Patterns of Afferent Input to the Caudal and Rostral Areas of ......Patterns of Afferent Input to...

Patterns of Afferent Input to the Caudal and RostralAreas of the Dorsal Premotor Cortex (6DC and 6DR)in the Marmoset Monkey

Kathleen J. Burman,1 Sophia Bakola,1,2 Karyn E. Richardson,1 David H. Reser,1 and Marcello G.P. Rosa1,2*1Department of Physiology, Monash University, Clayton, VIC 3800, Australia2Australian Research Council Centre of Excellence for Integrative Brain Function, Monash University, Clayton, VIC 3800, Australia

ABSTRACTCorticocortical projections to the caudal and rostral

areas of dorsal premotor cortex (6DC and 6DR, also

known as F2 and F7) were studied in the marmoset

monkey. Both areas received their main thalamic inputs

from the ventral anterior and ventral lateral complexes,

and received dense projections from the medial premo-

tor cortex. However, there were marked differences in

their connections with other cortical areas. While 6DR

received consistent inputs from prefrontal cortex, area

6DC received few such connections. Conversely, 6DC,

but not 6DR, received major projections from the pri-

mary motor and somatosensory areas. Projections from

the anterior cingulate cortex preferentially targeted

6DC, while the posterior cingulate and adjacent medial

wall areas preferentially targeted 6DR. Projections from

the medial parietal area PE to 6DC were particularly

dense, while intraparietal areas (especially the putative

homolog of LIP) were more strongly labeled after 6DR

injections. Finally, 6DC and 6DR were distinct in terms

of inputs from the ventral parietal cortex: projections to

6DR originated preferentially from caudal areas (PG and

OPt), while 6DC received input primarily from rostral

areas (PF and PFG). Differences in connections suggest

that area 6DR includes rostral and caudal subdivisions,

with the former also involved in oculomotor control.

These results suggest that area 6DC is more directly

involved in the preparation and execution of motor

acts, while area 6DR integrates sensory and internally

driven inputs for the planning of goal-directed actions.

They also provide strong evidence of a homologous

organization of the dorsal premotor cortex in New and

Old World monkeys. J. Comp. Neurol. 522:3683–3716,

2014.

VC 2014 Wiley Periodicals, Inc.

INDEXING TERMS: frontal cortex; marmoset; connectivity; evolution; motor control

INTRODUCTION

As part of an ongoing effort to understand the func-

tional anatomy of the cerebral cortex in the marmoset

monkey (Callitrhix jacchus), one of the smallest simian

primates, the present study provides a quantitative

analysis of the afferent connections of the dorsal pre-

motor cortex, based on the use of retrograde fluores-

cent tracers. In the most intensively studied primate

species, the premotor cortex (Brodmann’s cytoarchitec-

tural field 6) is formed by several functionally distinct

areas, which are usually grouped into medial, dorsal,

and ventral complexes (e.g., Geyer et al., 2000; Dum

and Strick, 2002; Kaas, 2004; Hoshi and Tanji, 2007).

Within the dorsal premotor complex two principal areas

are recognized, which, according to different nomencla-

tures, are referred to as the caudal and rostral subdivi-

sions of the dorsal premotor cortex (6DC and 6DR;

Barbas and Pandya, 1987; Burman et al., 2006), or

frontal areas 2 and 7 (F2 and F7; Matelli et al., 1985).

Following a recent review of the cortical organization in

the marmoset (Paxinos et al., 2012), and for consis-

tency with our previous studies (Burman et al., 2006,

2008, 2014), we will refer to these areas as 6DC and

6DR. Anatomical and physiological studies in macaques,

K.J.B. and S.B. contributed equally to this study.

Grant sponsor: National Health and Medical Research Council; Grantnumbers: 1020839 and 545865; Grant sponsor: Australian ResearchCouncil; Grant numbers: DP110101200, DP140101968.

*CORRESPONDENCE TO: Prof. Marcello G.P. Rosa, Department of Physi-ology, Monash University, Clayton, VIC 3800, Australia. E-mail:[email protected]

Received December 6, 2013; Revised April 29, 2014;Accepted May 27, 2014.DOI 10.1002/cne.23633Published online May 29, 2014 in Wiley Online Library(wileyonlinelibrary.com)VC 2014 Wiley Periodicals, Inc.

The Journal of Comparative Neurology | Research in Systems Neuroscience 522:3683–3716 (2014) 3683

RESEARCH ARTICLE

capuchins, and owl monkeys have shown that area 6DC

is heavily connected with the primary motor cortex and

spinal cord, and that microstimulation of this region can

elicit movements (Barbas and Pandya, 1987; Ghosh and

Gattera, 1995; Preuss et al., 1996; Dum and Strick,

2005; Stepniewska et al., 2006), highlighting the direct

involvement of this region in the control of movement.

In contrast, area 6DR has been hypothesized to have a

less direct role in motor control, as evidenced by

weaker connections with the primary motor cortex (Bar-

bas and Pandya, 1987; He et al., 1993; Lu et al.,

1994), as well as its functional properties and the

effects of lesions (Petrides, 2005). The present study

uses anatomical tracing to test the hypothesis that mar-

moset areas 6DC and 6DR, identified by previous stud-

ies on the basis of location, cytoarchitecture, and more

limited connectional and physiological evidence (Bur-

man et al., 2008; Reser et al., 2013), are homologous

to the homonymous areas in the macaque (Paxinos

et al., 2009; Fig. 1).

Marmosets belong to the family Callitrichidae, which

diverged from other members of primate radiation over

30 million years ago (Purvis et al., 1995). Since marmo-

sets are increasingly being used as research models in

studies of motor plasticity and recovery after injury,

including neuroprosthetics (Marshall and Ridley, 2003;

Fouad et al., 2004; Virley et al., 2004; Freret et al.,

2008; Yamane et al., 2010; Konomi et al., 2012; Pohl-

meyer et al., 2012, 2014), a more thorough understand-

ing of their cortical motor system is timely. Previous

work has focused on the marmoset primary motor area

(M1; Burish et al., 2008; Burman et al., 2008, 2014),

but little is known about the premotor areas. Whereas

it is clear that the marmoset brain cannot be regarded

simply as a small version of that of larger primates

(Chaplin et al., 2013), studies of sensory cortex have

shown fundamental similarities (e.g., Krubitzer and

Kaas, 1990; Huffman and Krubitzer, 2001; Qi et al.,

2002; Rosa, 2002; Rosa and Tweedale, 2005; Burman

et al., 2006; de la Mothe et al., 2006; Iyengar et al.,

2007; Reser et al., 2009). Furthermore, our previous

study of the cortical connections of marmoset M1 (Bur-

man et al., 2014) detected a high degree of similarity

with the macaque, which supported the idea of a

homologous organization, despite well-documented dif-

ferences in motor abilities between these species (e.g.,

mode of locomotion, as well as the capacity to exert

fine control of hand movements). The present study

provides not only the first quantitative insights into the

organization of the premotor networks in the marmoset,

but also contributes to our understanding of the evolu-

tion of the primate brain, through an analysis of similar-

ities and differences between species with different

brain sizes and motor repertoire.

MATERIALS AND METHODS

Animals and tracer injectionsFluorescent tracers were injected unilaterally into the

frontal cortex of 11 adult marmoset monkeys (see

Table 1 for animal and injection details). The results of

injections placed in the primary motor cortex of some

of these animals have already been described (Burman

et al., 2014), and those of injections in the medial and

ventral premotor areas will be reported separately. All

experiments conformed to the Australian Code of Prac-

tice for the Care and Use of Animals for Scientific Pur-

poses, and were approved by the Monash University

Animal Experimentation Ethics Committee.

The surgical procedures were the same as those

reported in recent studies from this laboratory (Reser

et al., 2013; Burman et al., 2014). Intramuscular (i.m.)

injections of atropine (0.2 mg/kg) and diazepam

(2 mg/kg) were administered as premedication, before

each animal was anesthetized with alfaxalone (10 mg/

kg, i.m.) 30 minutes later. Dexamethasone (0.3 mg/kg,

i.m.) and amoxicillin (50 mg/kg, i.m.) were also admin-

istered prior to positioning the animals in a stereotaxic

frame. Body temperature, heart rate, and blood oxygen-

ation (PO2) were continually monitored and, when nec-

essary, supplemental doses of anesthetic were

administered to maintain areflexia.

To place injections in different regions of the premo-

tor cortex, stereotaxic coordinates were calculated from

Figure 1. Proposed extents of three cortical motor areas in the mar-

moset monkey (top left), compared with the more extensively studied

macaque monkey (bottom right). C, caudal; L, lateral; M, medial; R,

rostral. These reconstructions were prepared (courtesy of T.A. Chap-

lin) with the software CARET (Van Essen et al., 2001), using digitized

representations of stereotaxic atlases of these species (Paxinos

et al., 2009, 2012). Scale bar 5 10 mm. [Color figure can be viewed

in the online issue, which is available at wileyonlinelibrary.com.]

K.J. Burman et al.

3684 The Journal of Comparative Neurology |Research in Systems Neuroscience

http://wileyonlinelibrary.com

previous studies (e.g., Burman and Rosa, 2009). Small

incisions of the dura mater were made immediately

over the intended injection sites to limit exposure of

the brain’s surface. Tracer injections were placed in the

same hemisphere in each animal. The marmoset motor

cortex is less excitable than that of most other primate

species, requiring stronger stimulation currents and lon-

ger search times (Blum et al., 1982; Burish et al., 2008;

Burman et al., 2008). Thus, microstimulation mapping

was not conducted in the current experiments, to mini-

mize surgery times and the risk of complications during

recovery. Instead, postmortem reconstruction was used

to determine the exact placement of each tracer injec-

tion relative to cytoarchitectural and myeloarchitectural

fields (Figs. 2, 3). The location of labeled cells within

the thalamus was also examined (Fig. 4), to yield com-

parisons with the known patterns of projections in

other primate species (Darian-Smith et al., 1990;

Matelli et al., 1996; Stepniewska et al., 2007).

