated portions of rat forelimb somatosensory cortex. forelimb. It is possible that all structures in this study were This seems likely since posterior portions of forelimb "mo- activated, in part, polysynaptically via motor-sensory con- tor cortex" partially overlap with forelimb "sensory cortex" nections and sensory feedback. Future experiments will be in the rat based upon electrophysiological studies (Hall and required to determine the role of sensory feedback in our Lindholm, '74). This is confirmed, in part, by horseradish present experiments. The activated pathways in this study peroxidase injections into posterior forelimb cortex that probably are similar to, but are not necessarily the Same label both the ventrolateral (motor) and ventrobasal (sen- as, pathways that would be activated during normal behav- sow) nuclei of thalamus (Donoghue et al., '79). The regions ioral movements of the left forelimb (Sharp and Evans, '82). activated by stimulation of forelimb neocortex in this study During conditioned motor movements of the forelimb in probably result from combined direct activation of forelimb monkeys, focal increases of (I4C) 2-deoxyglucose uptake MI and forelimb SI neocortex. have been detected in motor-sensory cortex, thalamus, mid-

Many regions activated can be explained on the basis of brain, pons, and cerebellum (Sharp, '76b; Schwartzman et monosynaptic activation of efferents and/or afferents Offore- al., '81; Matsunami et al., '81). In addition, focal increases limb MI or SI cortex. It is possible that Cortical Stimulation of cerebral blood flow have been detected in cerebral cortex retrogradely activated monosynaptic afferents to MI includ- of man during seizures (Hougaard et al., '76) and during ing SI, ?MII, VL, VM, CL, Pf-CM, and POm. Likewise, it is motor and sensory arm function (Roland et al., '80a,b; Or- also possible that cortical stimulation retrogradely a h - gogozo and Larsen, '79) and intended arm function (Ingvar vated monosynaptic afferents to SI including MI, SII, VB, and Risberg, '67; Orgogozo and Larsen, '79). VM, CL, and POm (Akers and Killackey, '78; Bowker and Others have previously shown that stimulation of motor Coulter, '81; Donaldson et al., '75; Donoghue et al., '79; cortex in experimental animals either with electrodes P r f e n and Clavier, '79; *n,s and Powell, '69; +neS et al., (Goldberg et al., '80; Sharp and Evans, '82) or epileptogenic 79; Klllackey and Leshln, 75; Pandya and Vlgnolo, '68, substances (Collins et al., '76; Collins, '78) results in dis-

'71; Sakai, '82; Strick '73; White and DeAmicis, '77). The crete 2DG uptake increases in most of the subcortical struc-


rat’s motor cortex or, instead, colonies of neurons with overlapping spinal cord projections. We can say that increased 2DG uptake in vibrissae and forelimb motor cortex does not occur in discrete anatomical columns nor do the borders of increased 2DG uptake have discrete edges. Pri- mates may differ since columnar projections have been described in frontal association cortex of monkeys (Gold- man-Rakic and Schwartz, ’82; Goldman and Nauta, ’77a) and “columnar” 2DG uptake has been reported in prefrontal monkey cortex during forelimb movement (Matsunami et al., ’81).

Prefrontal cortex anterior to the electrode site was activated during forelimb MI but not during vibrissae MI stimulation (Sharp and Evans, ’82). We labeled the activated region in prefrontal cortex as MII, indicating a “second motor region.” Region MI1 corresponds to the “second forelimb region” described in rat prefrontal cortex by Neafsey (Neafsey, ’80; Bold and Neafsey, ’82; Neafsey and Sievert, ’82). Stimulation of MI1 produces forelimb movements at a higher threshold than stimulation of MI but both MI and MI1 project to cervical spinal cord in the rat (Neafsey, ’80). The relationship of the region we have here labeled MI1 to the primate premotor cortex (Weinrich and Wise, ’82; Wie- sendanger, ’81; Moll and Kuypers, ’77) and primate supplementary cortex (Wise and Tanji, ’81; Brinkman and Porter, ’79; Tanji et al., ’80; Wiesendanger, ’81) is uncertain. Wein- rich and Wise (‘82), on the basis of physiological, cytoarchitectonic, and connectional similarities of the primate premotor and supplementary motor regions, are inclined to regard both as components of a frontal agranular belt of “secondary” motor cortex rostrally adjacent to the “primary” motor field MI. The region labeled MI in this and other studies in the rat (Hall and Lindholm, ’74; Woolsey, ’50, ’58) appears to be the rat analogue of primate MI. The region labeled MI1 in this study may be the rat analogue of primate premotor andor supplementary cortex but addi- tional anatomical and physiological rat data are needed. Within cat MI motor cortex, multiple representations of the forelimb have been described (Pappas and Strick, ’81) and evidence of two representations of the hand in primate area 4 cortex have been reported (Strick and Preston, ’82). Our data do not answer whether multiple representations of forelimb exist in rat MI cortex as well.

tures described here. Our studies differ in that they attempt to confine the motor movements to either vibrissae (Sharp and Evans, ’82) or forelimb (this study and companion paper). The production of facial and forelimb movements must share many common brain mechanisms since both would involve movement of a part of the body. However, there must also be many differences since different portions of the body are moving. In addition, the types and functions of the movements must be very different. Facial movements are frequently “voluntary,” not requiring “reflex” body movements when they occur. Movement of facial muscles would not ordinarily carry any inertia nor require complex body and limb adjustments to maintain balance, posture, andor locomotion. The discussion below will center on which brain structures are unique to either forelimb or facial motor function and which structures are common. If a structure is common, that is, a structure activated during both forelimb and facial movements, we will describe whether the activated regions within a structure show overlap or not during forelimb compared to facial movements. The presence or absence of such overlap within a structure suggests anatomical and functional differences between structures.

Motor cortex MI, MI1 Electrical stimulation of forelimb motor cortex activated

a region lateral and posterior to that which produced vibrissae movements (Sharp and Evans, ’82). This is consistent with electrophysiological studies showing “forelimb” motor cortex lateral and posterior to “vibrissae” motor cortex in the rat (Woolsey, ’58; Woolsey et al., ’50; Settlage et al., ’49; Hall and Lindholm, ’74). A somatotopic pattern of motor movement elicited by “motor cortex” stimulation has been described for every mammal studied (Asanuma and Ward ’71; Asanuma and Sakata, ’67; Asanuma ’75; Phillips and Porter, ’77; Anderson et al., ’75; Phillips, ’67; Penfield and Jasper ’54; Penfield and Rasmussen, ’50; Woolsey, ’58). Stimulation of forelimb motor cortex produced only contralateral forelimb movements in our experiments. This is consistent with metabolic activation of right forelimb motor cortex and little change in left MI. Vibrissae motor cortex stimulation (VMIS) frequently elicited bilateral vibrissae movements and bilateral increases of 2DG uptake in MI cortex (Sharp and Evans, ’82). These results are consistent with the anatomy of the primate where extensive homotopic callosal (commissural) connections between left and right motor cortex are restricted to face, trunk, and proximal extremity regions (Pandya and Vignolo, ’71). The motor cortex representations of the distal parts of the extremities lack or have many fewer callosal interconnec- tions (Pandya and Vignolo, ’71).

On the basis of microstimulation of motor cortex, Asan- uma and his colleagues (Asanuma, ’75) have proposed that particular movements are represented in cylindrical cortical columns. Others have proposed that for activation of individual motor neurons there is a “best point” in motor cortex. The “best point” consists of colonies of pyramidal cells that may activate a single motorneuron (Phillips and Porter, ’77). Considerable overlap exists between baboon motor cortex colonies that project to motor neuron pools of individual hand muscles (Andersen et al., ’751, which is consistent with observations that each motor neuron receives synapses from more than one corticospinal cell (Phil- lips and Porter, ’77; Phillips, ’67). Our data cannot resolve whether there are muscle-specific functional columns in the

Sensory cortex SI and SII The diffuse activation of forelimb motor cortex extended

posteriorly into a discrete, columar 2DG uptake increase in forelimb somatosensory (SI) cortex. Continuity of rat forelimb MI and SI cortex is compatible with anatomical and physiological observations of a partial overlap of posterior forelimb MI cortex with anterior forelimb SI cortex in rat (Hall and Lindholm, ’74; Donoghue et al., ’79). The complete separation of MI and SI cortical regions during vibrissae cortex-stimulated movements (Sharp and Evans, ’82) is compatible with separation of “motor” and “sensory” vibrissae cortical representations in the rat (Hall and Lindholm, ’74). Activation of forelimb SI during forelimb MI stimulation is probably due partly to direct electrode stimulation and partly to reciprocal cortical connections (Akers and Killackey, ’78; Donoghue et al., ’79; Gatter and Powell, ’78; Jones and Powell, ’69; White and DeAmicis, ’77). Sensory feedback from the moving forelimb may also activate SI since forelimb tactile stimulation increases monkey SI metabolism (Juliano et al., ’81).

274 F.R. SHARP

Forelimb MI (this study) and vibrissae MI stimulation and Sinha ('72), who describe physiological responses to (Sharp and Evans, '82) activates all layers of somatosensory vibrissae sensory stimulation only in the posteromedial SI cortex just as visual stimulation activates all layers of barrel field of SI and not in SII, whereas cortical cell re- visual cortex (Schoppmann and Stryker, '81). The column sponses to distal forelimb stimulation were found in SI and in forelimb SI extends so far anteroposteriorly that it can in SII. However, there is anatomical (White and DeAmicis, be thought of as a thin, saggital "slab." It lies posterior and '77) and physiological evidence (Welker and Sinha, '72) for dorsomedial to vibrissae SI cortex (Sharp and Evans, '821, nonvibrissae representations of face, jaw, and tongue in in accord with the proposed somatotopic organization of rat both SI and SII of mouse, rat and squirrel (Nelson et al. SI (Hall and Lindholm, '74; Welker, '71, '76; Welker and '79). In addition, the mystacial vibrissae of cat are repre- Woolsey, '75; Woolsey, '67; Woolsey and van der LOOS, '70; sented in SI and SII (Burton et al., '82). Whether the rat Woolsey et al., '75). mystacial vibrissae are represented in rat SII remains to

Multiple somatic areas for the forelimb have been de- be determined. scribed physiologically in primate SI (Woolsey, '81; Zimmer- man, '68). Our data, however, show only one long, thin, activated slab. If there is more than one forelimb representation in rat SI, the different representations are probably contiguous. It is possible that multiple forelimb representations in MI (Strick and Preston, '82) and SI (Woolsey, '81) cortex is a characteristic of primate neocortex lacking in rodents.

The bilateral SI activation during vibrissae MI stimulation (Sharp and Evans, '82) is probably due to interhemispheric MI-to-MI conduction (Pandya and Vignolo, '71) with subsequent MI-to-SI activation bilaterally. Entirely unilateral activation of forelimb SI during forelimb MI stimulation is compatible with the relative paucity of interhemispheric connections of distal forelimb MI (Pandya and Vignolo, '71). It is also compatible with previous studies of SI cortex that report either few (White and DeAmicis, '77; Yorke and Caviness, '75; Lorente de N6, '22) or no (Wise and Jones, '76; Ryugo and Killackey, '75; Akers and Kil- lackey, '78; Jacobson, '70; Jones and Powell, '69; Shanks et al., '75) interhemispheric distal forelimb SI connections. It seems reasonable that what SI interhemispheric connections do exist occur primarily between face (White and DeAmicis, '77), pharyngeal, trunk, and proximal extremity regions (Bowker and Coulter, '811, as also seem true for interhemispheric MI connections (Pandya and Vignolo, '71). Forelimb SI activation could also be due to sensory input from the contracting forelimb via inputs to SI from VB and POm (Donaldson et al., '75; Donoghue et al., '79; Hand and Morrison '70; Jones and Powell, '69; Jones and Burton, '74; Jones et al., '79; Pandya and Vignolo, '68; White and De- Amicis, '77; Wise and Jones, '77a).

The neocortex just ventral to forelimb SI, including the vibrissae barrel field and face SI cortex (Welker, '71, '761, was not activated. The activated region of forelimb SII (Welker and Sinha, '72) occurred ventral to SI and involved all layers (I through VI) of neocortex. This forelimb representation in SII occurs dorsal to the cortical gustatory area in the rat (Yamamoto et al., '80; Benjamin and Pfaffmann, '55). Forelimb SII activation could have occurred from reciprocal MI-SII and/or SI-SII connections (Akers and Kil- lackey, '78; Bowker and Coulter, '81; Gatter and Powell, '78; Jones and Powell, '69; Pandya and Vignolo, '71; White and DeAmicis, '77; Woolsey, '81) that have been described mainly in primate and cat neocortex. Activation of forelimb SII occurred only on the side ipsilateral to the motor cortex stimulation, which suggests that distal forelimb SII, like forelimb MI and SI, has few, if any, homotopic interhemispheric connections.

Forelimb motor cortex (MI) stimulation increased metabolism in discrete regions of both SI and SII. Vibrissae stimulation, on the other hand, primarily activated SI (Sharp and Evans, '82). This is consistent with the data of Welker

Caudate-putamen (CP) Dorsal lateral CP was activated during stimulation of

forelimb MI and vibrissae MI cortex (Sharp and Evans, '82). Vibrissae MI stimulation activated CP bilaterally. Fore- limb MI stimulation (FLMIS), however, primarily activated ipsilateral CP, though a small region of contralateral CP was activated. These results agree with bilateral motor cortex connections to striatum in rat, cat, rabbit, and primate (Webster, '61; Carman et al., '65; Kemp and Powell, '70; Kunzle, '75, '77, '78a,b; Kunzle and Akert, '77; Cospito and Kultas-Ilinsky, '81). Our results suggest that forelimb MI-CP connections are primarily, though not entirely, unilateral whereas vibrissae MI-CP connections are more bilateral.