Two fluorescent tracers were used: FluoroRuby (FR;

dextran-conjugated tetramethylrhodamine, molecular

weight 10,000, 15% in water; Life Technologies,

Bethesda, MD) and FluoroEmerald (FE; dextran-

conjugated fluorescein, molecular weight 10,000, 15%;

Life Technologies). Both tracers were injected using a

25 ll constant rate microsyringe (Hamilton, Reno, NV)

fitted with a fine glass micropipette tip (see Table 1 for

details of injection sites). Each tracer was injected over

15–20 minutes (50 nl per deposit at 2-minute intervals;

total volumes were 0.35–0.5 ll), at an initial depth of

�1.5 mm, but in reality distributed along the needle

track throughout the cortical thickness as the pipette

tip was being withdrawn. To minimize tracer reflux, the

pipette was left in place for 5 minutes after the last

deposit. In some of the cases two penetrations of the

pipette were made �0.5 mm apart. Examples of injec-

tion sites created using this protocol have been illus-

trated in recent publications from this laboratory

(Burman et al., 2011b; Reser et al., 2013). After the

injections, the dural flaps were carefully arranged back

over the cortical surface, and then covered with mois-

tened ophthalmic film. The wound was closed in ana-

tomical layers after securing the repositioned excised

bone fragment in place with dental acrylic. Postopera-

tive analgesics were administered immediately after the

animal began to regain consciousness (Temgesic

0.01 mg/kg, i.m.), and for the following 2–3 days (Car-

profen 4 mg/kg, subcutaneous).

Tissue processingAfter a survival time between 14 and 17 days (with

one exception, see Table 1), animals were anesthetized

with alfaxalone (10 mg/kg, i.m.) before being adminis-

tered an overdose of sodium pentabarbitone (100 mg/

kg, i.v.). Immediately upon respiratory arrest they were

perfused through the heart with 1 l of heparinized

saline, followed by 1 l of 4% paraformaldehyde in 0.1 M

phosphate-buffered saline (pH 7.4). The brains were

removed and postfixed in the same medium for up to

24 hours, before immersion in buffered paraformalde-

hyde containing increasing concentrations of sucrose

(10–30%), until sunk. A cryostat was used to obtain 40

lm-thick sections in the coronal plane. Every fifth sec-

tion was mounted unstained for examination of fluores-

cent tracers, and coverslipped with di-n-butyl phthalate

xylene (DPX) following quick dehydration (2 3 100%

ethanol) and immersion in xylene. Adjacent sections

were stained for Nissl substance, cytochrome oxidase,

and myelin, following standard protocols (Gallyas, 1979;

Wong-Riley, 1979). The remaining section in each series

was stored in cryoprotectant solution in a freezer, to be

TABLE 1.

Characteristics of the Animals and Injection Sites

Case Animal Sex Weight (g) Hemisphere Tracer 6D field Stereotaxic coordinates1 Survival (days) n2

1 CJ116 F 339 R FR 6DR AP13.5, ML4.0 17 15912 CJ101 M 430 L FR 6DR AP13.4, ML4.1 15 29243 CJ125 F 333 R FE 6DR AP13.2, ML4.5 17 6564 CJ100 F 365 R FR 6DR AP13.0, ML3.8 14 20895 CJ110 M 356 L FE 6DR AP13.0, ML4.0 17 23056 CJ118 M 296 L FR 6DR/DC AP12.5, ML3.5 1003 9247 CJ112 M 377 L FE 6DC AP12.4, ML3.7 17 40788 CJ115 F 340 R FE 6DC AP12.2, ML3.6 17 14669 CJ123 F 530 L FR 6DC AP12.0, ML4.0 17 51610 CJ111 M 334 L FR 6DC AP11.8, ML3.6 17 200211 CJ126 M 345 L FE 6DC AP11.8, ML4.9 17 367

1Coordinates estimated by comparison with the stereotaxic atlas of Paxinos et al. (2012)2Total number of labeled ipsilateral extrinsic neurons.3This animal had an extended postinjection survival time to allow participation in a behavioral experiment.

Afferent connections of dorsal premotor cortex

The Journal of Comparative Neurology | Research in Systems Neuroscience 3685

used either for BDA histochemistry (area 6M injections

in contralateral hemisphere, to be reported separately),

or as a backup in case of unsatisfactory staining or

damage during processing.

Nomenclature and assignment of injectionsites and labeled cells to different areas

To ascribe injection sites and labeled cells to a

cortical area, histological sections from each animal

were examined using the cytoarchitectural delinea-

tions illustrated by Paxinos et al. (2012) as a guide.

Table 2 provides a full list of the abbreviations of

cortical areas that contained labeled neurons. The

cortical areas portrayed in the Paxinos et al. (2012)

atlas incorporate a large amount of physiological and

neuroanatomical information obtained in previous

studies (e.g., de la Mothe et al., 2006; Burman et al.,

2006, 2011a,b, 2014; Burman and Rosa, 2009; Rosa

et al., 2009, Reser et al., 2013, among others), and

therefore represent the most comprehensive scheme

currently available for the marmoset. In addition, the

Figure 2. A,B: Cytoarchitectural characteristics of areas 6DR and 6DC in coronal sections stained for Nissl substance (medial to the left).

In A, a poorly defined layer IV and small cells in layer V give area 6DR a homogeneous appearance. Arrowheads indicate the approximate

location of borders. Enlarged section of area 6DR is shown on left. In B, a more caudal section through area 6DC shows the presence of

large cells in layer V. Enlarged section of area 6DC is shown on left. Scale bars 5 1 mm, left; 200 lm, right.

K.J. Burman et al.


histological analysis that led to the proposed cortical

areas in the frontal, parietal, and temporal lobes were

performed by the same experts that prepared a highly

used atlas of the macaque (Paxinos et al., 2009),

thereby ensuring consistency in criteria and nomen-

clature. Nonetheless, at this stage, it is important to

recognize that much research still needs to be done,

in order to establish firm homologies with areas pres-

ently recognized in other primate species, including

the macaque. While architectonic features and topo-

logical relationship to other areas (the main criteria

used for identification of many of the marmoset

areas) are important, ideally these need to receive

support from functional and connectional data; the

latter are still lacking, or are limited, for many of the

areas currently proposed. This caveat needs to be

kept in mind in the present analysis.

Architectural characteristics of areas 6DCand 6DR

In the marmoset, area 6DR (Fig. 2A) has a poorly

defined granular layer, unlike the rostrally adjacent area

8aD, where the granular layer is somewhat thin, but

sharply defined (Burman et al., 2006). 6DR is also distinct

from caudally adjacent area 6DC, which is agranular. Area

6DR lacks the large layer V neurons that characterize area

6DC in Nissl preparations (Fig. 2B), leading to an overall

poorly differentiated lamination in low-power views. Myelin

staining in 6DR is homogeneous from the white matter to

the middle of layer III, but myelination is lighter than that

in area 6DC (Fig. 3A,B; see also Burman et al., 2006). Area

6DR is bounded medially by area 8b, which has a broader

granular layer with gradual upper and lower limits (Burman

et al., 2006), and by area 6M, which has lighter staining

for myelin and shows an incipient separation between the

inner and outer bands of Baillarger, together with charac-

teristic large bundles of thick myelinated fibers fanning

out from the white matter, in the lower layers (Fig. 3B).

The histological characteristics of area 6DC are illus-

trated in Figures 2B and 3B. This area is agranular and

has scattered large neurons in layer V, but these are

not as large as those located in M1 (Burman et al.,

2008). The myelination of the two areas is also subtly

different: in M1 there is an incipient separation

between the inner and outer bands of Baillarger, which

is not present in area 6DC (Burman et al., 2006, 2014).

Myelination in area 6DC is also distinct from that in

medially adjacent area 6M (see above for description).

Laterally, area 6DC is bounded by area 8C, an architec-

turally distinct wedge-shaped field that inserts between

the dorsal and ventral premotor complexes (Paxinos

et al., 2012). Injections in area 8C led to a distinct pat-

tern of connections, particularly with extrastriate visual

areas (data to be reported separately).

Data analysisZeiss Axioplan 2 or AxioImager epifluorescence micro-

scopes fitted with 310 or 320 dry objectives were

used to examine sections for fluorescence labeling. The

locations of labeled neurons within the cortex and sub-

cortical structures were mapped in sections at 200-lm

intervals throughout the brain using a digitizing system

(MD Plot3, Accustage, Shoreview, MN) attached to the

microscope. Only clearly recognizable cell bodies, usually

with a discernable nucleus, were accepted as valid (see

Burman et al., 2011a). The locations of subcortical

labeled neurons were mapped, but these were not quan-

titatively analyzed as part of the present study.

The injection sites were defined as two concentric

zones, and we adopted the conservative view that

Figure 3. A,B: coronal sections stained for myelin using the Gal-

lyas (1979) technique (medial to the left). In A, the myelination

pattern of area 6DR is homogeneous to the middle of layer III,

and darker than medially adjacent area 8b, but overall less dense

than in laterally adjacent area 8aV. In B, the denser and more

homogeneous myelination of area 6DC is apparent, while area

6M has bundles of radial fibers running across the infragranular

layers, and area 8C is distinct as a patch of slightly denser myeli-

nation. Arrowheads indicate the approximate location of borders.

Scale bar 5 1 mm.



Figure 4.

K.J. Burman et al.


tracer uptake may occur in both zones. The inner dark

region depicted in the figures indicates brightly fluo-

rescing cortex where dye is present in the extracellular

space immediately surrounding the needle track

(Schmued et al., 1990). The light outer region indicates

cortex where numerous cell bodies were brightly

labeled. Any injection sites that invaded the white mat-

ter were excluded from analysis, and are not consid-

ered in the present report. However, some of the

injection sites (e.g., Fig. 8) did not extend across all

cortical layers. This limitation should be kept in mind as

a possible source of variation across cases of injections

in the same area.

Tracer injection sites always result in a disruption of

the cytoarchitecture of the cortex, which often makes it

difficult to judge fine details such as columnar structure

and neuronal size in their immediate neighborhoods.

Keeping this limitation in mind, assignment of injection

sites to specific areas required examination of many

adjacent sections, both rostral and caudal, and interpo-

lation of areal boundaries through disrupted zones. This

interpolation was further informed by examination of

mirror-symmetrical sites in the opposite hemispheres,

as well as earlier observations about the shape and

spatial relationship between areas in normal animals

(Burman et al., 2006, 2008; Burish et al., 2008; Burman

and Rosa, 2009; Paxinos et al., 2012).

The distribution of labeled neurons throughout the

cortex was visualized using 3D and 2D computer

graphic reconstructions. The 2D surface models were

created by manually tracing mid-thickness contours

from each section, resulting in a series of contours that

were then reconstructed into a 3D triangular mesh,

using the program CARET (Van Essen et al., 2001). The

locations of labeled neurons were added by extracting

their coordinates from the MDPlot data files using

CARET, and projection to the nearest polygon in the

mesh. Finally, the 3D surface was computationally flat-

tened using CARET.

The Kendall coefficient of concordance (W; Siegel,

1956) was employed to compare the distribution of

tracer injections across putative target areas. This anal-

ysis also implicitly tests the consistency of tracer injec-

tions into the same target area in different animals,

which may vary due to differences in injection volume,

tracer type, and/or survival time across cases. The

method was described in detail in Reser et al. (2013),

and has been employed in other recent studies of mar-

moset and macaque cortical connections (Bakola et al.,

2013; Burman et al., 2014). Briefly, we divided the

�120 architectonic areas of the marmoset neocortex

(Paxinos et al., 2012) into a smaller number of anatomi-

cal sectors, which not only reduced the dimensionality

of the dataset, but also partially corrected for areas

with zero or low cell counts. Kendall’s W is a computa-

tionally simple nonparametric measure, which allows for

direct comparison of multiple correlations, with post-

hoc testing by computation of partial W coefficients

(Legendre, 2005). The test statistic expresses the

agreement between the respective correlations of k

individual variables, facilitating assessment of interjudg-

ment or intertest reliability. The W coefficient repre-

sents the divergence of actual agreement between

variables from the idealized perfect agreement (Siegel,

1956), as represented by the calculated ranks (cell

counts) of labeled cells in each sector, for each target

region receiving multiple tracer injections (6DR or 6DC).

The W statistic is calculated as:

W5s

112

k2 N32Nð Þ½ �

where s 5 sum of squares of observed deviations from

100% agreement; k 5 number of sets of rankings

("observers"); and N 5 number of sectors (Siegel, 1956,

Figure 4. Coronal sections showing distribution of labeled cells in thalamic nuclei in cases 1, 5, and 10 (medial to the left). Abbreviations

(from Paxinos et al., 2012): 3n: oculomotor nerve; AD: anterodorsal nucleus; AM: anteromedial nucleus; AV: anteroventral nucleus; CL:

centrolateral nucleus; CM: central medial nucleus; CMn: centromedian nucleus; DLG: dorsal lateral geniculate nucleus; fr: fasciculus retro-

flexus; Hb: habenular nucleus; IAM: interanteromedial nucleus; LD: laterodorsal nucleus; MD: mediodorsal nucleus; MB: mamillary body;

mt: mamillothalamic tract; PC: paracentral nucleus; PH: posterior hypothalamic nucleus; Rt: reticular nucleus; Sthal: subthalamic nucleus;

VAL: ventral anterior nucleus, lateral part; VAM: ventral anterior nucleus, medial part; VLD: ventrolateral nucleus, dorsal part; VLLa: ventral

lateral nucleus, lateral part; VLM: ventral lateral nucleus, medial part; VPI: ventral posterior nucleus, inferior part; VPL: ventral posterior

nucleus, lateral part; VPM: ventral posterior nucleus, medial part; ZI: zona incerta. A–D: After an injection in the rostral part of area 6DR,

labeled cells are distributed as dorsoventral lamellae in the VAL and VLM nuclei, where they are most densely distributed dorsally. In VAL,

labeled cells generally occupy a medial position. Labeled cells are also present dorsally in VAM, in dorsal intralaminar nuclei, and laterally

and posteriorly in the MD nucleus. E–H: The distribution of labeled cells is similar after an injection in the caudal part of 6DR, but there

appears to be more spread into lateral VAL, ventral VLM, and VLLa. I–L: Following an injection in area 6DC, labeled cells are distributed

as dorsoventral lamellae in VAL, VLLa, and lateral VLM. Labeled cells are concentrated dorsally in VLLa and VLM, but do not occupy the

most dorsal part of VAL. Labeled cells are predominantly ventrally located in intralaminar nuclei, and are much more sparsely distributed

in MD. Triangles 5 FR labeled cells, squares 5 FE labeled cells. Scale bar 5 1 mm in L, applies to all.



TABLE 2.

Cortical Areas That Contained Labeled Neurons After Injections Restricted to Area 6DR (cases 1–5) or Area 6DC (Cases 7–

11), and the Percentages of the Extrinsic Labeled Neurons They Contained1

Abbreviation Designation Case 1 Case 2 Case 3 Case 4 Case 5 Case 7 Case 8 Case9 Case 10 Case 11

10 Cytoarchitectural area 10 — 0.7 — 0.4 0.1 — — — — —9 Cytoarchitectural area 9 0.4 — 0.5 0.4 — — — — — —32 Cytoarchitectural area 32 0.3 0.1 — 0.1 —11 and 13 Cytoarchitectural areas 11

and 13— 0.1 0.3 0.2 * *2 — — — —

46 Cytoarchitectural area 46 0.4 1.2 — 2.9 1.0 0.2 * 0.4 — —12 Cytoarchitectural area 12 0.4 2.5 1.5 2.1 * — — — — —45 Cytoarchitectural area 45 * 0.1 — 0.3 — — — — — —PrCO Precentral opercular cortex — 0.3 — 0.7 * — — 0.2 0.1 0.38b Cytoarchitectural area 8B 14.4 7.6 16.8 9.3 10.9 0.2 * — 0.2 —8aD Cytoarchitectural area 8a

dorsal9.4 11.9 12.2 1.2 1.3 * * — 0.2 —

8aV Cytoarchitectural area 8aventral

1.3 2.3 — 1.7 0.5 — — — — —

8C Cytoarchitectural area 8caudal

6.6 2.0 3.5 3.3 5.9 0.3 0.3 5.0 1.6 —

6DR Cytoarchitectural area 6dorsorostral

— — — — — 17.9 19.2 4.5 4.0 —

6DC Cytoarchitectural area 6dorsocaudal

1.7 1.3 1.1 13.7 15.7 — — — — —

6M Cytoarchitectural area 6medial

1.1 3.1 1.5 20.5 19.7 26.7 24.2 23.1 23.6 12.3

6Va Cytoarchitectural area 6ventral, subdivision a

0.3 0.5 0.5 2.3 1.7 0.4 0.4 0.2 0.4 2.7

6Vb Cytoarchitectural area 6ventral, subdivision b

* 0.1 0.2 0.4 0.1 — — — — 0.8

M1 Primary motor area — — — 0.2 0.2 15.7 15.5 10.1 31.8 21.524a/b Cytoarchitectural area 24,

subdivisions a and b0.8 0.6 — 0.9 * 0.6 0.6 2.7 1.2 0.3

24c Cytoarchitectural area 24,subdivision c

0.3 — — 1.0 1.1 1.5 3.8 0.4 1.8 0.8

24d Cytoarchitectural area 24,subdivision d

0.2 — — * 0.4 1.1 4.2 — 0.7 —

23a/b Cytoarchitectural area 23,subdivisions a and b

15.1 18.7 7.5 13.7 12.6 1.1 5.9 1.6 1.0 —

23c Cytoarchitectural area 23,subdivision c

— — — — * — — — — —

23V Cytoarchitectural area 23,ventral subdivision

0.8 2.5 — 0.4 — — — — — —

31 Cytoarchitectural area 31 5.0 0.9 6.0 0.9 10.4 5.5 1.8 6.2 1.1 0.329 Cytoarchitectural area 29 3.7 6.2 1.5 1.6 0.7 * — — * 0.330 Cytoarchitectural area 30 4.0 5.3 3.5 1.7 0.3 * — — 0.1 —3a Cytoarchitectural area 3a — * — * * * 0.5 1.4 0.4 1.13b Cytoarchitectural area 3b * — — — — 0.3 * — — 1.61/ 2 Cytoarchitectural areas 1

and 2— * — * 0.1 4.6 2.0 15.1 5.6 21.5

PV Parietal ventral somatosen-sory area

— — — 0.3 0.1 — — — — —

S2 Second somatosensoryarea

0.1 — — 2.0 1.1 0.7 1.1 3.5 1.0 3.5

GI Insular cortex, granular * — — 0.8 * — — — — —DI Insular cortex, dysgranular — * — — — — 0.1 0.6 — —ReI Retroinsular area — — — * — 0.1 0.3 — * 0.3PE Cytoarchitectural area PE 2.7 0.7 0.8 0.4 7.9 22.4 18.4 18.2 22.2 27.3PEC Cytoarchitectural area PE,

caudal0.3 0.3 0.6 — 1.5 — 1.0 3.3 1.9 —

PF Cytoarchitectural area PF — — — 0.6 0.2 * — 1.4 0.4 1.9PFG Cytoarchitectural area PFG 1.1 0.2 1.5 1.9 0.7 0.5 0.4 1.7 — 2.5PG/OPt Cytoarchitectural areas PG

and OPt4.9 2.2 3.5 0.9 0.3 — — — * —

AIP Anterior intraparietal area 0.3 0.3 6.1 0.1 0.3 — — — — —

K.J. Burman et al.


eq. 9.15). We first assessed the concordance of results

from tracer injections into the same target in different

cases with respect to the anatomical sector, confirming

that there was substantial agreement between injec-

tions into the same area. Cell counts from each target

area were then pooled and compared to assess con-

cordance across areas.

We also analyzed the laminar distribution of labeled

cells by examining the proportion of labeled neurons

located in the supragranular layers, as a percentage of

the total number of labeled neurons in a given area

(%SLN; Barone et al., 2000). For the analysis, we used

only projections that comprised 50 or more neurons,

visualized across all cases, to avoid bias introduced by

small samples. In our previous studies this method has

revealed the laminar features that are most consistent

across cases (Burman et al., 2011a, 2014).

RESULTS

Injection sitesThe following report describes the results of 11

tracer injections placed in different parts of the dorsal

premotor cortex of the marmoset (Table 1). As shown

in the flat reconstructions shown in Figure 5, the sam-

ple includes five injection sites that we regarded as

located completely within area 6DR (CJ116-FR, CJ101-

FR, CJ125-FE, CJ100-FR, and CJ110-FE), five injections

within area 6DC (CJ112-FE, CJ115-FE, CJ123-FR, CJ111-

FR, and CJ126-FE), and one injection that was primarily

located in area 6DC, but probably crossed slightly into

6DR (CJ118-FR). For convenience, these are referred to

below as cases 1–11, numbered from rostral to caudal.