Other regions that project to CP, and might activate CP, include SI, SII, CL, Pf-CM, and SN (Royce, '78a,b). SI and SII send ipsilateral projections to putamen in primate (Kun- zle, '77; Jones et al., '77) and rat (Webster, '61). Yeterian and Van Hoesen ('78) have shown that primate cortical areas that have reciprocal corticocortical connections project to overlapping regions of caudate. Since MI, SI, and SII are reciprocally connected, the activated region in dorsolateral CP could reflect combined activation of MI, SI, and SII inputs to dorsolateral CP. In fact, the activated region could represent convergence of all activated afferents to dorsolateral CP.

The patterns of CP activation differ for forelimb compared to vibrissae MI stimulation. Forelimb MI stimulation (FLMIS) activates the anterior dorsolateral CP whereas vibrissae MI stimulation (VMIS) does not (Sharp and Ev- ans, '82). Forelimb and vibrissae MI stimulation both activate the middle third of dorsolateral CP. The regions activated during FLMIS are ventral to, but may overlap, the areas activated during VMIS (Sharp and Evans, '82). FLMIS activated small separate patches or bars in the posterior third of CP. VMIS activated two separate parallel bands in posterior CP (Sharp and Evans, '82) that may overlap areas activated during FLMIS. Corticostriatal fibers end in interrupted clusters, strips, and bands, and cell groups are arranged in a similar fashion (Jones et al., '77; Goldman and Nauta, '77b).

Virtually all major cortical areas project upon caudate and putamen (Webster, '61; Carman et al., '65; Kemp and Powell, '71; Jones et al., '77; Kunzle, '771, and reciprocally connected cortical areas project upon the same region of striatum (Yeterian and Van Hoesen, '78). The above, cou- pled with our data, suggests that neocortex is composed of "systems" (prefrontal, sensory-motor, visual, auditory, lan- guage, etc.). Each cortical "system" projects to a given striatal region, and each cortical region within a cortical "system" would send partially overlapping projections to the same CP region. For example, monkey prefrontal cortex


nuclei also project to R including VL, VB, VM, and POm (Jones, '75). Jones ('75) has shown that each region of neocortex and its associated dorsal thalamic nucleus both project to the same sector of the reticular complex. This implies that if VL, VB, VM, and POm activate R, the activated regions of these nuclei probably project to anterior dorsal lateral R (Jones, '75). If VL, VB, VM, and POm project to approximately the same region of anterodorsolateral R, this region of R may be a "motor-sensory gate." It is notable that discrete portions of R are activated during FLMIS and VMIS. Scheibel and Scheibel ('66) have shown dendrites extending for considerable distances in dorsal thalamus with each cell having extensive axon collaterals. Because of this, it has been suggested that R has a nonspecific role in "gating" thalamocortical activity (Jones '75; Scheibel and Scheibel, '66). Our data together with topographic cortical and thalamic projections (Jones, '75; Carman et al., '64) suggest some specificity.

Ventrolateral (VL) nucleus of thalamus VL activation probably results from MI-VL connections

(Allen and Tsukahara, '74; Angaut, '73; Asanuma et al., '79; Catsman-Berevoets and Kuypers, '81; Donoghue and Ebner, '81; Donoghue et al., '79; Haroian et al., '81; Kunzle, '76; Rinvik and Grofova, '74; Rispal-Padel and Massion, '70; Rispal-Padel and Grangetto, '77; Rispal-Padel et al., '73; Sakai, '82; Strick, '73, '76). Forelimb MI stimulation activated central anterior VL and ventral middle and ventral posterior VL, whereas vibrissae MI stimulation activated dorsal middle and dorsal posterior VL (Sharp and Evans, '82). Rat MI-VL connections appear to be somatotopically organized (Bold and Neafsey, '821, as do primate (Kunzle, '76) and racoon (Sakai, '82). Physiological studies verify precise MI-VL projections in several species (Rispal- Padel and Massion, '70; Rispal-Padel et al., '73; Rispal- Padel and Grangetto, '77; Strick, '73).

Somatotopically organized, elongated strips of VL neurons project to MI cortex as bands (Kievit and Kuypers, '771, crescents (Strick, '76; Kunzle, '761, and concentric lamellae (Jones et al., '79). Rostrocaudally oriented strips of activated VL neurons occurred in our studies, though crescents and lamellae were not observed. The lack of crescents or lamellae may be due to combined activation of VL afferents from MI (Donoghue et al., '79; Jones and Leavitt, '74) lateral (NL) and interpositus (NT) nuclei of cerebellum (Bharos et al., '81; Chan-Palay, '77; Carter and Fibiger, '78; Faull and Carman, '78; Haroian et al., '81; Angaut, '73; Kalil, '81; Rinvik and Grofova, '74; Thach and Jones, '79; Martin et al., '74; Donoghue and Ebner, '81a,b), posterior entopeduncular (EPN) nucleus (Carter and Fibiger, '78; Fi- lion and Harnois, '78; Larsen and McBride, '79: Mehler and Nauta, '74; Nauta, '79; Van der Kooy and Carter, '81), and the reticular (R) nucleus of thalamus (Jones, '75). Cerebel- lar afferents to rat VL terminate throughout VL (Faull and Mehler, '76; Carter and Fibiger, '78; Donoghue et al., '79). Dentate, interpositus, and fastigial nuclei send topographic projections to VL in cat and rat (Angaut, '73; Chan-Palay, '77). Entopeduncular (EPN) afferents terminate in ventral VL, a region termed VAL, or the ventroanterolateral nucleus by Carter and Fibiger ('78). The distribution of reticular (R) nucleus afferents to VL is unknown, but they probably project throughout the nucleus (Scheibel and Scheibel, '66; Jones, '75). Vibrissae MI stimulation activated dorsal VL much more than ventral VL (Sharp and Evans, '82). However, forelimb MI stimulation activated

projects to caudate (Goldman and Nauta, '77b), and the rat prefrontal system projects to dorsomedial CP (Divac and Diemer, '80). Monkey motor-sensory cortex projects to putamen (Kunzle, '77; Jones et al., '77), and the rat motor- sensory system projects to dorsolateral CP (this study; Sharp and Evans, '82).

Globus pallidus (GP) Central GP is activated during forelimb MI stimulation

in contrast to dorsal GP activation during vibrissae MI stimulation (Sharp and Evans, '82). This is consistent with topographic striatopallidal connections in monkey (Szabo, '72) and rat (Brann and Emson, '80). However, neurophy- siological experiments have shown that the limbs are dorsal to face within monkey GP (De Long, '71). GP is polysynaptically activated since there are no known monosynaptic connections between GP and either MI or SI. GP activation could occur via caudate-putamen (Fox and Ra- fols, '75; Cowan and Powell, '66; Fox et al., '75; Szabo, '72; Kemp and Powell, '71; Brann and Emson, '80; Mehler and Nauta, '741, deep mesencephalic (DMN) nucleus (Edwards and deOlmos, '76; Veazey and Severin, '80a,b), and subthalamic (STN) nucleus inputs (Deniau et al., '78; Nauta and Cole, '78; Van der Kooy and Hattori, '80; Carpenter et al., '81). Tactile somatosensory input to GP from CP might also activate GP, since many GP units respond to sensory stimulation (Schneider et al., '82; Lidsky et al., '75). Striatopal- lidal fibers are poorly myelinated (Fox et al., '75) collaterals of the axons passing to the substantia nigra (Fox and Ra- fols, '75; Fox et al., '751, and may be y-aminobutyric acid (GABA)ergic (Nagy et al., '78). Deep mesencephalic nucleus (DMN) input to GP may be cholinergic (Hoover and Jaco- bowitz, '79). The neurotransmitter of the STN to GP pathway is unknown. CP, DMN, and STN all receive monosynaptic inputs from MI (Carman et al., '65; Veazey and Severin, '82; Kitai and Deniau, '81). GP outputs include STN, EPN, SN, CP, and R (Nauta, '79).

Reticular nucleus (R) thalamus Reticular (R) nucleus activation could have occurred from

MI-R (Carman et al., '64; Jones, '751, SI-R, and/or SII-R connections (Jones, '75). A precise topographical arrangement of corticoreticular connections has been described (Carman et al., '64; Jones, '75). Regions of reciprocally connected cortex may project to the same or overlapping regions of R. Both forelimb (FLMIS) and vibrissae MI stimulation (VMIS) activate anterior dorsolateral reticular nucleus (Sharp and Evans, '82). The regions of R activated during VMIS occur slightly anterior to those regions activated during FLMIS, though extensive overlap occurs. Re- ticular neurons may be GABA-containing inhibitory neurons (Ben-Ari et al., '76; Houser et al., '80) that "gate" activity in thalamocortical relay cells (Rapasardi et al., '74; Yingling and Skinner, '76) and play a role in selective attention (Schlag and Waszak, '71; Skinner and Yingling, '76). Our data suggest there is not a "face" or "forelimb" gate. Since the same region of R is activated during FLMIS and VMIS, this region may serve as a "motor gate" independent of which body part is moving (Dingledine and Kelly, '77).

The concept of a "motor-sensory" gate is supported by the subcortical afferents to R. The parafascicular (pf, and cen- trolateral (CL) nuclei of thalamus (Jones, '75) and the deep mesencephalic nucleus (Edwards and deOlmos, '76; Veazey and Severin, '80a,b) project to R. Most dorsal thalamic

276 F.R. SHARP

ventral VL much more than dorsal VL. This suggests that EPN inputs to VL could have a much more direct effect on forelimb than vibrissae VL function since EPN projects to ventral VL. In anesthetized cat physiological experiments, 14% of VL neurons respond to EPN stimulation, whereas 30% respond to motor cortex stimulation and 30% respond to cerebellar stimulation (Rivner and Sutin, '81).

Ventrobasal (VB) nucleus of thalamus Forelimb MI stimulation (FLMIS) activated large regions

of the ventrobasal nucleus (VB) of thalamus. VB activation may be due to direct SI stimulation of SI-VB reciprocal connections (Saporta and Kruger, '77; Jones and Burton, '74; Killackey, '73; Donoghue et al., '79; Hand and Morri- son, '70; Jones et al., '79; Killackey and Leshin, '75; Kunzle, '77; Donaldson et al., '75; Wise, '75; Donoghue and Ebner, '81a,b; Friedman and Jones, '81). Somatosensory input from the moving forelimb could also activate VB. The forelimb movements would stimulate "deep" and "cutaneous" recep- tors that relay to VB in part via the cuneate nucleus (Fried- man and Jones, '81; Lund and Webster, '67; Hand and Winkle, '77; Jones and Burton, '74).

FLMIS activated the ventral two-thirds of anterior VB, the ventral one-third of middle VB, and a ventral curvilin- ear region that becomes smaller and smaller and disap- pears in posterior VB. This pattern is similar to the distribution of labeled cells after forelimb SI cortical HRP injections (Saporta and Kruger, '77). This agrees with physiological observations of rat VB as well (Angel and Clarke, '73; Davidson, '65; Emmers, '65; Waite, '73).

The region activated involves a larger volume of VB than previously reported in anatomical and physiological studies (Saporta and Kruger, '77; Emmers, '65; Angel and Clarke, '75). This could be due to movements of proximal and distal forelimb muscles. In some experiments, smaller forelimb MI regions were activated and restricted VB regions were activated in patterns remarkably similar to Figure 17B from Saporta and Kruger ('77). The activated region of VB does not represent face or hindlimb since no movements of these regions occurred. Also, vibrissae MI stimulation (VMIS) does not activate VB (Sharp and Evans, '82). Pro- prioceptive input from moving vibrissae during VMIS may not be relayed to VB, whereas cutaneous input from objects touching the vibrissae probably is relayed to VB (Sharp and Evans, '82; Saporta and Kruger, '77). S1, SII, reticular nucleus, and cuneate project to VB and may activate the large volume of VB in this study (Jones and Burton, '74; Jones, '75; Saporta and Kruger, '77; Emmers, '65; Hand and Mor- rison, '70; Hand and Winkle, '77; Spreafico et al., '81). The lateral cervical nucleus also sends inputs to VB (Boivie, '80). Recently Spreafico et al. ('81) described a central core

sumably in part via spinothalamic tract fibers (Jones and Burton, '74; Boivie, '71, '79). The VB-VL transition zone also receives vestibular afferents (Kotchabhakdi et al., '80) as well as medial lemniscus and cervicothalamic tract afferents (Boivie, '71a,b, '78, '79, '80). The VB-VL transition zone projects to SI and SII in cat (Spreafico et al., '81) and at least to SI in primate (Strick, '73; Pearson and Haines, '80). The VB-VL transition zone appears to relay "deep receptor" input to cortex.

Posteromedial (POm) nucleus of thalamus The posteromedial nucleus of rat thalamus (POm) is dor-

sal to posterior VB, ventral to LP, and lateral to the intralaminar nuclei CM-Pf or CL. White and DeAmicis ('77) have suggested that parts of monkey PO and POm, portions of cat PO and POm, rat POm, and mouse PO are homolo- gous (DeVito and Simmons, '76; Jones and Leavitt, '74; Jones '71). Forelimb (FLMIS) and vibrissae (VMIS) MI stimulation activates ipsilateral POm (Sharp and Evans, '82). FLMIS activates a region of POm medial to that activated during VMIS (Sharp and Evans, '82). Rat POm may be somatotopically organized with face lateral to forelimb. However, there is not a somatopic arrangement of monkey spinothalamic afferents to POm (Boivie, '79).