Thalamic connectionsThe thalamic projections to areas 6DR and 6DC in the

marmoset resembled those previously reported for the

macaque (Matelli et al., 1996), with a few small differen-

ces. The distribution of labeled cells in thalamic nuclei after

rostral 6DR injections was similar for cases 1–3 (data from

case 1 are shown in Fig. 4A–D and Fig. 8G,H). Labeled cells

were distributed as dorsoventral lamellae in the lateral part

of the ventral anterior nucleus (VAL), and medial part of the

ventral lateral (VLM) nucleus. In both nuclei, the labeled

cells were most densely distributed dorsally. In the VAL,

labeled cells generally occupied a medial position. Labeled

cells were also present dorsally in the medial part of the

ventral anterior nucleus (VAM), dorsally in the intralaminar

nuclei (e.g., the centrolateral [CL] and paracentral [PC]

nuclei), and posterior/ laterally in the mediodorsal nucleus

(MD). The distribution of labeled cells in cases 4 and 5

TABLE 2. Continued

Abbreviation Designation Case 1 Case 2 Case 3 Case 4 Case 5 Case 7 Case 8 Case9 Case 10 Case 11

MIP Medial intraparietal area 2.3 5.2 0.9 0.1 1.1 — * — 0.3 —VIP Ventral intraparietal area 1.2 1.1 2.7 0.2 0.7 — — 0.2 0.2 —LIP Lateral intraparietal, lateral 9.5 4.8 18.0 0.3 0.4 — * — — —MST Medial superior temporal

area0.1 0.7 — 1.0 0.2 — — — — 0.3

MTC Middle temporal crescent 0.2 0.6 0.3 0.1 — — — — — —FST Fundus of the superior

temporal sulcus area0.2 1.2 — 1.4 0.4 — — — — —

STP Superior temporal polysen-sory areas

0.6 3.4 0.2 1.7 0.3 — — — * —

V6a Visual area 6a 0.1 * — 0.3 — — — — * —TE/TEO Temporal areas TE and

TEO1.3 1.1 1.1 1.9 0.4 — — — — —

19M Area 19, medial — 1.0 — 1.3 0.2 — — — — —DA (V3a) Dorsoanterior visual area 0.6 * 0.8 0.1 — — — — — —DM Dorsomedial visual area 0.1 * — 0.1 — — — — —VLA (V4) Ventrolateral anterior visual

area0.1 0.1 0.3 0.1 — — — — — —

VLP (V4) Ventrolateral posterior vis-ual area

— — 0.9 — — — — — — —

V2 Visual area 0.4 0.1 — 0.1 — — — — — —PGM Cytoarchitectural area PG

medial6.8 7.6 6.0 3.3 0.8 — * — * —

TPt Temporoparietal transitionarea

0.2 — — 0.5 0.3 * — 0.4 0.2 0.8

CM Caudomedial auditory area 0.5 0.7 — 0.4 * — — — * —ProSt Area prostriata 0.1 0.4 — 0.1 — — — — — —

1For equivalence between these designations and other commonly used nomenclatures of cortical areas, see Reser et al., 2013.2Asterisks indicate areas where the labeled cells accounted for <0.1% of the extrinsic label. In some cases, this corresponded to single, but well-

defined labeled cells.



Figure 5. "Unfolded" dorsal reconstructions of cortical layer IV in all cases, showing the location and extent of all injection sites. These

reconstructions were created using the lateral border of area 6M as a constant zero reference point. The thicknesses of the gray zones

between areas indicate an estimate of the imprecision of the assignment of borders, based on the separation of sections and independent

estimates by two observers. The insert in the bottom right is dorsal view of a marmoset brain (adapted from Paxinos et al., 2012), showing

location of areas included in a representative adult individual (M, medial; R, rostral). As in all illustrations in this article, reconstructions

are shown in an orientation appropriate for the right hemisphere, to facilitate comparisons. Scale bar 5 2 mm.

K.J. Burman et al.


(caudal 6DR injections) was similar, but appeared to

spread further laterally into the ventrolateral complex,

including the lateral part of the ventral lateral thalamic

nucleus (VLLa), as shown for case 5 (Fig. 4E–H; Fig. 10G–

I). Generally, this distribution pattern is similar to that found

in the macaque (Matelli et al., 1996).

The thalamic projections to area 6DC were consistent

among all cases. Labeled cells were distributed as dorso-

ventral lamellae in the VAL, VLLa, and lateral VLM. They

were more densely distributed dorsally in VLLa and VLM

nuclei, but were absent in the most dorsal part of VAL

(e.g., case 10; Fig. 4I–L; Fig. 13H–J). Labeled cells were

not present in the VAM nucleus in any of the 6DC injec-

tion cases. Labeled cells were predominantly located in

the ventral portions of the intralaminar nuclei (primarily

the PC nucleus), and were sparsely distributed in the

posterior MD nucleus. The projections from VAL and MD

were clearly sparser than those observed in the 6DR

injection cases. The distribution patterns of labeled cells

following injections in area 6DC were similar to those

Figure 6. Summary of the ipsilateral areas that sent projections to areas 6DR and 6DC, shown in a computerized reconstruction of corti-

cal layer IV of a template marmoset brain (Paxinos et al., 2012). A,B: Lateral view is shown at the bottom and the medial view at the top

(rostral to the right). A: Illustrates areas sending projections to area 6DC, and B shows the areas sending projections to area 6DR. Areas

indicated in colored shading are those which contained an average of >1% of labeled neurons, and other labeled areas indicate lesser pro-

jections. Black represents the injected area, in which labeled cells (intrinsic connections) were not counted. C: Summary of the density of

the ipsilateral connections in each of the cases of injections restricted to 6DC or 6DR, represented as percentage of the total number of

extrinsic connections (see color scale bar). In some cases, functionally related areas were grouped for this analysis. [Color figure can be

viewed in the online issue, which is available at wileyonlinelibrary.com.]




reported for the macaque (Matelli et al., 1996) after

injections in F2. However, the macaque data appeared to

show comparatively sparser label within the VA nuclei,

and denser label in the intralaminar and MD nuclei.

Summary of the patterns of corticalafferents

Figure 6 highlights the cortical areas that sent the

main projections to the dorsal premotor areas of the

Figure 7. Percentages of labeled neurons located in different cortical areas or groups of adjacent areas, after 11 retrograde tracer injec-

tions in the dorsal premotor areas. Top: results from injections in area 6DR; Bottom: results from injections involving area 6DC. Results

from individual cases are indicated by color, according to the legends shown on the top right of each panel. The black bars in the bottom

graph indicate results from an injection that slightly invaded area 6DR. For purposes of illustration, some projections from functionally

related areas were grouped. The column labeled “Visual” indicates all projections from visual areas (MST, MTC, FST, TE, 19M, DA, DM,

V2, VLA, and VLP), and “Insula” indicates combined projections from the dysgranular and granular insular areas, as well as the retroinsular

area. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

K.J. Burman et al.



Figure 8. A–L: Coronal sections through the brain of case 1, showing the locations of labeled neurons (black triangles) relative to various

areas. The anteroposterior level of each section is indicated. Inset (bottom right): lateral view of the brain, showing the levels of the sec-

tions. Scale bar 5 2 mm.



marmoset. Colors indicate areas contributing �1% of

the total extrinsic ipsilateral projection to area 6DC

(Fig. 6A) or 6DR (Fig. 6B), when averaged across cases,

while the dashed outlines indicate areas that originated

sparse projections (i.e., projections that were <1% of

the extrinsic labeled neurons, averaged across cases).

The density of projections observed in each case is

summarized in Figure 6C. The key finding is that there

were significant differences between the afferent con-

nections of 6DC and 6DR. For example, with respect to

the frontal lobe afferents, even a cursory analysis of

Figure 6C reveals that projections from the prefrontal

cortex preferentially targeted area 6DR, while projec-

tions from motor areas M1 and 6M targeted area 6DC

more densely. Moreover, while area 6DC receives the

bulk of its parietal connections from the putative homo-

log of area PE, 6DR receives from a wider variety of

parietal sources, including, in particular, the putative

lateral intraparietal area (LIP; Rosa et al., 2009; Paxinos

et al., 2012; Reser et al., 2013). Sensory afferents to

area 6DC originated primarily from somatosensory

areas, while 6DR received sparse connections from a

wider variety of visual areas.

Quantitative aspects of the patterns of label result-

ing from all 11 injections are summarized in Figure 7,

where the results are presented as percentages of

labeled neurons observed in different cortical areas, or

groups of functionally related areas. This analysis only

included ipsilateral extrinsic projections. A comprehen-

sive list of all connections observed is presented in

Table 2, in this case including all areas where very

small numbers of labeled cells were observed.

Together, these representations illustrate both the

main consistent patterns observed, and also the varia-

tion between cases (including minor projections; Mar-

kov et al., 2013, 2014).

Figure 9. Pattern of label resulting from an injection in the rostral part of area 6DR (case 1), visualized in computer graphic reconstruc-

tions of the cortex prepared with the program CARET (Van Essen et al., 2001). Left: "unfolded" view of the cortex. The gray shading repre-

sents curvature: convex (outward-projecting) surfaces such as dorsal midline and the lips of the lateral fissure appear lighter than the gray

background, whereas concave (inward-projecting) surfaces such as the banks of the lateral fissure appear darker than the background.

Several discontinuities were introduced along the perimeter of the cortex, to reduce distortions (see Reser et al., 2013 for full details). D:

dorsal, R: rostral. Red symbols represent individual neurons labeled with FR, the center of the injection site is indicated by a black circle,

and the approximate extent of area 6DR by yellow shading. For orientation, the locations of several areas containing labeled neurons are

indicated (abbreviations as in Table 2). Right: Lateral (bottom) and medial (top) views of the 3D model used to generate the flat map, with

the density of labeled neurons indicated relative to the maximum count observed in a node of the mesh in this case. Scale bar 5 5 mm.

[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

K.J. Burman et al.



Figure 10. A–L: Coronal sections through the brain of case 5, showing the locations of labeled neurons (black squares) relative to various

areas. The anteroposterior level of each section is indicated. Inset: lateral view of the brain, showing the levels of the sections. Scale

bar 5 2 mm.



Cortical inputs to area 6DRFive injection sites were localized to area 6DR. As

shown in Figures 6C and 7, the injections in cases 1–3

revealed similar percentages of labeled cells in different

areas, while cases 4 and 5, located more caudal and

medially within 6DR, revealed a slightly different pat-

tern, characterized by greater quantitative emphasis on

motor and somatosensory projections, and fewer pro-

jections from intraparietal areas (see also Table 2).

These observations are compatible with the existence

of rostral (oculomotor) and caudal (predominantly soma-

tomotor) subdivisions in area 6DR, a result that resem-

bles observations in the macaque by Luppino (2003).

To demonstrate the common and variable features of

the connections of sites within area 6DR, we illustrate

in detail data from rostral (case 1, in Figs. 8, 9) and

caudal injections (case 5, in Figs. 10, 11). Summaries

of the data obtained in the other three cases are shown

in Figure 12A–C.

In all three rostral cases, labeled neurons were observed

in many prefrontal areas. The area 8 complex provided the

strongest connections, which originated predominantly

from areas 8b and 8aD (Figs. 8B,C, 9, 12A,B). In area 8b,

labeled cells were distributed according to a rostrocaudal

gradient, being concentrated primarily in the caudal part of

this area (Fig. 9). Area 8aV, which overlaps in part with

the marmoset’s frontal eye field (Burman et al., 2006;

Reser et al., 2013), had much sparser connections (Fig.

8C). Small numbers of labeled cells were also observed in

prefrontal areas 46 and in the lateral part of area 12 in

most cases involving rostral 6DR injections (Figs. 8A, 9,

12A,B). Inputs from areas 10, 9, 11, 13, 32, and 45 were

very sparse, and less consistent. A projection was also

observed from the precentral opercular cortex (PrCO); this

projection consisted of isolated cells in most cases, but

was more obvious in case 2 (Fig. 12A).

In premotor cortex, intrinsic connections within area

6DR were quite dense and widely distributed mediolat-

erally throughout its rostrocaudal extent. Inputs origi-

nated from other premotor areas (6M, 6DC; Fig. 8D,E),

as well as from area 8C (a wedge-shaped area located

at the ventral border of the dorsal premotor cortex,

identified by Paxinos et al., 2012). In area 6M, labeled

cells occupied a predominantly dorsomedial position on

the hemisphere and were concentrated in approxi-

mately the rostral third of this field (Figs. 9, 12A,B),

which may include the marmoset homolog of pre-

supplementary motor area (pre-SMA, or F6, as dis-

cussed in Burman et al., 2014). In contrast, labeled

cells in area 6DC were located predominantly in its ros-

tral half. While knowledge about the topographic organi-

zation of area 6DC in the marmoset remains

fragmentary (Burish et al., 2008; Burman et al., 2008),

comparison of this distribution pattern with

Figure 11. Pattern of label resulting from an injection in the caudal part of area 6DR (case 5). The green symbols represent individual neurons

labeled with FE. Other conventions as in Figure 9. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

K.J. Burman et al.



observations in the macaque suggests that rostral area

6DR is preferentially targeted by neurons in the fore-

limb representation in area 6DC (He et al., 1993; God-

schalk et al., 1995; Raos et al., 2003). Sparse input

was observed from ventral premotor area 6 (6V), where

most labeled cells were located in cytoarchitectural

subdivision 6Va (Burman et al., 2008; see Fig. 8D). No

labeled neurons could be unequivocally attributed to

area M1.

On the medial wall of the hemisphere, sparse con-

nections from cytoarchitectural areas 24a–d were pres-

ent in cases 1 (Fig. 8E,F, 9), and 2 (Fig. 12A), but were

absent from case 3 (an injection which resulted in rela-

tively fewer labeled cells overall). One of the richest

connections to area 6DR originated in posterior cingu-

late areas 23a–b, with most labeled cells located in

caudal area 23b (e.g., Fig. 8I). Sparse projections from

area 23V (Palmer and Rosa, 2006b) and the ventrally

Figure 12. Patterns of label resulting from three injections in area 6DR (A–C), and one injection that crossed the border between areas 6DR

and 6DC (D). Other conventions as in Figure 9. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]




Figure 13. A–L: Coronal sections through the brain of case 10, showing the locations of labeled neurons (black triangles) relative to vari-

ous areas. Conventions as in Figures 8 and 10.

K.J. Burman et al.


adjacent area prostriata in the anterior calcarine sulcus

(ProSt; Yu et al., 2012) were also present in cases 1

and 2 (Figs. 8L, 9, 12A), but these were not detected

in case 3. Other caudal areas on the medial wall that

sent variable but generally strong inputs to rostral area

6DR were areas 31, PGM and retrosplenial areas 29–

30 (Fig. 8G–K). Collectively, the input to rostral area

6DR from posterior areas on the medial wall was sub-

stantial, in cases 1 and 2 constituting about 40% of the

total ipsilateral extrinsic connection. Despite the lower

number of labeled neurons in case 3, the extrinsic pro-

jections from posterior medial areas were also numer-

ous (nearly 25%).

Projections originating in primary somatosensory

areas (3a, 3b, 1 and 2), and insular cortex were negligi-

ble in cases 1–3. A projection was observed from pos-

terior parietal cytoarchitectural area PE (e.g., Fig. 8I),

where labeled cells were concentrated caudally (Figs. 9,

12A,B). A small number of labeled cells were also

located in cytoarchitectural area PEC (Fig. 8J). Ventral

parietal areas cytoarchitectural PFG, PG, and OPt, as

well as intraparietal areas AIP, MIP, VIP, and LIP (Rosa

et al., 2009) contributed variable, but often substantial

projections to rostral area 6DR; for example, in case 1,

areas PG/OPt and LIP contained clear patches of

labeled neurons (Fig. 8J). Across cases 1–3, the dens-

est projection from the intraparietal cortex originated in

area LIP (Figs. 7, 9, 12A,B), which has been identified

in the marmoset based on myeloarchitecture and con-

nections with visual dorsal stream areas (Rosa et al.,

2009).

Extrastriate visual areas sent very limited projections

to rostral area 6DR. These included the motion-

sensitive areas MST, FST, and MTC (Rosa and Elston,

1998), the peripheral representations of areas VLA and

V2 (Rosa and Tweedale, 2000), occipitoparietal areas

DA and DM (Rosa and Schmid, 1995), medial occipital

area 19M (Palmer and Rosa, 2006b), and cytoarchitec-

tural subdivisions of inferior temporal area TE (Paxinos

et al., 2012; Figs. 9, 12A,B). Labeled cells were also

sparsely distributed in the putative homolog of parieto-

occipital visuomotor area V6a (Figs. 9, 12A; this has

been previously referred to as the medial subdivision of

the posterior parietal cortex, PPm; Rosa et al., 2005).

Finally, the superior temporal polysensory areas (STP,

here defined as comprising cytoarchitectural areas

PGa/IPa and TPO of Paxinos et al., 2012) and the cau-

dal auditory belt region (CM; de la Mothe et al., 2006)

contained labeled neurons, in cases 1 and 2 (Figs. 8,

12A).

Injections in the caudomedial part of cytoarchitec-

tural area 6DR (cases 4 and 5) resulted in a pattern of

label that showed many similarities, but also a few key

differences (Figs. 10, 11, 12C). Most notably, premotor

areas 6M and 6DC sent much stronger projections, in

comparison with those targeting rostral injection sites.

As in the latter, labeled cells were concentrated in the

rostral third of area 6M; however, labeled cells not only

occupied a dorsomedial position, but were also distrib-

uted across the convexity of the hemisphere and onto

the medial wall (Fig. 10D,E). This pattern suggests input

from both forelimb and hindlimb representations of 6M

(Burman et al., 2014). Furthermore, cases 4 and 5 had

the greatest number of labeled cells in the caudal two-

thirds of area 6M. In area 6DC, labeled cells were

located within its rostral half, but unlike in cases 1–3,

were widespread mediolaterally. Inputs from the ventral

premotor cortex were slightly denser than those to ros-

tral area 6DR (e.g., Fig. 10E). Finally, in cases 4 and 5,

a few labeled cells were observed in the lateral part of

M1 (cytoarchitectural subdivision 4c; Fig. 10E), which

includes the face representation (Burman et al., 2008,

2014). Projections from the medial hemisphere were

similar to those seen in cases 1–3, although with a

slightly greater proportion of labeled cells in anterior

cingulate area 24c, where the putative anterior cingu-

late motor field is located in the marmoset (Burman

et al., 2014).

Another difference in the pattern of connections to

caudomedial area 6DR, compared with rostrolateral

area 6DR, was the less prominent projection from area

8aD in the prefrontal cortex. Other prefrontal connec-

tions were variable, but generally similar to that

observed after rostral 6DR injections (Figs. 11, 12C). In

addition, the caudal injection sites received projections

from somatosensory areas S2 (Fig. 10G) and PV (parie-

tal ventral area; Krubitzer and Kaas, 1990). Finally, ven-

tral parietal area PF projected sparsely to caudal area

6DR (Fig. 10H), but not to rostral area 6DR. Conversely,

connections with intraparietal areas AIP, MIP, VIP, and

LIP were sparser.

Despite the differences highlighted above, statistical

comparisons showed that the pattern of connections

across all injections in area 6DR was highly concordant

(W 5 0.78, P< 0.001). Thus, there was no reason to

reject the hypothesis that 6DR is a single area,

although it may have a rostrocaudal functional topogra-

phy that leads to some variation in connections.

Cortical inputs to area 6DCBecause differences between cases of injections in

6DC were not marked (Figs. 6C, 7, Table 2), we will

illustrate in detail one case, and provide summaries of

the data for the other cases. Figure 13 illustrates coro-

nal sections from case 10. A flat reconstruction of the

cortex in this case, as well as lateral and medial views



of the distribution of labeled cells, is shown in Figure

14. For comparison, flat reconstructions of the cortex

for cases 7, 8, 9, and 11 are presented in Figure 15.