POm activation probably occurred via MI-POm connections (Donoghue et al., '79; Sharp, unpublished observations). MI-POm connections have not been described in cat or primate, but would be of great interest as a possible source of short-latency somatosensory input to primate motor cortex. POm also has reciprocal connections with SI in rat (Donoghue et al., '79; Wise and Jones, '771, mouse (White and DeAmicis, '77), cat, and monkey (DeVito and Simmons, '76; Jones and Burton, '74; Spreafico et al., '81). POm also has reciprocal connections with SII in cat (Spreafico et al., '81). It is possible, though unproven, that POm has reciprocal connections with MI, SI, and SII in rat. POm receives afferents from spinothalamic tract (Lund and Webster, '67; Lund, '67; Jones and Burton, '74; DeVito and Simmons, '76; Boivie, '71a,b, '79), dorsal column nuclei (Devito and Sim- mons, '76; Boivie, '71a,b, '78; Jones and Burton, '74), and the lateral cervical nucleus (Boivie, '80). POm receives convergent sensory inputs from most sensory pathways including spinothalamic, medial lemniscal, and cervicothalamic. In turn, POm projects widely on motor and sensory neocortex. Cells within POm respond to light touch and noxious stimuli (Poggio and Mountcastle, '60; Curry, '72; Guilbaud et al., '77).

Centre median (CM) and parafascicular (PO nuclear complex of thalamus

of cat VPLm- that projects to SI, an inner shell of VPL that Forelimb MI stimulation (FLMIS) and vibrissae MI stim- projects to SI and SII, and an outer shell outside VPL that ulation (VMIS) both activated the CM-Pf complex (Sharp has divergent cortical connections. If a similar organization and Evans, '82). The CM-Pf regions completely overlap. holds for rat VB, FLMIS may activate the central core and There is not a somatotopic organization of CM-Pf for face inner shell of VB in our studies. The central core would compared to forelimb movements. project to SI and the inner shell to SI and SII. FLMIS may The region we labeled CM-Pf here was called the parafas- also activate the outer shell, which includes POm and the cicular nucleus (FTJ in our previous study (Sharp and Evans, VB-VL transition zone (Spreafico et al., '81). The VB-VL '82) and is called Pf by most authors (Jones and Leavitt, transition zone was described in the cat and monkey by '74; Carter and Fibiger, '78; Bentivoglio et al., '81; Comans Boivie ('71a,b, '79) as the target of spinothalamic tract and Snow, '81; Donoghue et al., '79; Herkenham, '80; Van fibers. Though this VB-VL transition zone has not been der Kooy, '79). We have called this region CM-Pf because of described in rat, a continuous zone of increased 2DG uptake anatomical comparisons with cat and monkey. Monkey CM runs from lateral VB to medial VL and would include this and Pf (Kunzle, '75, '76, '77; Strick, '75), and rat Pf have VB-VL transition region. Forelimb Group I afferents (Ro- reciprocal connections with motor cortex (Herkenham, '80; sen, '69) activate cells in the VB-VL transition zone, pre- Bentivoglio et al., '81). In monkey, Pf and CM are separate


nuclei, probably with different connections. Pf is rostrome- dial and CM is ventrolateral (Jones and Leavitt, '74).

CM-Pf activation probably occurred via MI afferents (Her- kenham, '80; Bentivoglio et al., '81). Other afferents that might activate CM-Pf include entopeduncular nucleus (EPN; Carter and Fibiger, '78; Van der Kooy and Carter, '811, deep mesencephalic nucleus (DMN; Edwards and De Olmos, '76; Veazey and Severin, '80a,b), lateral nucleus (NL) of cerebellum (Bharos et al., '81; Chan-Palay, '77; Faull and Carman, '78; Haroian et al., '81j, deep layers of the superior colliculus (SCsgp), substantia nigra pars reticulata (SNr; Beckstead et al., '79; Clavier et al., '76; Faull and Mehler, '78), and laminae VI to VIII of the cervical spinal-cord (Comans and Snow, '81; Lund and Webster, '67; Jones and Burton, '74; Boivie, '79). EPN, DMN, NL, SCsgp, SNr, and spinal cord were activated during FLMIS.

CM-Pf projects heavily upon caudate-putamen (CP; Cowan and Powell, '55; Jones and Leavitt, '74). FLMIS activates dorsolateral CM-Pf and dorsolateral CP; and dorsolateral CM-Pf projects to dorsolateral CP (Van der Kooy, '79). CM- Pf also projects diffusely to motor, premotor, and prefrontal cortex (Herkenham, '80; Jones and Leavitt, '74; Bentivoglio et al., '81) and to SNr and STN (Gerfen et al., '82). We cannot state whether other intralaminar nuclei including the central lateral (CL), paracentral (Pc), and central medial (Ce) nuclei were activated because of the limited reso- lution of the method.

Entopeduncular nucleus (EPN) FLMIS and VMIS activate the posterior one-half of EPN

(Sharp and Evans, '82). Therefore, EPN is not somatotopically divided into forelimb and face regions. EPN may be the rodent and cat homologue of the medial segment of primate globus pallidus (Fox and Schmitz, '44; Fox and Rafols, '75). EPN must be polysynaptically activated since neither forelimb MI nor SI connects monosynaptically to EPN. EPN afferents include caudate-putamen (Nagy et al., '78; Van der Kooy and Carter, 'Sl), possibly the external segment (GPe) of the globus pallidus (Carter and Fibiger, '78; Deniau et al., '78; Nauta, '79), subthalamic nucleus (Carpenter et al., '81a,b; Carpenter and Strominger, '67; Nauta and Cole, '78), and deep mesencephalic nucleus-nucleus cuneiformis (Edwards and De Olmos, '76; Veazey and Severin, '80a,b). EPN projects to VA-VL, lateral VM, CM- Pf, and DMN-NCU (Carter and Fibiger, '78; Filion and Harnois, '78; Herkenham, '80; Larsen and McBride, '79; Nauta, '79; Van der Kooy and Carter, '81; Veazey and Severin, '82; Parent and DeBellefeuille, '82). The rostra1 one-half of EPN projects to lateral habenula (HL) and nucleus tegmenti pedunculopontis (NTP) (Carter and Fibiger, '78; Van der Kooy and Carter, '81). Rostra1 EPN and HL are not activated during FLMIS or VMIS.

That EPN may not be somatotopically organized is sur- prising. There is a somatotopic organization of primate motor corticoputamen projections and putamen neural activity (Kiinzle, '75; Crutcher and Delong, '82). Since CP and external segment of globus pallidus (GPe) are somatotopically organized, it would seem parsimonious to predict that CP and GPe afferents to EPN might be somatotopically organized. It is possible that there is a somatotopic arrangement of afferents to different portions of individual EPN cells, or to different EPN cells that are immediately adjacent to one another. If this were so, then the same regions of EPN would appear to be activated during FLMIS compared to VMIS, but the neural output from different EPN cells might be much different. In addition, if there were a

significant somatotopy within EPN this might be obscured in part by the small size and few cells in rat EPN. This question could be more easily settled in the primate. No evidence for somatotopic or topographic distribution of posterior EPN efferents has been found in the cat, however (Larsen and McBride, '79). In the rat it has been suggested that individual neurons in the posterior one-third of EPN send axon collaterals to VA-VL, the CM-Pf complex and to the tegmenti pedunculopontinus area of the brainstem (Van der Kooy and Carter, '81). The lack of somatotopy within EPN, and the fact that EPN neurons send divergent collaterals to many areas, suggests that outflow information from EPN may not deal with a given body part that is moving or with a given sensory input. EPN may only signal that an event is occurring or "modulate" such an event. GABA may be the neurotransmitter of EPN neurons (Pen- ney and Young, '81). Medial pallidal cells are tonically active (Georgopoulous and DeLong, '78) and inhibit VL (Uno and Yoshida, '75). In some ways the reticular nuclei of thalamus (R) and entopeduncular (EPN) nucleus are similar. Both may be GABA-containing nuclei that are not somatotopically organized and inhibit thalamus but that differ primarily in their inputs. R inputs come from thalamus, cortex, and reticular formation. EPN inputs come from basal ganglia and also reticular formation (Veazey and Severin, '80a,b). Activation of R or EPN would inhibit thalamus.

Subthalamic nucleus (STN) Forelimb MI stimulation (FLMIS) activated ipsilateral

STN, whereas VMIS activated STN bilaterally (Sharp and Evans, '82). Experimental lesions of STN in monkey result in contralateral hemiballismus of the forelimb and hindlimb (Carpenter, '76) whereas little comment is made as to whether face movements occur. A topographic organization within monkey STN has been suggested (Carpenter et al., '81a,b), and cortical projections to STN are somatotopically organized (Hartmann-Von Monakow et al., '78). Our data are not detailed enough to determine whether rat STN is somatopically organized.

STN activation probably occurred via MI-STN connections (Hartmann-Von Monakow et al., '78; Kitai and Den- iau, '81; Kiinzle, '78a; Ricardo, '80; Romansky et al., '79) that are excitatory (Kitai and Deniau, '81) and may be reciprocal (Jackson and Crossman, '81). Other STN inputs include deep mesencephalic nucleus (Veazey and Severin, '80a,b), globus pallidus (Carpenter et al., '81a,b; Carpenter, '76; Kemp and Powell, '71; Nauta, '79; Van der Kooy and Hattori; '80; Van der Kooy et al., '811, the CM-Pf complex, and the pedunculopontine nucleus (Gerfen et al., '82). STN efferents include GP, EPN, and SNr (Carpenter et al., '81a,b; Ricardo, '80; Nauta and Cole, '78; Van der Kooy and Hat- tori, '80; Carpenter and Strominger, '67; Jackson and Cross- man, '81; Mehler and Nauta, '741, perhaps via single STN cell axon collaterals (Deniau et al., '78; Van der Kooy and Hattori, '80). Other STN efferents include nucleus tegmenti pedunculopontinus and cerebral cortex (Jackson and Cross- man, '81). STN output cells are inhibitory (Larsen and Sutin, '78) but their transmitter is unknown.

Zona incerta (ZI) ZI was activated in some animals. There is no suggestion

of a somatotopic organization within ZI when FLMIS- and VMIS-activated regions are compared. Afferents which might activate ZI include MI and SI cortex (Kiinzle, '77,

278 F.R. SHARP

'78a,b; Kunzle and Akert, '771, NL and NI (Faull and Car- man, '78; Chan-Palay, '77), CU (Hand and Van Winkle, '771, spinal cord (Ricardo, '811, SCsgp (Graham, '771, DMN (Edwards and de Olmos, '76), as well as other regions (Ri- cardo, '81). ZI efferents include DMN, RTP, pontine nuclei. 10, SCsgp, RNp, spinal cord, CM-Pf, CL, VM, EPN, and GP (Ricardo, '81).

Substantia nigra pars reticulata (SNr) FLMIS activated the caudal one-half of ventrolateral SNr

whereas VMIS activated the rostral one-half of ventrolateral SNr (Sharp and Evans, '82). Though a somatotopic organization within SNr or SNc has not been previously suggested, many authors have demonstrated a topographic organization of SN afferents and efferents (Gerfen et al., '82; Beckstead et al., '79; Bentivoglio et al., '79; Bunney and Aghajanian, '76; Carpenter et al., '76; Clavier et al., '76; Faull and Mehler, '78; Graybiel, '78; Hopkins and Nies- sen, '76; Nagy et al., '78; Rinvik et al., '76; Grofova, '79; Mehler and Nauta, '74). Direct cortex to SN connections have been suggested by several authors (Rinvik, '66; Gerfen et al., '82; Bunney and Aghajanian, '76; Grofova, '79; Kiin- zle, '78a,b; Van der Kooy and Hattori, '80) and might activate SNr. Other afferents that could activate SNr include CP, GP, STN, and CM-Pf (Bunney and Aghajanian, '76; Hattori et al., '75; Nagy et al., '78; Gerfen et al., '82). SNr projects to CP, GP, STN, VM, CM-Pf, DMN, and SCsgp (Beckstead et al., '79 ; Beckstead, '79; Bentivoglio et al., '79; Faull and Mehler, '78; Graybiel, '78; Mehler and Nauta, '74; Carpenter et al., '76; Rinvik et al., '76). Single SNr cells send axon collaterals to VM and SCsgp (Bentivoglio et al., '79). The ventrolateral most layers of SNr were activated. Cells within SN have been divided into three dorso- ventral layers based upon dendritic fields (Grofova et al., '82). The dorsalmost layer is SNc, and the ventralmost layer contains dendrites of cells situated in all three layers. The dorsal part of CP projects to ventral SNr (Tulloch et al., '78; Nauta et al., '78), and lateral SNr projects to lateral VM (Herkenham, '79) and lateral CP (Van der Kooy, '79). FLMIS activates dorsolateral CP, ventrolateral SNr, and lateral VM. Nigrotectal and nigrostriatal cells are espe- cially abundant in ventral portions of rat SNr (Faull and Mehler, '78; Bentivoglio et al., '79; Beckstead et al., '81) whereas nigrothalamic cells are either distributed throughout SNr or located in the dorsal portions of SNr (Faull and Mehler, '78; Bentivoglio et al., '79; Grofova et al., '82).

FLMIS activated the posterior half of lateral SNc and VMIS activated the anterior half of lateral SNc (Sharp and Evans, '82). This suggests possible somatotopy within SNc. SNc is a dopamine-containing cell group (Dahlstrom and Fuxe, '64) that projects to CP and receives afferents from GP (Hattori et al., '75) and other regions (Bunny and Agha- janian, '76).