An additional case, with an injection that is likely to

have crossed slightly into area 6DR is shown in Figure

12D.

In contrast with 6DR, projections from prefrontal areas

to area 6DC were negligible in all cases. When present,

isolated labeled cells were found in areas 46, 8b, 8aD

(Figs. 7B, 13A, 14, 15). A small but variable projection

originated in area 8C (Figs. 7B, 13B, 14, 15A–C). More

caudally, isolated projection neurons were also found in

area PrCO. In addition, in four cases (7–10) we observed

projections from area 6DR (e.g., Fig. 13B). No labeled

cells were observed in this area in case 11, where the

injection site was located caudoventrally in area 6DC;

however, this may also reflect the overall lower number

of labeled neurons in this case. Labeled cells in area

6DR occupied the same dorsolateral level as the injec-

tion site (Figs. 14, 15), suggesting a parallel topographic

organization. Intrinsically labeled cells in 6DC were dis-

tributed across the entire anteroposterior and mediolat-

eral extents of this area (Figs. 14, 15).

Rich projections to area 6DC originated from motor

areas 6M and M1 (Table 2, Figs. 6C, 7B, 11–13). In

area 6M, the main concentrations of labeled cells were

located in the caudal half, including the dorsal convex-

ity of the hemisphere in cases 7–10 (e.g., Fig. 13B–D),

and also the medial wall in cases 7–8. In M1, the dens-

est concentration of cells occupied a similar dorsolat-

eral position to the corresponding injection sites (Figs.

14, 15). In cases 7, 8, and 10, a small number of

labeled cells were also found medially on the convexity

of the hemisphere and on the medial wall in the histo-

logically defined M1 hindlimb field (e.g., Fig. 13F). In

cases 7 and 8, isolated labeled cells were also

observed in the lateral part of M1 (face representation

field); however, across cases, most of the M1 projec-

tion occupied the intermediate M1 forelimb representa-

tion field.

In all area 6DC cases, only sparse label was found in

area 6V, with these cells being found almost exclusively

in cytoarchitectural subdivision 6Va (Table 2, Figs. 13B,

14, 15). Case 11, the most lateral injection in 6DC (Fig.

15D), showed the strongest proportional input from 6V

(Fig. 7) and was the only case in which we observed

isolated labeled cells in cytoarchitectural subdivision

6Vb.

Projections from areas on the medial wall of the

hemisphere were somewhat variable across cases

(Table 2, Fig. 7B). In contrast with injections in area

6DR, distinct clusters of labeled cells were commonly

Figure 14. Pattern of label resulting from an injection in area 6DC (case 10). The red symbols represent individual neurons labeled with

FR. Other conventions as in Figure 9. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

K.J. Burman et al.



found in the anterior cingulate cortex (areas 24b–d; Fig.

13E,F), which includes the putative anterior cingulate

motor area (Burman et al., 2014). However, in cases 9

and 11 label was not present in area 24d, which

encompasses the putative hindlimb representation field

(Burman et al., 2014), mirroring the topographic distri-

bution of label in M1. Other clusters of labeled neurons

were consistently observed within the limits of the pos-

terior cingulate areas 23a and 23b, and in area 31

(Figs. 7, 13K,L). In another significant difference from

the 6DR injection cases, only isolated labeled cells

were found in retrosplenial areas 29 and 30, and in the

putative homolog of medial parietal area PGM (defined

by cytoarchitecture according to Paxinos et al., 2012).

Figure 15. Patterns of label resulting from four injections in the medial half of area 6DC (A–D) and one injection in the caudolateral part of area

6DC (E). The injection site in case 6 (A) slightly invaded area 6DR. The red or green symbols represent individual neurons labeled with FR or FE,

respectively. Other conventions as in Figure 9. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]




The distribution of labeled cells from areas on the

medial wall was most restricted in case 11 (Fig. 15D),

with a caudoventral injection site. In this case, sparsely

distributed cells were located only in areas 24b, 31 and

29.

In primary somatosensory areas, labeled cells were

most numerous in area 1/2 (a single cytoarchitectural

field that, in the marmoset, probably includes the

homologs of macaque areas 1 and 2; Paxinos et al.,

2012; e.g., Figs. 13H,I, 14). However, the percentages

of labeled cells in this area were variable, being particu-

larly high in cases 9 and 11 (Fig. 7B). Labeled cells

were distributed in area 1/2 at a similar mediolateral

position as the injection sites. Connections with areas

3a and 3b were always sparse (e.g., Fig. 13G), while a

small but consistent projection was observed from S2

(Table 2, Figs. 7B, 13I,J). In the insular cortex, isolated

labeled cells were found only in granular and retroinsu-

lar regions of some cases (Table 2).

More caudally in parietal cortex, a consistently rich

projection originated in posterior parietal area PE,

defined by cytoarchitecture according to Paxinos et al.

(2012; e.g., Fig. 13J,K). Labeled cells were most com-

monly found in the rostral half of this region. These

neurons were located dorsomedially and, with the

exception of case 11, distributed also on the convexity

of the hemisphere (Figs. 14, 15). In cases 8–10, the

labeled zone extended into the putative homolog of

area PEC (Fig. 13L). In all cases, cytoarchitectural ven-

tral posterior parietal areas PF and PFG provided sparse

or minor inputs (Fig. 13H), with the densest projections

occurring in cases 9 and 11 (Fig. 7). Very sparsely dis-

tributed labeled cells were also found in intraparietal

areas, these being primarily found in cases 8–10 (e.g.,

Fig. 13L), an observation which contrasted with the pat-

tern observed after injections in area 6DR. In addition,

almost no input was observed from extrastriate areas,

with the exception of isolated cells in MST and V6a

(Table 2), or from STP. Isolated labeled cells were found

in cytoarchitectural area TPt of cases 10 and 11 (e.g.,

Fig. 13J).

In case 6, the injection site was located rostrome-

dially within area 6DC, but also most likely extended

into caudomedial area 6DR (Fig. 12D). The distribution

pattern of labeled cells in this case was generally simi-

lar to that observed for cases 7–11, but was peculiar in

some respects. Labeled cells were located throughout

area 6DR, albeit becoming sparser at rostral levels,

probably reflecting intrinsic connections. There were

also fewer labeled cells in M1, in comparison with other

cases of 6DC injection, but this may have been due to

unintentional damage to this area incurred during the

surgical procedure.

Statistical comparisons showed that the pattern of

connections in cases 7–11 (cases in which the injec-

tions were restricted to area 6DC) was highly concord-

ant (W 5 0.59, P< 0.001), in agreement with the

hypothesis that these injections were all located in the

same cortical area.

Contralateral cortical connectionsTable 3 summarizes the interhemispheric connections

observed after injections in 6DC and 6DR, using only

cases in which the injection sites were confirmed as

being contained within each area. The majority of the

labeled cells in the contralateral hemisphere were

TABLE 3.

Interhemispheric Input to Area 6D: Areas of Origin and

Percentages of Labeled Neurons

Labeled area Cases 1–5 Cases 7–11

10 *1 —9 0.2 —32 *11 * —46 0.7 *12 0.3 —45 * —PrCO 0.2 —8b 16.9 *8aD 4.2 *8aV 0.4 —8C 5.0 0.86M 12.6 30.86DR 48.8 11.36DC 3.3 40.26Va 2.6 0.16Vb * —4 0.4 6.124a/b 0.5 2.424c 1.0 4.124d * 3.123a/b 0.3 0.2PGM 0.2 —3a * *1/2 * *PV 1 S2 0.3 —DI * —ReI — *PE * 0.5PG/OPt 0.5 —PFG 0.2 —AIP * —VIP * —LIP 0.5 —MST/MTC * —Prostriata * —29 0.2 —30 0.2 —31 * —TPt * —

1Asterisks indicate areas where the labeled cells accounted for

<0.1% of the interhemispheric label.

K.J. Burman et al.


observed in homotopic regions of the same area.

Another major interhemispheric connection originated

in area 6M, preferentially targeting area 6DC, but also

projecting strongly to area 6DR. Contralateral ventral

premotor area 6V projected mainly to area 6DR, while

contralateral M1 favored area 6DC. Other significant

projections to area 6DR originated in areas 8b, 8aD

and 8C. On the medial wall, anterior cingulate areas

24a–d sent contralateral projections to area 6DR and

to area 6DC, the latter receiving stronger inputs.

Other contralateral projections were sparse, and also

originated from many of the same areas that sent ipsi-

lateral projections. For example, area 6DR received

sparse contralateral inputs from frontal areas 9, 46, 12,

8aV, and PrCO; caudal medial wall areas 23a/b and

PGM; parietal areas S2, PFG, PG/OPt, and LIP; and ret-

rosplenial areas 29, 30, and 31. Area 6DC received

sparse contralateral inputs from fewer areas, including

46, 8b, 8aD, 8C, 6Va, 23a/b, 3a, 1/2, PE, and ReI.

Laminar distributionsThe laminar distribution of labeled cells is summar-

ized in Table 4. For this analysis we pooled the results

of the five cases with injections within the borders of

area 6DR, and separately, the five cases with injections

confined to area 6DC. In our sample, the projections to

both areas were found to originate predominantly from

supragranular layers. However, the projections from

areas 6DC, 6M, and ventral cingulate areas 24a/b to

area 6DR consisted of relatively balanced numbers of

neurons in supra- and infragranular layers, which are

usually interpreted as lateral connections between

areas at a same hierarchical level (Grant and Hilgetag,

2005).

DISCUSSION

We compared the afferent connections of dorsal pre-

motor areas 6DC and 6DR in the marmoset monkey.

Based on location, cytoarchitecture, and previous stud-

ies of connections with frontal and parietal areas, we

hypothesized that these areas are homologous to 6DC

and 6DR (F2 and F7) described in the macaque (Fig. 1).

The issue of homologies between species is a thorny

one, as comprehensive information may not be avail-

able for the different species being compared. In addi-

tion, the concept of homology is based on common

developmental and evolutionary origin, not identical

morphology or physiological function (importantly,

homologous areas do not need to be identical in all

respects). For example, other studies have highlighted

examples of more extensive networks of corticocortical

connections in the marmoset, compared to macaque

(Palmer and Rosa, 2006a; Burman et al., 2011a), in line

with the hypothesis that smaller brains show a higher

degree of monosynaptic integration across areas, in

comparison with larger brains (Ringo, 1991 Striedter,

2005).