Red nucleus (RN) pars magnocellularis (Rm) Forelimb MI stimulation (FLMIS) activated ventral mid-

dle Rm and medial posterior Rm. VMIS activated rostral, dorsal parvocellular (Rp) red nucleus (Sharp and Evans, '82). These results suggest that the rat RN somatotopic organization is similar to cat and monkey (Larsen and Yumiya, '80; Kohlerman et al., '82; Humphrey and Rietz, '76; Kuypers and Lawrence, '67; Massion, '67; Brown, '74; Caughell and Flumerfelt, '77; Edwards, '72; Flumerfelt et al., '73; Gwyn and Flumerfelt, '74; Miller and Strominger,

Castiglioni et al., ,'78; Pompeiano and Brodal, '57). Face is represented rostrodorsally in monkey, cat, and rat RN, and forelimb is represented medially in caudal RN (Larsen and Yumiya, '80; Ghez, '75; Pompeiano and Brodal, '57). MI-Rm connections probably activate Rm. Corticorubral fibers are somatotopically organized in cat and monkey (Rinvik and Walberg, '63; Pompeiano and Brodal, '57; Kuypers and Lawrence, '67; Hartmann-von Monakow et al., '79) and probably in rat (present study; Brown, '74). Cortical inputs to RN are excitatory (Tsukuhara and Kosaka, '681, the neurotransmitter being unknown. Corticorubral fibers are not collaterals of corticospinal fibers (Humphrey and Rietz, '76). The lateral (NL) and interpositus (NI) nuclei of cerebellum project to RN (Caughell and Flumerfelt, '77; Flu- merfelt et al., '73; Chan-Palay, '77; Gwyn and Flumerfelt, '74). NI stimulation excites RN neurons (Toyama et al., '70). RN projects to spinal cord, lateral reticular nucleus (LR), inferior olive (101, cuneate (CU) and external cuneate nuclei, facial nucleus, certain vestibular nuclei, and interpositus nucleus (NI) and lateral nucleus (NL) of cerebellum (Allen and Tsukahara, .'74; Anderson, '71; Berkley and Wor- den, '78; Bloedel, '73; Brodal, '81; Chan-Palay, '77; Cour- ville, '66; Courville and Otabe, '74; Conde and Conde, '82; Edwards, '72; Evarts and Thach, '69; Ghez, '75; Kuypers and Lawrence, '67; Larsen and Yumiya, '80; Martin et al., '74; Massion, '67; Miller and Strominger, '73; Nyberg-Han- sen and Brodal, '64; Padel et al., '73; Padel and Jeneskog, '81; Pompeiano and Brodal, '57; Rinvik and Walberg, '63; Tolbert et al., '78; Tsukahara and Bando, '70; Walberg, '56; Walberg and Nordby, '81). Spinal cord, LR, 10, CU, NI, and NL were activated during FLMIS.

Deep layers of superior colliculus (SCsgp) MI and SI connections to SCsgp probably activated pos-

terior SCsgp during FLMIS and anterior and middle SCsgp during VMIS (Wise and Jones, '77; Kuypers and Lawrence, '67; Garey et al., '68; Price and Webster, '72; Goldman and Nauta, '76; Kunzle, '78a,b; Kassel, '82). Face SI cortex projects to rostral SCsgp (Wise and Jones, '77; Kassel, '82). The tectospinal projection to the cervical enlargement (lower cervical segments) arises from the caudolateral quadrant of the SCsgp, whereas the tectal projection to rostral cord and medulla orginates from rostral parts of SCsgp (Murray and Coulter, '82). A somatotopic arrangement of face and forelimb within SCsgp is also supported by stimulation of rostral and middle SCsgp that elicits pinna and face movements and stimulation of caudal SCsgp that elicits limb movements (Stryker and Schiller, '75; Roucoux et al., '80; Stein et al., '80; Schiller and Stryker, '72). Other inputs that might activate SCsgp include prefrontal cortex (Gold- man and Nauta, '76), sensory cortex (Kuypers and Law- rence, '67; Garey et al., '68; Price and Webster, '72), spinal cord (Antonetty and Webster, '751, pretectal region (Ber- man, '77), lateral and interpositus nuclei of cerebellum (Chan-Palay, '77; Edwards et al., '79; Roldad and Reinoso- Suarez, %1), substantia nigra (Edwards et al., '79; Graybiel, '78; Hopkins and Niessen, '76; Rinvik et al., ' 76 Fadl and Mehler, '76; Beckstead et al., '79; Dichiara et al., '79; Rin- vik et al., '76), ventromedial nucleus of thalamus (Herken- ham, '79), deep mesencephalic nucleus-nucleus cuneiformis (Edwards and deOlmos, '76; Veazey and Severin, '80a,b), zona incerta (Ricardo, '811, dorsal column nuclei (Blomquist et al., '78), reticular nucleus of thalamus, reticular tegmental uontine nucleus. and other structures (Brodal, '81; Ed-

'73; Padel et al., '73; Toyama et al., '70; Anderson, '71; wa&setal., '79). '


SCsgp may play a multimodal, sensory-motor role in the initiation or control of saccadic eye movements, head and neck movements, ear pinna movements, and vibrissae movements related to visual function (Ingle and Sprague, '75; Mohler and Wurtz, '77; Rhoades, '81; Stein et al., '76; Drager and Hubel, '76; Edwards and Henkel, '78; Killackey and Erzurumlu, '81; Stryker and Schiller, '75; Roucoux et al., '80; Schiller and Stryker, '72; Anderson et al., '71; Sprague and Meikle, '65; Stein et al.,, '76, '80; Sharp and Evans, '82). SCsgp efferents include spinal cord, 10, pontine nuclei, DMN, R, intralaminar nuclei, SNr, and VM (Henkel and Edwards, '78; Herkenham, '79; Kawamura et al., '74; Kawamura and Tsutomu, '78; Burne et al., '81; Kassel, '82; Ingle and Sprague, '75; Frankfurter et al., '76; Nagata and Kruger, '79; Veazey and Severin, '82; Walberg, '74; Weber et al., '78; Saint-Cyr and Courville, '82).

Deep mesencephalic nucleus 0MN)-nucleus cuneiformis (NCU)

FLMIS and VMIS both activate mesencephalic reticular formation (Sharp and Evans, '82). This region is termed the mesencephalic tegmentum (Anderson et al., '72; Johnson and Clemente, '59), mesencephalic reticular formation (Fu- kushima et al., '81; Mulas et al., '81; Catsman-Berrevoets and Kuypers, '811, nucleus cuneiformis (NCU), and subcu- neiformis (Edwards, '75; Edwards and deOlmos, '761, deep mesencephalic nucleus (Veazey and Severin, '80a,b, '82; Huber et al., '43), and mesencephalic locomotor region (Shik and Orlovsky, '76; Grillner and Shik, '73; Severin et al., '67). Most authors do not use the above terms synony- mousIy. Most authors do agree that midbrain reticular formation is ventral to inferior colliculus and superior colliculus. In the present and previous study we used the term deep mesencephalic nucleus (DMN) to describe that portion of the mesencephalic reticular formation bounded by the superior colliculus dorsally, substantia nigra ventrally, medial geniculate laterally, and red nucleus and periaqueductal gray medially. This terminology is in accord with Veazey and Severin ('80a,b, '821, who described the connections of this region.

Forelimb MI stimulation (FLMIS) and vibrissae MI stimulation (VMIS) activate rostral deep mesencephalic nucleus (DMN) (Sharp and Evans, '82). The DMN regions activated during FLMIS, compared to those activated during VMIS (Sharp and Evans, '82), overlap extensively. DMN is not somatotopically organized. A triangular region of ventral deep mesencephalic nucleus was activated during FLMIS and VMIS, which we labeled NCU in our present and previous study (Sharp and Evans, '82). We unfortunately named this region the nucleus cuneiformis previously (Sharp and Evans, '82). Various authors have used the term nucleus cuneiformis to describe the entire mesencephalic reticular formation (Valverde, '621, dorsal mesencephalic reticular formation (Edwards, '75; Edwards and deOlmos, '76), or the mesencephalic locomotor region in the cat (Shik and Orlovsky, '76). It might be best to use the term "nucleus cuneiformis" to describe the small region, as outlined by Berman ('68) in the cat, that lies just lateral and ventral to inferior colliculus. The region we have labeled NCU appears to correspond best to the most posterior portions of the anterior pretectal nucleus as described by Scalia ('72) and Bucher and Nauta ('54). Using the term pretectal nucleus also seems a poor choice since this region receives no retinal afferents in the rat (Scalia, '721, and the region is situated very ventrally in mesencephalic reticular forma-

tion. Because of these considerations, we have named NCU the "ventral deep mesencephalic nucleus." The ventral deep mesencephalic nucleus (NCU) has a cytoarchitectonic cor- relate (labeled NCU, Sharp and Evans, '82). It is easily distinguished on (14C) 2-deoxyglucose autoradiographs, being situated medial to the medial geniculate, dorsal to red nucleus, lateral to central gray, and running in ventral mesencephalic reticular formation from middle superior colliculus to rostral superior colliculus. The ventral deep mesencephalic nucleus (NCU) is activated during FLMIS and VMIS and could correspond to the cat mesencephalic locomotor region in rostroventral mesencephalic reticular formation (Shik and Orlovsky, '76). Veazey and Severin ('80a,b, '82) did not find any difference of dorsal and ventral DMN connections but did describe differences for medial and lateral DMN.

Primary motor (MI) and sensory (SI) cortex project to DMN and NCU (Veazey and Severin, '82; Brown, '74; Ka- wamura and Tsutomu, '78; Catsman-Berrevoets and Kuy- pers, '81). Many of the corticomesencephalic fibers appear to be collaterals of corticospinal neurons (Catsman-Berre- voets and Kuypers, '81). Other afferents to DMN that may activate DMN-NCU include EPN, SNr, SCsgp, ZI, NI, NL, DMN, and perhaps spinal cord (Veazey and Severin, '82; Catsman-Berrevoets and Kuypers, '81; Menetrey et al., '82). DMN efferents include STN, ZI, EPN, GP, LD and LP, and perhaps MD (Veazey and Severin, '80a,b). Lateral DMN projects to STN, GP, EPN, and contralateral DMN (Veazey and Severin, '80a,b).

DMN should be considered a n integral part of motor- sensory pathways. Stimulation of DMN may produce locomotion in cats and monkeys (Griilner and Shik, '73; Shik and Orlovsky, '76; Severin et al., '67; Eidelberg et al., '81). DMN and SCsgp appear to play a role in turning behavior elicited from SNr (Imperato et al., '81; Mulas et al., '81). Lastly, FLMIS and VMIS both actcivate DMN.

Nucleus tegmenti pedunculopontinus (NTPP) How FLMIS activated ipsilateral NTPP is uncertain since

NTPP connections have not been systematically studied. NTPP does receive afferents from entopeduncular nucleus (medial pallidal segment), subthalamic nucleus, and substantia nigra (Nauta and Cole, '78; Kim et al., '76; Nauta and Mehler, '66; Beckstead et al., '79). NTPP did not appear to be activated during VMIS (Sharp and Evans, '82).

ACKNOWLEDGMENTS This research was supported by a Basil O'Connor starter

research grant from the March of Dimes Birth Defects Foundation and by a grant from the Easter Seals Research Foundation. Frank Sharp is the recipient of a Teacher- Investigator Development Award, NS00584, from the NIW NINCDS.

I gratefully acknowledge Ms. Kathleen Evans for superb technical assistance and Mrs. Dorie Kehew for typing the manuscript. Many thanks to Patty Koutz, Angie Preston, and Kenneth Cluff for their donated time on this project.

NOTE ADDED IN PROOFS It has recently been shown that the cat anterior pretectal

nucleus (labeled NCU in this study) sends efferents to the pontine nuclei and inferior olive, and receives afferents from the dorsal column nuclei (cu) (Bull, M.S., J.G. May, R. J. Budell, and K. J. Berkley (1983). Intricate relations result between the dorsal column nuclei, pretectum, infe-

280 F.R. SHARP

rior olive, pons, and cerebellum in the cat. Neurosci. (Ab- stracts. 92368).

LITERATURE CITED Akers, R.M., and H.P. Killackey (1978) Organization of cortico-cortical con-

nections in the parietal cortex of the rat J. Comp. Neurol. 181:513-538. Allen, G.I., and N. Tsukahara (1974) Cerebro-cerebellar communication

systems. Physiol. Rev. 54:957-1006. Andersen, P., P.S. Hagan, C.G. Phillips, and T.P.S. Powell (1975) Mapping

by microstimulation of overlapping projections from area 4 to motor units of the baboon’s hand. Proc. R. Soc. Lond. [Biol.] 188:31-60.

Anderson, M.E. (1971) Cerebellar and cerebral inputs to physiologically identified efferent cell groups in the red nucleus of the cat. Brain Res. 30:49-66.

Anderson, M.E., M. Yoshida, and V.J. Wilson (1971) Influence ofthe superior colliculus on cat neck motoneurons. J. Neurophysiol. 34:898-907.

Anderson, M.E., M. Yoshida, and V.J. Wilson (1972) Tectal and tegmental influences on cat forelimb and hindlimb motoneurons. J Neurophysiol. 35:462-470.

Angaut, P. (1973) Bases anatomofonctionelles des interrelations cerebello- cerebrales. J. Physiol. (Paris) 67:53A-l16A.

Angel, A., and K.A. Clarke (1975) An analysis of the representation of the forelimb in the ventro-basal thalamic complex of the albino rat. J. Physiol. (Lond.) 249:399-424.

Antonetty, C.M., and K.E. Webster (1975) The organization of the spinotec- tal projection. An experimental study in the rat. J. Comp. Neurol. 163.449-466.

Asanuma, H. (1975) Recent developments in the study of the columnar arrangement of neurons within the motor cortex. Physiol. Rev. 55:143- 156.

Asanuma, H.J., and J.E. Ward (1971) Patterns of contraction of distal forelimb muscles produced by intracortical stimulation in cats. Brain Res. 27:97-109.

Asanuma. H.. K.D. Larsen. and Y. Yumiva (1979) Receotive fields of thalamic neurons projecting to the motor cortex in tce cat. Brain Res. 172-217-218,

Asanuma, H., and H. Sakata (1967) Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J. Neu- rophysiol. 30:34-54.

Beckstead, R.M., V.B. Domesick, and W.J.H. Nauta (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175:191-217.

Beckstead, R.M. (1979) Convergent prefrontal and nigral projections to the striatum of the rat. Neurosci. Lett. 1259-64.

Ben-Ari, Y., R. Dingledine, I. Kanazawa, and J.S. Kelly 11976) Inhibitory effects of acetylcholine on neurons in the feline nucleus reticularis thalami. J. Pbysiol. (Lond.) 261:647-671.

Benjamin, R.M., and C. Pfaffman (1955) Cortical localization of taste in albino rat. J. Neurophysiol. 18:56-64.

Bentivoglio, M., D. Van der Kooy, and H.G.J.M. Kuypers (1979) The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labeling study. Brain Res. 174:l-18.

Bentivoglio, M., G. Macchi, and A. Albanese (1981) The cortical projections of the thalamic intralaminar nuclei as studied in cat and rat with the multiple fluorescent retrograde tracing technique. Neurosci. Lett. 26:5- 10.

Berkley, K.J., and I.G. Worden (1978) Projections to the inferior olive of the cat. I . Comparisons of input from the dorsal column nuclei, the lateral cervical nucleus, the spino-olivary pathways, the cerebral cortex, and the cerebellum. J. Comp. Neurol. 180:237-252.

Berman, N. (1977) Connections of the pretectum in the cat. J. Comp. Neurol. 174:227-254.

Berman, A.L. (1968) The Brainstem of the Cat. A Cytoarchitectonic Atlas With Stereotaxic Coordinates. Madison: The University of Wisconsin Press, pp. 38-43.

Bharos, T.B., H.G.J.M. Kuypers, R.N. Lemon, and R.B. Muir (1981) Diver- gen collaterals from deep cerebellar neurons to thalamus and tectum, and to medulla oblongata and spinal cord: Retrograde fluorescent study. Exp. Brain Res. 42399-411.

Bloedel, J.R. (1973) Cerebellar afferent systems: a review. Prog. Neurobiol. 2:l-68.

Blomquist, A,, R. Fink, D. Bowsher, S. Griph, and J. Westman (1978) Tectal and thalamic projections of dorsal column and lateral cervical nuclei; a quantitative study in the cat. Brain Res. 141:335-344.

Boivie, J. (1978) Anatomical observations on the dorsal column nuclei, their thalamic projection and the cytoarchitecture of some somato-sensory thalamic nuclei in the monkey. J. Comp. Neurol. 178:17-48.

Boivie, J. (1971a) The termination of the spinothalamic tract in the cat. An experimental study with silver impregnation. Exp. Brain Res. 12:331- 353.

Boivie, J. (1971b) The termination in the thalamus and the zona incerta of fibres from the dorsal column nuclei DCN in the cat. An experimental study with silver impregnation methods. Brain Res. 28:459-490.

Boivie, J. (1980) Thalarnic projections from lateral cervical nucleus in monkey. Brain Res. 198:13-26.

Boivie, J. (1979) An anatomical reinvestigation of the termination of the spinothalamic tract in the monkey. J. Comp. Neurol. I86:343-370.

Bold, E.L., and E.J. Neafsey (1982) A comparison of thalamic afferents to the rostra1 and caudal forelimb regions of rat motor cortex. Neurosci. Abstr. 8.542.

Bowker, R.M., and J.D. Coulter (1981) Intracortical connectivities of somatic sensory and motor areas. In C.N. Woolsey (ed): Cortical Sensory Orga- nization. I. Multiple Somatic Areas. Clifton, N J Humana Press.

Brann, M.R., and P.C. Emson (1980) Microiontophoretic injection of fluorescent tracer combined with simultaneous immunofluorescent histochemistry for the demonstration of efferents from the caudate putamen projecting to the globus pallidus. Neuroscience Lett. 16:61-65.

Brinkman, C., and R. Porter (1979) Supplementary motor area in the monkey: Activity of neurons during performance of a learned motor cortex. J. Neurophysiol. 42681-709.

Brodal, A., A.M. Destombes, A.M. Lacerda, and P. Angaut (1972) A cerebellar projection onto the pontine nuclei. An experimental anatomical study in the cat. Exp. Brain Res. 16:115-139.

Brodal, A. (1981) Neurological Anatomy in Relation to Clinical Medicine. New York Oxford University Press, pp. 1-600.

Brooks, V.B., and S.D. Stoney (1971) Motor mechanisms: the role of the pyramidal system in motor control. Annu. Rev. Physiol. 33:337-392.

Brown, L.T. (1974) Cortico-rubral projections in the rat. J. Comp. Neurol. 154:149-168.

Bucher, V.M., and W.J.H. Nauta (1954) A note on the pretectal cell groups in the rat’s brain. J. Comp. Neurol. 100:287-295.

Bunney, B.S., and G.K. Aghajanian (1976) The precise localization of nigral afferents in rat as determined by retrograde tracing technique. Brain Res. 117:423-435.

Burne, R.A., S.A. Azizi, G.A. Mihailoff, and D.J. Woodward (1981) The tectopontine projection in the rat with comments on visual pathways to the basilar pons. J. Comp. Neurol. 202287-307.

Burton, H., G. Mitchell, and D. Brent (1982) Second somatic sensory area in the cerebral cortex of rats: Somatotopic organization and cytoarchitecture. J. Comp. Neurol. 210:109-135.

Carman, J.B., W.M. Cowan, and T.P.S. Powell (1964) Cortical connexions of the thalamic reticular nucleus. J. Anat 98:587-598.

Carman, J.B., W.M. Cowan, T.P.S. Powell, and K.E. Webster (1965) A bilateral corticostriate projection. J. Neurol. Neurosurg. Psychiatry 28:71- 77.

Carpenter, M.B. (1976) Anatomical organization of the corpus striatum and related nuclei. In M. Yahr (ed): The Basal Ganglia, New York: Raven Press, pp. 1-36.

Carpenter, M.B., and N.L. Strominger (1967) Efferent fibers of the projections of the subthalamic nucleus in the monkey. A comparison of the efferent projections of the subthalamic nucleus, substantia nigra and globus pallidus. Am. J. Anat. 121:41-72.

Carpenter, M.B., K. Nakano, and R. Kim (1976) Nigrothalamic projections in the monkev demonstrated bv autoradiomaphic techniques. J. Comp. - . Neurol. 165:401-416.

tions of the subthalamic nucleus in the monkey. Brain Res. 224:l-29. Carpenter, M.B., S.C. Carleton, J.T. Keller, and P. Conte (1981a) Connec-

Carpenter, M.B., R.R. Batton, S.C. Carleton, and J.T. Keller (1981b) Inter- connections and organization of pallidal and subthalamic nucleus neurons in the monkey. J. Comp. Neurol. 1974.579-605,

Carter, D.A., and H.C. Fibiger (1978) The projections of the entopeduncular nucleus and globus pallidus in rat as demonstrated by autoradiography and horseradish peroxidase histochemistry. J. Comp. Neurol. 177:113- 124.

Castiglioni, A.J., M.C. Gallaway, and J.D. Coulter (1978) Spinal projections from the midbrain in monkey. J. Comp. Neurol. 178:329-346.

Catsman-Berrevoets, C.E., and H.G.J.M. Kuypers (1981) A search for corticospinal collaterals to thalamus and mesencephalon by means of multiple retrograde fluorescent tracers in cat and rat. Brain Res. 218:15-33.


Caughell, K.A., and B.A. Flumerfelt (1977) The organization of the cerebel- lorubral projection: An experimental study in the rat. J. Comp. Neurol. 176295-306.

Chan-Palay, V. (1977) Cerebellar Dentate Nucleus. New York: Springer, pp. 1-400.

Clavier, R.M., S. Atmadja, and H.C. Fibiger (1976) Nigrothalamic projections in the rat as demonstrated by orthograde and retrograde tracing techniques. Brain Res. Bull. 1:379-384.

Collins, R.C. (1978) Kindling of neuroanatomic pathways during recurrent focal penicillin seizures. Brain Res. 150:503-517.

Collins, R.C., C. Kennedy, L. Sokoloff, and F. Plum (1976) Metabolic anatomy of focal motor seizures. Arch. Neurol. 33:536-542.

Comans, P.E., and P.J. Snow (1981) Ascending projections to nucleus para- fasicularis of the cat. Brain Res. 230:337-341.

Conde, F., and H. Conde (1982) The rubro-olivary tract in the cat, as demonstrated with the method of retrograde transport of horseradish peroxidase. Neuroscience 7:715-724.

Cospito, J.A., and K. Kultas-Ilinsky (1981) Synaptic organization of motor corticostriatal projections in the rat. Exp. Neurol. 725257366,

Courville, J. (1966) Rubrobulhar fibers to the facial nucleus and the lateral reticular nucleus (nucleus of the lateral funiculus). An experimental study in the cat with silver impregnation methods. Brain Res. 1.317- 337.

Courville, J., and S. Otabe (1974) The rubroolivary projection in the ma- caque: An experimental study with silver impregnation methods. J. Comp. Neurol. 158.479-494.

Cowan, W.M., and T.P.S. Powell (1966) Striopallidal projection in the monkey. J. Neurol. Neurosurg. Psychiatry 29.426-439.

Cowan, W.M., and T.P.S. Powell (1955) The projection of the midline and intralaminar nuclei of the thalamus of the rabbit. J. Neurol. Neurosurg. Psychiatry 18:266-279.

Crutcher, M.D., and M.R. DeLong (1982) Functional organization of the primate putamen. Neurosci. Abstr. 8.960.

Curry, M.J. (1972) The effects of stimulating the somatic sensory cortex on single neurons in the posterior group (PO) of the cat. Brain Res. 44:463- 481.

Dahlstrom, A., and K. Fuxe (1964) Evidence for the existence of monoamine containing neurons in the central nervous system. Acta Physiol. Scand. 62[Suppl. 232]:1.

Davidson, N. (1965) The projection of afferent pathways in the thalamus of the rat. J. Comp. Neurol. 124t377-390.

De Long, M. (1971) Activity of pallidal neurons during movement. J. Neu- rophysiol. 34:414-427.

Deniau, J.M., C. Hammond, G. Chavalier, and J. Feger (1978) Evidence for branched subthalamic nucleus projections to substantia nigra, entopeduncular nucleus and globus pallidus. Neurosci. Lett. 9.117-121.

DeVito, J.L., and D. Simmons (1976) Some connections of the posterior thalamus in monkey. Exp. Neurol. 51~347-362.

Dichiara, G., M.L. Porceddu, M. Morelli, M.L. Mulas, and O.L. Gessa (19791 Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res. 176:273-284.

Dingledine, R., and J.S. Kelly (1977) Brainstem stimulation and the acetylcholine-evoked inhibition of neurones in the feline nucleus reticularis thalami. J. Physiol (Lond.) 271r135-154.

Divac, I., and N.H. Diemer (1980) F'refrontal system in the rat visualized by means of labeled deoxyglucose-further evidence for functional heteroge- neity of the neostriatum. J. Comp. Neurol. 190.1-13.

Donaldson, L., P.J. Hand, and A.R. Morrison (1975) Cortical-thalamic rela- tionships in the rat. Exp. Neurol. 47r448-458.

Donoghue, J.P., and F.F. Ebner (1981a) The laminar distribution and ultra- structure of fibers projecting from three thalamic nuclei to somatic sensory-motor cortex of the opossum. J. Comp. Neurol. 198:389-420.

Donoghue, J.P., K.L. Kerman, and F.F. Ebner (1979) Evidence for two organization plans within the somatic sensory-motor cortex of the rat. J. Comp. Neurol. 183:647-664.

Donoghue, J.P., and F.F. Ebner (1981a) The organization of thalamic projections to the parietal cortex of the Virginia opossum. J. Comp. Neurol. 198:365-388.

Drager, U.C., and D.H. Huhel (1976) Topography of visual and somatosensory projections to mouse superior colliculus. J. Neurophysiol. 39:91- 101.

Edwards, S.B. (1972) The ascending and descending projections of the red nucleus in the cat: An experimental study using an autoradiographic

tracing method. Brain Res. 48:45-63. Edwards, S.B. (1975) Autoradiographic studies of the projections of the

midbrain reticular formation: Descending projections of nucleus cuneiformis. J. Comp. Neurol. 161:341-359.

Edwards, S.B., and J.S. deOlmos (1976) Autoradiographic studies of the projection of the midbrain reticular formation: Ascending projections of nucleus cuneiformis. J. Comp. Neurol. 165:417-432.

Edwards, S.B., and C.K. Henkel(1978) Superior colliculus connections with the extraocular motor nuclei. J. Comp. Neurol. 179r451-468.