The present study, together with previous work in

other marmoset frontal and parietal areas (e.g., Burman

et al., 2006, 2011, 2014; Reser et al., 2013), demon-

strate that areas 6DC and 6DR in the marmoset corre-

spond closely with those identified in the macaque in

terms of patterns of connections (Fig. 16). While our

data also highlights some intriguing differences, these

are comparatively minor, and in our view are insufficient

TABLE 4.

Percentage of Supragranular Layer Neurons Projecting

to Area 6D Subdivisions (Ipsilateral Connections)

Area 6DR Area 6DC

Area1 n2 %SLN3 n4 %SLN

46 125 83.2 — —12 136 93.3 — —8b 1008 74.5 — —8aD 632 78.0 — —8aV 132 87.9 — —8C 390 78.2 77 83.16DR — — 1118 80.56DC 718 59.5 — —6M 1002 52.4 2079 79.76Va 108 71.3 — —4 — — 1629 90.624a/b 50 54.0 71 78.924c 51 70.6 155 88.424d — — 119 93.323a/b 1413 93.4 158 94.923V 95 93.7 — —31 401 94.5 307 93.229 300 97.7 — —30 283 93.6 — —1/2 — — 487 98.4PV 1 S2 79 79.7 94 91.5PE 258 97.7 1821 89.2PEC 51 96.1 69 94.2PFG 90 92.2 — —PG 117 82.9 — —OPt 71 94.4 — —AIP 64 92.2 — —MIP 221 98.2 — —VIP 90 93.3 — —LIP 427 94.8 — —STP 151 94.0 — —FST 76 98.7 — —TE1TEO 108 95.4 — —19M 61 100.0 — —PGM 455 98.5 — —

1Only areas containing at least 50 labeled neurons across all cases

following injection sites restricted to areas 6DR or 6DC are listed.2Total number of labeled neurons following 5 injections restricted to

area 6DR (cases 1–5).3Percentage of labeled neurons located in supragranular layers.4Total number of labeled neurons following 5 injections restricted to

area 6DC (cases 7–11).



to reject the hypothesis of a homologous organization.

The similarities and differences, and possible reasons

for the latter, are discussed in detail below. Still, it

must be recognized that some of these conclusions

may need to be revised in the future, as additional

research may lead to refinement of the currently recog-

nized boundaries of cortical areas in both marmoset

and macaque (as well as other primates, including

humans). In summary, in addition to its value in clarify-

ing the cortical circuitry in the marmoset, including

quantitative information about consistent and variable

features of their connectivity (an issue about which

very little is documented), the present results provide

strong evidence of a homologous organization of the

dorsal premotor cortex in New and Old World monkeys.

We found that areas 6DC and 6DR had reciprocal

connections, and together received major projections

from the medial premotor area (6M), with some evi-

dence of a rostrocaudal gradient of connections in the

latter. However, there were differences in their pattern

of connections with other areas (Fig. 16). For example,

while area 6DR received consistent inputs from prefron-

tal cortex (in particular, areas 8b and 8aD), area 6DC

received few such connections. Conversely, 6DC

received a major projection from M1, which only sent

very sparse and variable projections to 6DR. On the

medial wall, projections from the anterior cingulate cor-

tex preferentially targeted 6DC, while the posterior cin-

gulate and adjacent medial wall areas formed one of

the main sets of afferents to 6DR. In parietal cortex,

somatosensory areas and the putative homolog of area

PE preferentially targeted area 6DC, whereas the region

likely to correspond to the macaque intraparietal areas

projected mainly to area 6DR.

While confirming that both 6DC and 6DR are part of

the cortical motor control network (Vogt and Vogt, 1919;

Barbas and Pandya, 1987; Kurata, 1991; He et al., 1993;

Godschalk et al., 1995; Preuss et al., 1996; Wise et al.,

1997; Geyer et al., 2000; Luppino et al., 2003; Stepniew-

ska et al., 2006; Mirabella et al., 2011; Kaas et al.,

2011; Burman et al., 2008, 2014), these results demon-

strate that these areas are distinct in terms of their con-

nectivity, and likely function. In particular, they suggest

that, as in the macaque, area 6DC is more directly

involved in the preparation and execution of motor acts,

while area 6DR integrates sensory and internally driven

inputs for the planning of goal-directed actions (Barbas

and Pandya, 1987; Rizzolatti et al., 1998; Geyer et al.,

2000; Hanakawa et al., 2002; Luppino et al., 2003;

Cisek and Kalaska, 2005; Mirabella et al., 2011). These

similarities, across species with different motor reper-

toires and patterns of corticospinal projections (Bortoff

and Strick, 1993; Lemon et al., 2004; Lemon and Grif-

fiths, 2005), attest to the fundamental similarity of the

dorsal premotor cortex across simian primates, suggest-

ing a homologous organization inherited from a common

ancestor of New and Old World monkeys.

Connections with prefrontal areasSeveral prefrontal areas in the macaque and marmo-

set have been reported to connect with the rostral part

of the dorsal area 6 complex, but not with its caudal

part (Barbas and Pandya, 1987; Petrides and Pandya,

Figure 16. Summary of the main cortical projections to the dorsal premotor cortex in the marmoset monkey. The thickness of the arrows

is in proportion to the percentage of labeled neurons with injections restricted to either 6DR or 6DC (see scale at bottom). A shows the

projections to area 6DC, and B shows the projections to area 6DR.

K.J. Burman et al.


1999; Geyer et al., 2000; Luppino et al., 2003; Step-

niewska et al., 2006; Reser et al., 2013). Our results

confirm this distinction, as only occasional isolated cells

were observed in prefrontal areas following injections in

area 6DC.

The richest prefrontal projections to area 6DR origi-

nated in areas 8b and 8aD, with modest inputs from

areas 8aV, 46 and 12. Projections from area 45 were

sparse, and more variable. A similar distribution has

been reported in a detailed analysis of prefrontal connec-

tions with F7 (6DR) in the macaque. In particular, projec-

tions from this same complement of prefrontal areas

target the supplementary eye field, which is located in

the rostral part of F7 (F7-SEF; Luppino et al., 2003;

Wang et al., 2005). We also found that area 8b sent

strong projections throughout 6DR, while the caudal part

of area 6DR received comparatively much weaker projec-

tions from area 8aD in comparison with the rostral part.

This observation is reflected in the available data in the

macaque, which showed that area 8b and the dorsal

part of area 46 are the primary sources of prefrontal

input to sites in the ventral and caudal parts of F7 (F7-

nonSEF). These subregions of macaque F7 are thought

to be involved in the control of arm reaching to target

movements (di Pelligrino and Wise, 1991). A possible

point of difference between species may be the relative

paucity, in the marmoset, of projections from area 45 to

rostral area 6DR, which are robust in the macaque (Pet-

rides, 1996; Petrides and Pandya, 2002); however, this

may simply reflect the paucity of data about the exact

limits of this prefrontal area in the marmoset.

With the exception of area 8b, the prefrontal areas

that send projections to area 6DR are interconnected

with the extrastriate cortex (Burman et al., 2006, 2008;

Rosa et al., 2009; see Kravitz et al., 2011, for compari-

son with macaques), indicating that visual information

reaches 6DR through both direct and indirect pathways.

Area 8b is thought to play a role in reward processing

and error monitoring during task performance, including

the integration of cognitive and emotive limbic informa-

tion during decision-making (Mitchell, 2011; Ray and

Zald, 2012; Reser et al., 2013). Interestingly, marmoset

area 6DR not only has rich reciprocal connections with

area 8b, but also has many other connections in com-

mon with this area, including prefrontal, posterior mid-

line cortex, and superior temporal multimodal

association areas (Reser et al., 2013), suggesting a

close functional association between the two regions.

Areas 8aD and 8aV, on the other hand, appear to par-

ticipate in spatial cognition, including working memory.

While area 8aV is concerned more specifically with the

visual modality (Burman et al., 2006), area 8Ad may

integrate information about peripheral vision with audi-

tory and somatosensory information (Petrides and Pan-

dya, 1999; Reser et al., 2013). Studies in the macaque

have also indicated that areas 46 and the lateral part

of area 12 are also involved with different aspects of

working memory (Petrides, 1996; Petrides and Pandya,

2002). In combination, these prefrontal connections

suggest that area 6DR is involved in the planning of

actions according to information about target location,

either in response to stimuli currently present in peri-

personal space, or kept in working memory (Rizzolatti

and Fabbrio-Destro, 2009; Stuphorn et al., 2010).

Sparse projections to area 6DR originated from other

frontal areas, including areas 9, 10, 11, 13, 32, and

PrCO. Prefrontal connections to the rostral part of the

dorsal premotor complex have also been reported in

the owl monkey (Stepniewska et al., 2006), but these

have not been correlated with cytoarchitectural areas.

Currently, the functional significance of these projec-

tions is unknown, although they may influence motor

planning by monitoring the consequences of decisions,

providing inputs related to internal states, such as moti-

vation and drives (Tsujimoto et al., 2010; Burman et al.,

2011a), and social context (Sallet et al., 2013).

Connections with premotor and primarymotor areas

In addition to the dorsal premotor areas considered

in the present report, the other major subdivisions of

the primate premotor cortex include the medial (6M)

and ventral (6V) premotor areas (Barbas and Pandya,

1987; Geyer et al., 2000). Data on the connections of

M1 (Burman et al., 2014) indicate that there may be

two functional fields within the marmoset area 6M,

probably corresponding to areas F3 (supplementary

motor area, SMA) and F6 (pre-SMA) identified in the

macaque (Matelli et al., 1985). Architectural studies

also suggest that there are two subdivisions in the mar-

moset 6V complex, which occupy dorsocaudal (6Va)

and ventrorostral (6Vb) positions (Burman et al., 2008;

Paxinos et al., 2012); these probably correspond to

macaque areas F4 and F5 (Matelli et al., 1985). Finally,

Paxinos et al. (2012) proposed a strip-like architectural

field that inserts between the dorsal and ventral premo-

tor complexes in the marmoset, named area 8 caudal

(8C), about which little is known. In a previous study,

this region was included in area 6DC, although its pat-

tern of myelination was noted as being distinct (Burman

et al., 2006)

Area 6M projected to both dorsal premotor areas,

with the strongest inputs targeting area 6DC, and the

caudal portion of area 6DR. In addition, area 6DR, but

not 6DC, received connections originating in the rostral



part of area 6M, likely to include the pre-SMA (F6; Bur-

man et al., 2014). In light of previous results in the

macaque, the interconnections between the rostral part

of area 6M and 6DR could play a role in the temporal

organization and coordination of complex forelimb and/

or oculomotor movements (Luppino et al., 1991; Matsu-

zaka et al., 1992; Shima et al., 1996; Shima and Tanji,

2000; Isoda and Tanji, 2004; Wang et al., 2005), includ-

ing inhibition of inappropriate actions (Nachev et al.,

2007). In addition, the much stronger 6M projections to

6DC and to the caudal part of 6DR could reflect a

greater importance of information about complex limb

movements to non-oculomotor regions of the dorsal

premotor complex.