Edwards, S.B., C.L. Ginsburgh, C.K. Henkel, and B.E. Stein (1979) Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neurol. 184r309-329.

Eidelberg, E., J.G. Walden, and L.H. Nguyen (1981) Locomotor control in monkeys. Brain 104:647-663.

Emmers, R. (1965) Organization of the first and second somesthetic regions (SI and SII) in the rat thalamus. J. Comp. Neurol. 124.215-228.

Evarts, E.V., and W.T. Thach (1969) Motor mechanisms of the CNS: Cerebro- cerebellar interrelations. Annu. Rev. Physiol. 31r451-498.

Faull, R.L.M., and W.R. Mehler (1976) Subdivision of the ventral tier nuclei in the rat thalamus based on their afferent fiber connections. Anat. Rec. 184:400.

Faull, R.L.M., and W.R. Mehler (1978) The cells of origin of nigrotectal, nigrothalamic, and nigrostriatal projections in the rat. Neuroscience 3:989-1002.

Faull, R.L.M., and J.B. Carman (1978) The cerebellofugal projections in the brachium conjunctivum in the rat. I. The contralateral ascending pathway. J. Comp. Neurol. 178r495-518.

Filion, M., and C. Harnois (1978) A comparison of projections of entopendun- cular neurons to the thalamus, the midbrain and the habenula in the cat. J. Comp. Neurol. 181:763-780.

Flumerfelt, B.A., S. Otabe, and J. Courville (1973) Distinct projections to the red nucleus from the dentate and interposed nuclei in the monkey. Brain Res. 50:408-414.

Fox, C.A., and J.A. Rafols (1975) The radial fibers in the globus pallidus. J. Comp. Neurol. 159r177-200.

Fox, C.A., and J.T. Schmitz (1944) The suhstantia nigra and the entopeduncular nucleus in the cat. J. Comp. Neurol. 80:323-334.

Fox, C.A., J.A. Rafols, and W.M. Cowan (1975) Computer measurements of axis cylinder diameters of radial fibers and comb bundle fibers. J. Comp. Neurol. 159.201-224.

Frankfurter, A., J.T. Weber, G.J. Royce, N.L. Stommger, and J.K. Harting (1976) An autoradiographic analysis of the tecto-olivary projection in primates. Brain Res. 118:245-257.

Friedman, D.P., and E.G. Jones (1981) Thalamic input to areas 3a and 2 in monkeys. J. Neurophysiol. 45:59-85.

Fukushima, K., M. Ohno, and M. Kato (1981) Responses of cat mesencephalic reticulospinal neurons to stimulation of superior colliculus, peri- cruciate cortex, and neck muscle afferents. Exp. Brain Res. 44r441-444.

Garey, L.J., E.G. Jones, and T.P.S. Powell (1968) Interrelationships of striate and extrastriate cortex with the primary relay sites of the visual pathway. J. Neurol. Neurosurg. Psychiatry 31r135-157.

Gatter, K.C., and T.P.S. Powell (1978) The intrinsic connections of the cortex of area 4 of the monkey. Brain 101r513-541.

Georgopoulos, A.P., and M.R. Delong (1978) The globus pallidus of the monkey: neuronal activity in relation to movement. Neurosci. Abstr. 4:43.

Gerfen, C.R., and R.M. Clavier (1979) Neural inputs to the prefrontal agranular insular cortex in the rat. Horseradish peroxidase study. Brain Res. Bull. 4:347-353.

Gerfen, C.R., W.A. Staines, G.W. Arbuthnott, and H.C. Fibiger (1982) Crossed connections of the substantia nigra in the rat. J. Comp. Neurol. 207.283- 303.

Ghez, C. (1975) Input-output relations of the red nucleus in the cat. Brain Res. 98:93-108.

Goldberg, L., J. Courville, J.P. Lund, and J.S. Kauer (1980) Increased uptake of C'H) deoxyglucose and (14C) deoxyglucose in localized regions of the brain during stimulation of the motor cortex. Can. J. Physiol. Pharma- col. 58.1086-1091.

Goldman-Rakic, P.S., and M.L. Schwartz (1982) Interdigitation of contralat- era1 and ipsilateral columnar projections to frontal association cortex in primates. Science 216:755-757.

Goldman, P.S., and W.J.H. Nauta (1976) Autoradiographic demonstration of a projection from the prefrontal association cortex to the superior colliculus in the rhesus monkey. Brain Res. 116:145-149.

282 F.R. SHARP

Ingvar, D.H., and J. Risberg (1967) Increase of regional cerebral blood flow during mental effort in normals and patients with focal brain disorders. Exp. Brain Res. 3:195-211.

Jackson, A,, and A.R. Crossman (1981) Subthalamic projection to nucleus tegmenti pendunculopontius in the rat. Neurosci. Lett. 22(1):17-23.

Jackson, A,, and A.R. Crossman (1981) Subthalamic nucleus efferent projection to the cerebral cortex. Neuroscience 6:2367-2377.

Jacobson, S. (1970) Distribution of the commissural axon terminals in the rat neocortex. Exp. Neurol. 2&?:193-205.

Johnson, F.H., and C. Clemente (1959) An experimental study of the fiber connections between the putamen, globus pallidus, ventral thalamus, and midbrain tegmentum in cat. J. Comp. Neurol. 113.43-102.

Jones, E.G., J.D. Coulter, H. Burton, and R. Porter (1977) Cells of origin and terminal distribution of corticostriatal fihers arising in the sensory- motor cortex of monkeys. J. Comp. Neurol. 17353-80.

Jones, E.G. (1971) An analysis of the posterior group of thalamic nuclei on the basis of its afferent connexions. J. Comp. Neurol. 143:185-216.

Jones, E.G., and T.P.S. Powell (1969) Connexions of the somatic sensory cortex in the rhesus monkey. I. Ipsilateral cortical connexions. Brain 92:477-502.

Jones, E.G., and H. Burton (1974) Cytoarchitecture and somatic sensory connectivity of thalamic nuclei other than the ventrobasal complex in the cat. J. Comp. Neurol. 154:395-432.

Jones, E.G., and T.P.S. Powell (1969) Connexions of the somatic sensory cortex of the rhesus monkey. 11. Contralateral cortical connexions. Brain 92:717-730.

Jones, E.G., S.P. Wise, and J.D. Coulter (1979) Differential thalamic rela- tionships of sensory-motor and parietal cortical fields in monkeys. J. Comp. Neurol. 1835333-882.

Jones, E.G., J.D. Coulter, and S.H.C. Hendry (1978) Intracortical connectivity of architectonic fields in the somatic sensory motor, and parietal cortex of monkeys. J. Comp. Neurol. 181:291-348.

Jones, E.G., and R.Y. Leavitt (1974) Retrograde axonal transport and the demonstration of nonspecific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J. Comp. Neurol. 154:349-378.

Jones, E.G., (1975) Some aspects of the organization of the thalamic reticular complex. J. Comp. Neurol. 162:285-308.

Jones, E.G., H. Burton, and R. Porter (1975) Commissural and corticocortical “columns” in the somatic sensory cortex of primates. Science 190:572-574

Juliano. S.L., Hand, P.J., and B.L. Whitsel (1981) Patterns of increased metabolic activity in somatosensory cortex of monkeys Macaca fascicularis, subjected to controlled cutaneous stimulation: A 2-deoxyglucose study. J. Neurophysiol. 46:1260-1284.

Kaitz, S.S., and R.T. Robertson (1981) Thalamic connections with limbic cortex. 11. Corticothalamic projections. J. Comp. Neurol. 195:527-545.

Kalil, K. (1981) Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey. J. Comp. Neurol. 195r25-50.

Kassel, J. (1982) Somatotopic organization of SI corticotectal projections in rats. Brain Res. 231:247-255.

Kawamura, K., A. Brodal, and G. Hoddevik (1974) The projection of the superior colliculus onto the reticular formation of the brainstem. An experimental anatomical study in the cat. Exp. Brain Res. 19:l-19.

Kawamura, K., and H. Tsutomu (1978) Cell bodies of origin of reticular projections from the superior colliculus in the cat: An experimental study with the use of horseradish peroxidase as a tracer. J. Comp. Neurol. 181:1-16.

Keller, J.H., and P.J. Hand (1970) Dorsal root projections to nucleus cuneatus of the cat. Brain Res. 2O:l-17.

Kemp, J.M., and T.P.S. Powell (1970) The corticostriate projection in the monkey. Brain 93:525-546.

Kemp, J.M., and T.P.S. Powell (1971) The connexions of the striatum and globus pallidus: Synthesis and speculation. Philos. Trans. R. SOC. Lond. [Biol.] 262:441-457.

Kennedy, C., M.H. DesRosiers, J.W. Jehle, M. Reivich, F.R. Sharp, and L. Sokoloff (1975) Mapping of functional neural pathways by autoradiographic survey of local metabolic rate with 14C deoxyglucose. Science 187350-853.

Kievit, J., and H.G.J.M. Kuypers (1977) Organization of thalamocortical connections to the frontal lobe in the rhesus monkey. Exp. Brain Res. 29.299-322.

Killackey, H.P. (1973) Anatomical evidence for cortical subdivisions based on vertical discrete thalamic projections from the ventral posterior nucleus to cortical barrels in the rat. Brain Res. 51:326-331.

Goldman, P.S., and W.J.H. Nauta (1977a) Columnar distribution of corticocortical fihers in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res. 1221393-413.

Goldman, P.S., and W.J.H. Nauta (1977b) An intricately patterned pre- fronto-caudate projection in the rhesus monkey. J. Comp. Neurol. 171:369-386.

Graham, J. (1977) An autoradiographic study of the efferent connections of the superior colliculus in the cat. J. Comp. Neurol. 173:629-654.

Graybiel, A.M. (1978) The organization of the nigrotectal connection: An experimental tracer study in the cat. Brain Res. 143:339-348.

Grillner, S., and M.I. Shik (1973) On the descending control of the lumbosa- cral spinal cord from the “mesencephalic locomotor region.” Acta Phys- iol. Scand. 87:320-333.

Grofova, I. (1979) Extrinsic connections of the neostriatum. In I. Divac and R.G.E. Oberg (eds): The Neostriatum. New York: Perganion Press, pp, 37-51.

Grofova, I., J.M. Deniau, and S.T. Kitai (1982) Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J. Comp. Neurol. 208:352-368.

Guilbaud, G., D. Caille, J.M. Besson, and G. Benelli (1977) Single unit activities in ventral posterior and posterior group thalamic nuclei during nociceptive stimulations in the cat. Arch. Ital. Biol. 115r38-56.

Gwyn, D.G., and B.A. Flumerfelt (1974) A comparison of the distribution of cortical and cerebellar afferents in the red nucleus of the rat. Brain Res. 69:130-135.

Hall, R.D., and E.P. Lindholm (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res. 66:23-38.

Hand, P.J., and A.R. Morrison (1970) Thalamo-cortical projections from the ventrobasal complex to somatic sensory areas I and 11. Exp. Neurol. 26.291-308.

Hand, P.J., and T.V. Winkle (1977) The efferent connections of the feline nucleus cuneatus. J. Comp. Neurol. 171t83-110.

Haroian, A.J., L.C. Massopust, and P.A. Young (1981) Cerebello-thalamic projections in the rat: An autoradiographic and degeneration study. J. Comp. Neurol. 197(2):217-237.

Hartmann-Von Monakow, K., K. Akert, and H. Kiinzle (1978) Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. 33:395-403.

Hartmann-Von Monakow, K., K. Akert, and H. Kiinzle (1979) Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in Macaca fascicularis. Exp. Brain Res. 34:91-105.

Hattori, T., H.C. Fibiger, and P.L. McGeer (1975) Demonstration of a palli- donigral projection innervating dopaminergic neurons. J. Comp. Neurol. 162487-504.

Henkel, C.K., and S.B. Edwards (1978) The superior colliculus control of pinna movements in the cat: Possible anatomical connections. J. Comp. Neurol. 182:763-776.

Herkenham, M. (1979) The afferent and efferent connections of the ventromedial nucleus in the rat. J. Comp. Neurol. 183:487-510.

Herkenham, M.A. (1980) Laminar organization of thalamic projections to the rat neocortex. Science 207:532-535.

Hoover, D.B., and D.M. Jacohowitz (1979) Neurochemical and histochemical studies of the effect of a lesion of the nucleus cuneiformis on the cholinergic innervation of discrete areas of rat brain. Brain Res. 170:113-122.

Hopkins, D.A., and L.W. Niessen (1976) Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat, and monkey. Neurosci. Lett. 2253-259.

Hougard, K., T. Oikawa, E. Sveinsdottier, E. Skinhoj, D.H. Ingvar, and N.A. Lassen (1976) Regional cerebral blood flow in focal cortical epilepsy. Arch. Neurol. 33:527-535.

Houser, C.R., J.E. Vaugh, R.P. Barber, and E. Roberts (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res. 200(2):341-355.

Huber, G.C., E.C. Crosby, B. Tamthai (1943) The mammalian midbrain and isthmus regions. Part I. The nuclear pattern. J. Comp. Neurol. 78:129- 534.

Humphrey, D.R., and R.R. Rietz (1976) Cells of origin of cortico-rubral projections from the arm area of primate motor cortex and their synaptic actions in the red nucleus. Brain Res. 110:162-169.

Imperato, A,, M.L. Porceddu, M. Morelli, G. Faa, and G. Dichiara (1981) Role of dorsal mesencephalic reticular formation and deep layers of superior colliculus as output stations for turning behaviour elicited from the substantia nigra pars reticulata. Brain Res. 216:437-443.

Ingle, D., and J.M. Sprague (1975) Sensorimotor function of the midbrain tectum. Neurosci. Res. Program Bull. 13:169-288.


Killackey, H.P., and S. Leshin (1975) The organization of specific thalamocortical projections to the posteromedial barrel subfield of the rat somatic sensory cortex. Brain Res. 86469-472.

Killackey, H.P., and R.S. Erzurumlu (1981) Trigeminal projections to the superior colliculus of the rat. J. Comp. Neurol. 201:221-242.

Kim, R., K. Nakano, A. Jayaraman, and M.B. Carpenter (1976) Projections of the globus pallidus and adjacent structures: An autoradiographic study in the monkey. J. Comp. Neurol. 169~263-290.

Kitai, S.T., and J.M. Deniau (1981) Cortical inputs to the subthalamus: Intracellular analysis. Brain Res. 214:411-416.

Kohlerman, N.J., A.R. Gibson, and J.C. Houk (1982) Velocity signals related to hand movements recorded from red nucleus neurons in monkeys. Science 217:857-860.

Kotchabhakdi, N., E. Rinvik, F. Walberg, and K. Yingchareon (1980) The vesihulothalamic projections in the cat studied by retrograde axonal transport of horseradish peroxidase. Exp. Brain Res. 40:405-418.

Kiinzle, H. (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 88:195-210.

Kunzle, H. (1976) Thalamic projections from the precentral cortex in Macaca fascicularis. Brain Res. 105.253-267.

Kunzle, H. (19771 Projections for the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp. Brain Res. 30:481-492.

Kunzle, H., and K. Akert (1977) Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J. Comp. Neurol. 173:145-164.

Kiinzle, H. (1978a) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in Macaca fascicularis. Brain Behav. Evol. 15:185-234.

Kiinzle, H. (1978b) Cortico-cortical efferents of primary motor and somatosensory regions of the cerebral cortex in Macaca fascicularis. Neurosci- ence 3.25-39.

Kuypers, H.G.J.M., and J.D. Tuerk (1964) The distribution of the cortical fibres within the nuclei cuneatus and gracillis in the cat. J. Anat. 98: 143-162.

Kuypers, H.G.J.M., and D.G. Lawrence (1967) Cortical projections to the red nucleus and the brainstem in the rhesus monkey. Brain Res. 4:151- 188.

Kuypers, H.G.J.M., and J. Brinkman (19701 Precentral projections to different parts of the spinal intermediate zone in the rhesus monkey. Brain Res. 24.29-48.

Larsen, K.D., and J. Sutin (19781 Output organization of the feline entopeduncular and subthalamic nuclei. Brain Res. 1572-31.

Larsen, K.D., and R.L. McBride (19791 The organization of feline entopeduncular nucleus projections: Anatomical studies. J. Comp. Neurol. 184293- 308.

Larsen, K.D., and H. Yumiya (1980) The red nucleus of the monkey: Topo- graphic localization of somatosensory input and motor output. Exp. Brain Res. 40,393-404.

Lidsky, T.I., N.A. Buchwald, C.D. Hull, and M.S. Levine (1975) Pallidal and entopeduncular single unit activity in cats during drinking. Electroen- cephalog. Clin. Neurophysiol. 39:79-84.

Lorente de NO, R. (1922) La corteza cerebral del raton. Trab. Inst. Cajal Invest. Biol. 2O:l-38.

Lund, R.D. (1967) Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. J. Comp. Neurol. I30:313-328.

Lund, R.D., and K.E. Webster (19671 Thalamic afferents from the dorsal column nuclei. An experimental anatomical study in the rat. J. Comp. Neurol. 130:301-312.

Martin, G.F., R. Don], S. Katz, and J.S. King (1974) The organization of projection neurons in opossum red nucleus. Brain Res. 78:17-34.

Massion, J. (1967) The mammalian red nucleus. Physiol. Rev. 47:359-436. Matsunami, K., T. Kageyama, and K. Kubota (1981) Radioactive 2-deoxy-d-

glucose incorporation into the prefrontal and premotor cortex of the monkey performing a forelimb movement. Neurosci. Lett. 26:37-41.

Mehler, W.R., and W.J.H. Nauta (1974) Connections of the basal ganglia and of the cerebellum. Confin. Neurol. 36:205-222.

Mehler, W.R. (1971) Idea of a new anatomy of the thalamus. J. Psychiatr. Res. 8:203-217.

Menetrey, D., A. Chaouch, D. Binder, and J.M. Besson (1982) The origin of the spinomesencephalic tract in the rat: An anatomical study using the retrograde transport of horseradish peroxidase. J. Comp. Neurol. 206:193-207.

Miller, R.A., and N.L. Strominger (1973) Efferent connections of the red nucleus in the brainstem and spinal cord of the rhesus monkey. J. Comp. Neurol. 152327-346.

Mohler, C.W., and R.H. Wurtz (1977) Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. J. Neurophysiol. 4Or74-94.

Moll, L., and H.G.J.M. Kuypers (1977) Premotor cortical ablations in monkeys: Contralateral changes in visually guided reaching behavior. Sci- ence 198:317-319.

Mulas, A., R. Longoni, L. Spina, M. Delfiacco, and G. DiChiara (1981) Ipsiversive turning behavior after discrete unilateral lesions of the dorsal mesencephalic reticular formation by kainic acid. Brain Res. 208:468-472.

Murray, E.A., and J.D. Coulter (1982) Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Res. 243.201-214.

Nagata, T., and L. Kruger (1979) Tactile neurons of the superior colliculus of the cat. Input and physiological properties. Brain Res. 174:19-37.

Nagy, J.I., D.A. Carter, and H.C. Fibiger (1978) Anterior striatal projections to the globus pallidus, entopeduncular nucleus and substantia nigra in the rat: The GABA connection. Brain Res. 158:15-29.

Nauta, W.J.H., and W.R. Mehler (1966) Projections of the lentiform nucleus in the monkey. Brain Res. 1:3-42.

Nauta, H.J.W., and M. Cole (1978) Efferent projections of the subthalamic nucleus: An autoradiographic study in monkey and cat. J. Comp. Neu- rol. 18O:l-16.

Nauta, W.J.H., G.P. Smith, R.L.M. Faull, and V.B. Domesick (1978) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3:385-401.

Nauta, H.J.W. (1979) Projections of the pallidal complex: An autoradiographic study in the cat. Neuroscience 4:1853-1873.

Neafsey, E.J. (1980) A second forelimb motor area exists in rat frontal cortex. Neurosci. Abstr. 6:156.

Neafsey, E.J., and C. Sievert (1982) A second forelimb area exists in rat frontal cortex. Brain Res. 232151-156.

Nelson, R.J., M. Sur, and J.H. Kaas (1979) The organization of the second somatosensory area (smll) of the grey squirrel. J. Comp. Neurol. 184:473- 490.

Nyberg-Hansen, R., and A. Brodal (1964) Sites and mode of termination of rubrospinal fibres in the cat. An experimental study with silver impregnation methods. J. Anat. 98:235-253.

Orgogozo, J.M., and B. Larsen (1979) Activation of the supplementary motor area during voluntary movement in man suggests it works as a supra- motor area. Science 206:847-850.

Padel, Y., A.M. Smith, and J. Armand (1973) Topography of projections from the motor cortex to rubrospinal units in the cat. Exp. Brain Res. 17:315- 332.

Padel, Y., and T. Jeneskog (1981) Inhibition of rubrospinal cells by somesthetic afferent activity. Neurosci. Lett. 21:177-182.

Pandya, D.N., and L.A. Vignolo (1971) Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey. Brain Res. 26217-233.

Pandya, D.N., and L.A. Vignolo (1968) Interhemispheric neocortical projections of somatosensory areas I and I1 in the rhesus monkey. Brain Res. 7:300-303.

Pappas, C.L., and P.L. Strick (1981) Anatomical demonstration of multiple representation in the forelimb region of the cat motor cortex. J. Comp. Neurol. 200:491-501.

Parent, A., and L. DeBellefeuille (1982) Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by fluorescence retrograde labeling method. Brain Res. 245.201-213.

Paxinos, G., and C. Watson (1982) Rat brain atlas. In: Stereotaxic Coordi- nates. New York Academic Press, pp. 1-69.

Pearson, J.C., and D.E. Haines (1980) Somatosensory thalamus of a prosi- mian primate (Galago senegalensis). 11. An HRP and Golgi study of the ventral posterolateral nucleus (VPL). J. Comp. Neurol. 190;559-580.

Penfield, W., and H. Jasper (1954) Epilepsy and the Functional Anatomy of the Human Brain. Little-Brown, Boston.

Penfield, W., and T. Rasmussen (1950) The Cerebral Cortex of Man. New York: The Macmillan Company.

Penney, J.B., and A.B. Young (1981) GABA as the pallidothalamic neurotransmitter: Implications for basal ganglia function. Brain Res. 207:195- 199.

Phillips, C.G. (1967) Cortico motorneuronal organization. Projection from the arm area of the Baboon’s motor cortex. Arch. Neurol. 17:188-195.

284 F.R. SHARP

Phillips, C.G., and R. Porter (1977) Corticospinal neurons. Their role in movement. Monogr. Physiol. Soci. No. 34, London: Academic Press.

Poggio, G.F., and V.B. Mountcastle (1960) A study of the functional contri- butions of the lemniscal and spinothalamic systems to somatic sensibil- ity. Bull. Johns Hopk. Hosp. 106r266-316.

Pompeiano, O., and A. Brodal (1957) Experimental demonstration of a somatotopical organization of rubrospinal fibers in the cat. J. Comp. Neurol. 108.225-252.

Price, T.R., and K.E. Webster (1972) The corticothalamic projection from the primary somatosensory cortex of the rat. Brain Res. 44:636-640.

Rapasardi, S.C., P.D. Wilson, and F.L. Alvarez (1974) Reticular modulation of evoked potentials a t the cortex and lateral geniculate nucleus of the unanesthetized squirrel monkey. Exp. Neurol. 44:282-294.

Rhoades, R.W. (1981) Organization of somatosensory input to the deep collicular laminae in hamster. Behav. Brain Res. 3.201-222.

Ricardo, J.A. (1980) Efferent connections of the subthalamic region in the rat. I. The subthalamic nucleus of Luys. Brain Res. 202257-271.

Ricardo, J.A. (1981) Efferent connections of the subthalamic region in the rat. 11. The zona incerta. Brain Res. 214t43-60.

Rinvik, E., and F. Walberg (1963) Demonstration of a somatotopically arranged corticorubral projection in the cat. An experimental study with silver methods. J. Comp. Neurol. 120:393-407.

Rinvik, E. (1966) The cortico-nigral projection in the cat. An experimental study with silver impregnation methods. J. Comp. Neurol. 126:241-254

Rinvik, E., and I. Grofova (1974) Cerebellar projections to the nuclei ven. tralis lateralis and ventralis anterior thalami. Experimental electron microscopical and light microscopical st.udies in the cat. Anat. Embryol. 146:95-111.

Rinvik, E., I. Grofova, and O.P. Ottersen (1976) Demonstration of nigrotectal and nigroreticular projections in the cat by axonal transport of proteins. Brain Res. 112r388-394.

Rispal-Padel, L. and J. Massion (1970) Relations between the ventrolateral nucleus and the motor cortex in the cat. Exp. Brain Res. 10:331-339.

Rispal-Padel, L., and A. Grangetto (1977) The cerebello-thalamo-cortical pathway. Topographical investigation at the unitary level in the cat. Exp. Brain Res. 28:lOl-123.

Rispal-Padel, L., J. Massion, and A. Grangetto (1973) Relations between the ventrolateral thalamic nucleus and motor cortex and their possible role in the central organization of motor control. Brain Res. 6O:l-20.

Rivner, M., and J. Sutin (1981) Locus coeruleus modulation of the motor thalamus: Inhibition in nuclei ventralis lateralis and ventralis anterior. Exp. Neurol. 73:651-673.

Roland, P.E., B. Larsen, N.A. Lassen, and E. Skinhoj (1980a) Supplementary motor area and other cortical areas in organization of voluntary movements in man. J. Neuroohvsiol. 43r118-136.

Scalia, F. (1972) The termination of retinal axons in the pretectal region of mammals. J. Comp. Neurol. 145.223-258.

Scheibel, M.E., and A.B. Scheibel (1966) The organization of the nucleus reticularis thalami: A Golgi study, Brain Res. 1.43-62.

Schiller, P.H., and M. Stryker (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 35:915-924.

Schlag, J., and M. Waszak (1971) Electrophysiological properties of units of the thalamic reticular complex. Exp. Neurol. 3279-97.

Schneider, J.S., J.R. Morse, and T.I. Lidsky (1982) Somatosensory properties of globus pallidus neurons in awake cats. Exp. Brain Res. 46.311-314.

Schoppmann, A,, and M.P. Stryker (1981) Physiological evidence that the 2- deoxyglucose method reveals orientation columns in cat visual cortex. Nature 293:574-576.

Schwartzman, R.J., J. Greenberg, M. Reivich, K.J. Klose, and G.M. Alex- ander (1981) Functional metabolic mapping of a conditioned motor task in primates utilizing 2-(I4C) deoxyglucose. Exp. Neurol. 72(1):153-164.

Settlage, P.H., W.G. Bingham, H.M. Suckle, A.F. Borge, and C.N. Woolsey (1949) The pattern of localization in the motor cortex of the rat. Fed. Proc. 8:144.

Severin, F.V., M.L. Shik, and G.N. Orlovsky (1967) Work of the muscles and single motor neurons during controlled locomotion. Biophysics (Russia) 12762-772.

Shanks, M.F., A.J. Rockel, and T.P.S. Powell (1975) The commissural connections of the primary somatic sensory cortex. Brain Res. 98:166-171.

Sharp, F.R., and K. Evans (1982) Regional (14C) 2-deoxyglucose uptake during vibrissae movements evoked by rat motor cortex stimulation. J. Comp. Neurol. 208:255-287.

Sharp, F.R. (1976a) Activity-related increases of glucose utilization associated with reduced incorporation of glucose into the derivative. Brain Res. 107~663-666.

Sharp, F.R. (1976b) In neuroanatomical functional mapping by the radioactive 2-deoxy-d-glucose method. Neurosci. Res. Program Bull. 14:461- 518.

Sharp, F.R., T.S. Kilduff, S. Bzorgchami, H.C. Heller, and A.F. Ryan (1983) The relationship of local cerebral glucose utilization to optical density ratios. Brain Res. 263:97-103.

Shik, M.L., and G.N. Orlovsky (1976) Neurophysiology of locomotor auto- matism. Physiol. Rev. 56:465-501.

Skinner, J.E., and C.D. Yingling (1976) Regulation of slow potential shifts in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. Electroencephalogr. Clin. Neurophy- siol. 40:288-296.

Sokoloff, L. (1979) The (14C) deoxyglucose method: Four years later. Acta Neurol. Scand. 72[Suppl. 60]:640-649.

I "

Roland, P.E., E. Skinhoj, N.A. Lassen, and B. Larsen (1980b) Different cortical areas in man in the organization of voluntary movements in extra personal space. J. Neurophysiol. 43,137-150.

Roldad, M. and F. Reinoso-Suarez (1981) Cerebellar projections to the superior colliculus in the cat. J. Neurosci. 1r827-834.

Romansky, K.V., K.G. Usunoff, D.P. Ivanov, and G.P. Galabov (1979) Corti- cosubthalamic projection in the cat: An electron microscopic study. Brain Res. 163.319-327,

Rosen, I. (1969) Excitation of Group I activated thalamocortical relay neurons in the cat. J. Physiol. (Lond.)205:237-255.

Roucoux, A,, D. Guitton, and M. Crommelinck (1980) Stimulation of the superior colliculus in the alert cat. 11. Eye and head movements evoked when the head is unrestrained. Exp. Brain Res. 39:75-85.

Royce, G.J. (1978a) Cells of origin of subcortical afferents to the caudate nucleus; a horseradish peroxidase study in the cat. Brain Res. 153r465- 475.

Royce, G.J. (1978b) Autoradiographic eyidence for a discontinuous projection to the caudate nucleus from the ceutromedian nucleus in the cat. Brain Res. 146:146-150.

Ryugo, R., and H.P. Killackey (1975) Cortico-cortical connections of the barrel field of rat somatosensory cortex. SOC. Neurosci. Abstr. 1.126.

Saint-Cyr, J.A., and J. Courville (1982) Descending projections to the infe- riar olive from the mesencephalon and superior colliculus in the cat. Exp. Brain Res. 45:333-348.

Sakai, S.T. (1982) The thalamic connectivity of the primary motor cortex (MI) in the raccoon. J. Comp. Neurol. 204:238-252.

Saporta, S., and L. Kruger (1977) The organization of thalamocortical relay neurons in the rat ventrobasal complex studied by the retrograde transport of horseradish peroxidase. J. Comp. Neurol. 174:187-208.

Sokoloff, L., M. Reivich, C.H. Kennedy, M.H. DesRosiers, C.S. Patlak, K.D. Pettigrew, P. Sakurada, and M. Shinohara (1977) The 14C deoxyglucose method for the measurement of local cerebral glucose utilization: The- ory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28:897-916.

Sprague, J.M., and T.H. Meikle (1965) The role of the superior colliculus in visually guided behaviour. Exp. Neurol. 11r115-146.

Spreafico, R., N.L. Hayes, and A. Rustioni (1981) Thalamic projections to the primary and secondary somatosensory cortices in c a t Single and double retrograde tracer studies. J. Comp. Neurol. 203:67-90.

Starr, M.S., and I.C. Kilpatrick (1981) Distribution of aminobutyrate in the rat thalamus: Specific decreases in thalamic-aminobutyrate following lesion or electrical stimulation of the substantia nigra. Neuroscience 6r1095-1104.

Stein, B.E., B. Magalhaes-Castro, and L. Kruger (1976) Relationship between visual and tactile representation in cat superior colliculus. J. Neurophysiol. 39:401-419.

Stein, B.E., H.P. Clamann, and S.J. Goldberg (1980) Superior colliculus: control of eye movements in neonatal kittens. Science 210:78;80.

Strick, P.L. (1973) A light microscopic analysis of the cortical projection of the thalamic ventrolateral nucleus in the cat. Brain Res. 55:l-24.

Strick, P.L. (1975) Multiple sources of thalamic input to the primate motor cortex. Brain Res. 88372-377.

Strick, P.L. (1976) Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J. Neurophysiol. 39rlO20-1031.

Strick, P.L., and J.B. Preston (1982) Two representations of the hand in area 4 of a primate. I. Motor output organization. J. Neurophysiol. 48:139- 150.

Stryker, M.P., and P.H. Schiller (1975) Eye and head movements evoked by


electrical stimulation of monkey superior colliculus. Exp. Brain Res. 23t103-112.

Szabo, J. (1972) The course and distribution of the efferents from the tail of the caudate nucleus in the monkey. Exp. Neurol. 37:562-572.

Tanji, J.K., K. Taniguchi, and T. Saga (1980) The supplementary motor area: neuronal responses to motor instructions. J. Neurophysiol. 43:60- 68.

Thach, W.T., and E.G. Jones (1979) The cerebellar dentatothalamic connection: Terminal field, lamellae, rods and somatotopy. Brain Res. 169:168- 172.

Tolbert, D.L., H. Bantli, and J.R. Bloedel (1978) Multiple branching of cerebellar efferent projections in cats. Exp. Brain Res. 31:305-316.

Toyama, K., N. Tsukahara, K. Kosaka, and K. Matsunami (1970) Synaptic excitation of red nucleus neurones by fibres from interpositus nucleus. Exp. Brain Res. 11:187-198.

Tsukahara, N., and T. Bando (1970) Red nuclear and interposate nuclear excitation of pontine nuclear cells. Brain Res. 19:295-298.

Tsukahara, N., and K. Kosaka (1968) The mode of cerebral excitation of red nucleus neurons. Exp. Brain Res. 5:102-117.

Tulloch, I.F., G.W. Arbuthnott, and A.K. Wright (1978) Topographical organization of the striatorigral pathway revealed by anterograde and retrograde neuroanatomical tracing techniques. J. Anat. 127t425-441.

Uno, M., and M. Yoshida (1975) Monosynaptic inhibition of thalamic neurons produced hy stimulation of the pallidal nucleus in cats. Brain Res. 99:377-380.

Valverde, J. (1962) Reticular formation of the albino rat’s brainstem. Cy- toarchitecture and corticofugal connections. J. Comp. Neurol. 119:25- 53.

Van der Kooy, D. (1979) The organization of the thalamic, nigral and raphe cells projecting to the medial vs lateral caudate putamen in rat. A fluorescent retrograde double-laheling study. Brain Res. 169:381-387.

Van der Kooy, D.V., and T. Hattori (19801 Single subthalamic nucleus neurons project to both the globus pallidus and substantia nigra in rat. J. Comp. Neurol. 192(4):751-769.

Van der Kooy, D., and D.A. Carter (1981) The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res 211:15-36.

Van der Kooy, D., T. Hattori, K. Shannak, and 0. Hornykiewicz (1981) The pallido-subthalamic projection in rat: Anatomical and biochemical studies. Brain Res. 204:253-268.

Veazey, R.B., and C.M. Severin (1980a) Efferent projections of the deep mesencephalic nucleus (pars lateralisl in the rat. J. Comp. Neurol. 190:231-244.

Veazey, R.B., and C.M. Severin (1980b) Efferent projections of the deep mesencephalic nucleus (pars medialis) in the rat. J. Comp. Neurol. 190:245-258.

Veazey, R.B., and C.M. Severin (1982) Afferent projections to the deep mesencephalic nucleus in the rat. J. Comp. Neurol. 204:134-150.

Waite, P.M.E. (1973) Somatotopic organization of vibrissal responses in the ventro-basal complex of the rat thalamus. J. Physiol. (Lond.) 228:527- 540.

Walberg, F. (1956) Descending connections to the inferior olive. An experimental study in the cat. J. Coinp. Neurol. 104.77-174.

Walberg, F. (1974) Descending connections from the mesencephalon to the inferior olive: an experimental study in the cat. Exp. Brain Res. 20:145- 156.

Walberg, F., and T. Nordhy (1981) A re-examination of the rubro-olivary tract in the cat, using horseradish peroxidase as a retrograde and an anterograde neuronal tracer. Neuroscience 6:2379-2391.

Webster, K.E. (1961) Cortico-striate interrelations in the albino rat. J. Anat.

Weinrich, M., and S.D. Wise (1982) The premotor cortex of the monkey. J. 95:532-544.

Neurosci. 21329-1345.

Welker, C. (1971) Microelectrode delineation of fine grain somatotopic organization of SmI cerebral neocortex in albino rat. Brain Res. 26t259-275.

Welker, C. (1976) Receptive field of barrels in the somatosensory neocortex of the rat. J. Comp. Neurol. 166:173-190.

Welker, C., and M.N. Sinha (1972) Somatotopic organization of SmII cerebral neocortex in albino rat. Brain Res. 37:132-136.

Welker, C., and T.A. Woolsey (1975) Structure of layer IV in the somatosensory neocortex of the rat: Description and comparison with the mouse. J. Comp. Neurol. 158:437-454.

White, E.L., and R.A. DeAmicis (1977) Afferent and efferent pr~ljections of tract in the cat, using horseradish peroxidase as a retrograde and an anterograde neuronal tracer. Neuroscience 6~2379-2391.

Weber, J.T., G.D. Partlow, and J.K. Harting (1978) The projection of‘ the superior colliculus upon the inferior olivary complex of the cat: An the region in mouse SmI cortex which contains the posteromedial barrel subfield. J. Comp. Neurol. 175:455-482.

Wiesendanger, M. (1981) Organization of secondary motor areas of cerebral cortex. In V.B. Brooks (ed): Handbook of Physiology, Section I. The Nervous System. Vol. 11, Motor Control, part 2. Bethesda, MD: Ameri- can Physiology Society, pp. 1121-1147.

Wise, S.P., and J. Tanji (1981) Supplementary and precentral motor cortex: Contrast in responsiveness to peripheral input in the hindlimb area of the unanesthetized monkey. J. Comp. Neurol. 195:433-451.

Wise, S.P., and E.G. Jones (1977a) Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J. Comp. Neurol. 175:129-158.

Wise, S.P., and E.G. Jones (1976) The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J. Comp. Neurol. 168:313-344.

Wise, S.P., and E.G. Jones (1977b) Somatotopic and columnar organization in the corticotectal projection of the rat somatic sensory cortex. Brain Res. 133:223-235.

Woolsey, C.N. (1958) Organization of somatic sensory and motor areas of the cerebral cortex. In. H.F. Harlow and C.N. Woolsey (eds): Biological and Biochemical Bases of Behavior. Madison: Univ. of Wisconsin Press, pp. 63-81.

Woolsey, C.N., P.H. Settlage, D.R. Meyer, W. Spencer, T.P. Hamuy, and A.M. Travis (1950) Patterns of localization in precentral and “supplementary” motor area. A. Res. Nerv. Ment. Dis. Proc. 30~238.

Woolsey, C.N. (ed) (1981) Cortical Sensory Organization. I. Multiple Somatic Areas, NJ: Humara Press.

Woolsey, T.A. (1967) Somatosensory, auditory and visual cortical areas of the mouse. Johns Hopk. Med. J. 121:91-112.

Woolsey, T.A., G. Welker, and R.H. Schwartz (1975) Comparative anatomical studies of the SmI face cortex with special reference to the occur- rernce of “barrels” in layer IV. J. Comp. Neurol. 164t79-94.

Woolsey, T.A., and H. van der Laos (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res. 17205-242.

Yamamoto, T., R. Matsuo, and Y. Kawamura (1980) Localization of cortical gustatory area in rats and its role in taste discrimination. J. Neurophy- siol. 44:440-455.

Yeterian, E.H., and G.W. van Hoesen (1978) Corticostriate projections in the rhesus monkey: The organization of certain corticocaudate connections. Brain Res. 139:43-63.

Yingling, C.D., and J.E. Skinner (1976) Selective regulation of thalmic sensory relay nuclei by nucleus reticularis thalmi. Electroencephalogr. Clin. Neurophysiol. 42:476-482.

Yorke, Jr., C.H., and V.S. Caviness, Jr. (1975) Interhemispheric neocortical connections of the corpus callosum in the normal mouse: A study based on anterograde and retrobTade methods. J. Comp. Neurol. 164:233-246.

Zimmerman, I.D. (1968) A triple representation of the body surface in the sensorimotor cortex of the squirrel monkey. Exp. Neurol. 2Ot415-431.

Date post:	09-Dec-2023
Category:	Documents
Upload:	ucdavis
View:	0 times
Download:	0 times

Regional (14C) 2-deoxyglucose uptake during forelimb movements evoked by rat motor cortex...

Documents