Areas 6DC and 6DR were reciprocally intercon-

nected. In our data, the density of the 6DR input to

6DC diminished progressively from rostral to caudal

sites in the latter, pointing to an anatomical gradient

across the dorsal premotor complex. This observation

can be related to the results of electrophysiological and

functional imaging studies in humans and macaques

(Cisek and Kalaska, 2005; Hanakawa, 2011), which

revealed functional gradients across the same region.

For example, the meta-analysis by Hanakawa (2011)

indicated a rostrocaudal trend from mainly cognitive

(motor planning and imagery) in rostral 6DR, to mainly

movement execution, in caudal 6DC.

Ventral area 6 only sent modest projections, which

targeted mainly caudal sites in area 6DR, and caudolat-

eral sites in area 6DC. In the macaque, both area 6V

and caudolateral area 6DC participate in the control of

hand movement (Fogassi et al., 2001; Cerri et al.,

2003; Fluet et al., 2010; Gharbawie et al., 2011a), and

the present results support the idea that caudal area

6DR in the marmoset is also involved in the control of

distal movements. Another source of input to both 6DC

and 6DR originated in area 8C, a region which, based

on its location relative to previously published func-

tional maps, appears to be concerned with control of

head and eye movements, in other primate species

(Preuss et al., 1996; Tian and Lynch, 1996; Moschova-

kis et al., 2004).

Finally, in agreement with previous reports in maca-

ques (Tokuno and Tanji, 1993; Preuss et al., 1996;

Hatanaka et al., 2001; Dum and Strick, 2005; Stepnie-

weska et al., 2006), we found in the marmoset a robust

connection from M1 to area 6DC, but not to area 6DR.

These differences are also consistent with previous

descriptions of the afferent connections to M1 in vari-

ous primate species (Barbas and Pandya, 1987; Geyer

et al., 2000; Brasted and Wise, 2004; Muhammad

et al., 2006; Burman et al., 2014).

Connections with the cingulate cortex andother areas on the medial wall

Cytoarchitectural studies have identified marmoset

homologs of areas in the anterior (areas 24a–d), and

posterior cingulate cortex (areas 23a–c and 23V; Bur-

man and Rosa, 2009; Paxinos et al., 2012). Additionally,

the medial wall cortex contains several other areas that

figured prominently in the results of the present study:

area 31, which is dorsally adjacent to area 23b, retro-

splenial areas 29 and 30, and medial parietal area

PGM. At present, the definition of these areas in the

marmoset is based exclusively on cytoarchitectural

comparisons with the macaque, and location relative to

other areas.

Two motor-related areas have been identified in the

primate cingulate cortex. In macaques, an anterior field

is encompassed within cytoarchitectural areas 24c and

24d, while a second field is in rostral area 23c (Hutch-

ins et al., 1988; Dum and Strick, 1991, 1996; Morecraft

and van Hoesen, 1992; Stepniewska et al., 1993; Galea

and Darian-Smith, 1994; Roullier et al., 1994; Nimchin-

sky et al., 1996). Cingulate areas differentially targeted

areas 6DR and 6DC. In the present data, a modest pro-

jection from the anterior cingulate complex favored

area 6DC. Our data suggested a trend whereby rostral

area 6DC received input primarily from dorsal sites,

while caudal 6DC received most of its input from ven-

tral sites. In the macaque, the anterior cingulate motor

field sends direct projections to the spinal cord, and

has connections with prefrontal, limbic, and sensory

areas (Galea and Darian-Smith, 1994; He et al., 1995;

Dum and Strick, 1996; Morecraft et al., 2012) that are

likely to provide cognitive, emotional, and motivational

influence on motor function. The anterior cingulate

motor field has also been reported to be involved in the

control of forelimb reaching, grasping, and defense

movements in New World monkeys (Gharbawie et al.,

2011b).

The area 23 complex formed one of the major inputs

to area 6DR. However, we found negligible inputs from

rostral area 23c, the location of the posterior cingulate

motor field described in the macaque (Dum and Strick,

1996; Morecraft and van Hoesen, 1998; Parvizi et al.,

2006) and marmoset (Burman et al., 2014), to either

6DC or 6DR. Instead, most of the connection to area

6DR originated in caudal areas 23a and 23b, together

with sparse input from area 23V in some cases. Caudal

area 23 has been shown to be involved in visuospatial

orientation, memory, and attention (Vogt and Laureys,

2005; Vann et al., 2009; Kravitz et al., 2011), including

peripheral vision (Palmer and Rosa, 2006b; Yu et al.,

2012).

K.J. Burman et al.


A consistent projection from area 31 to both 6DR

and 6DC was evident. Functional interpretations are

presently hampered by the fact that this medial area

has only been defined in the marmoset based on

cytoarchitecture, and thus the extent to which it corre-

sponds to area 31 in other species remains to be deter-

mined. In the macaque area 31 is heavily

interconnected with retrosplenial areas 23, 29, 30, and

medial parietal area V6a (Morecraft et al., 2004; Parvizi

et al., 2006; Gamberini et al., 2009). Here, we found

that areas 29 and 30 primarily targeted the rostral part

of area 6DR, where the putative SEF homolog is likely

to be located. Human functional imaging studies indi-

cate the posteromedial cortex to be involved in cogni-

tive processing and the default mode network of brain

regions that are active during awake passive rest

(Raichle et al., 2001; Greicius et al., 2003). In addition,

reciprocal connections with the parahippocampal region

and parietal area PG indicate that two functions com-

mon to all of these posteromedial areas may be a role

in navigation and arm reaching movements, respectively

(Parvizi et al., 2006; Vann et al., 2009).

Our data also indicate that the putative homolog of

PGM, a visuomotor area on the medial wall, sent con-

sistently rich projections to rostral area 6DR, in agree-

ment with results in Cebus and macaque monkeys

(Leichnetz, 2001; Matelli et al., 1998). In contrast, its

connections with marmoset caudal area 6DR and area

6DC were sparse. In the study by Leichnetz (2001),

area PGM (7m) in Cebus and macaque monkeys was

shown to have many oculomotor connections, and neu-

ral activity related to visually guided reaching has also

been reported (Ferraina et al., 1997).

Connections with somatosensory and insularcortices

Somatosensory areas predominantly targeted area

6DC. This connection was characterized by strong input

from area 1/2, and weaker connections from areas 3a

and S2. These connections, in combination with a major

input from posterior parietal area PE, indicate that area

6DC is concerned primarily with somatomotor transfor-

mations guiding limb movement. The often rich input

from rostral parietal somatosensory areas appears to

be at odds with the results of tracer injections in the

forelimb reach zones of the dorsal premotor cortex in

squirrel and owl monkeys (Gharbawie et al., 2011b).

However, the exact homology of the premotor areas

identified in these species and the present subdivisions

is unclear; it is possible that these injections were

placed in sites corresponding to area 6DR in the pres-

ent nomenclature, while 6DC corresponds to "rostral

M1" (M1r) (Burman et al., 2008). In an earlier study in

owl monkeys (Stepniewska et al., 1993), somatosensory

connections with M1r had a similar distribution and

density pattern to those revealed by our area 6DC

injections (e.g., their fig. 16). In contrast, marmoset

area 6DR received very sparse and inconsistent input

from areas 3a, 3b, 1, and 2, in agreement with results

reported for Galago (particularly from an injection site

placed rostrally in the premotor region; Fang et al.,

2005), and for the squirrel monkey premotor forelimb

reach zone (Gharbawie et al., 2011b).

Modest connections were observed with S2, most

commonly in the area 6DC cases, but also in the most

caudal 6DR cases. In macaques, S2 appears to be part

of a lateral corticolimbic pathway transmitting cutane-

ous information (Friedman et al., 1986; Qi et al., 2002).

Finally, very sparse connections from insular cortex to

both subdivisions were observed in most cases. How-

ever, it is interesting to note that area 6DR, the target

of projections from the granular insular cortex, also has

a six-layered cortex, albeit with an incipient layer IV,

and has a cognitive function, whereas agranular area

6DC is connected with the same insular regions as M1

(Burman et al., 2014).

PrCO, which has been considered as part of the gus-

tatory association cortex (Ogawa, 1994; Burman and

Rosa, 2009), receives somatosensory information from

the orofacial region (Kaas, 2005). Its connections with

the M1 face representation sector (Burman et al.,

2014) and ventral premotor cortex (Barbas and Pandya,

1987; Kurata et al., 1991; Dum and Strick, 2005), sug-

gest a role in coordinating feeding actions.

Connections with posterior parietal cortexThe rostral posterior parietal cortex of the marmoset

has not yet been studied extensively, and most of the

information to date derives from cytoarchitectural com-

parisons, as well as limited connectional data (e.g., Bur-

man et al., 2008). Presently, a large region that has the

architectural characteristics of area PE is recognized,

but, as in the macaque, this is likely to contain finer

subdivisions (Lewis and Van Essen, 2000). The present

data showed that area PE sent a robust projection to

area 6DC, and a generally weaker projection to area

6DR. A rostrocaudal trend was evident, with labeled

cells projecting to area 6DC located more rostrally than

those projecting to area 6DR. In macaques, connec-

tions between PE and 6DC (F2) primarily involved sites

in the rostral part of the dorsal bank of the intraparietal

sulcus (Marconi et al., 2001; Tanne-Gariepy et al.,

2002; Bakola et al., 2013), which also projects to the

spinal cord (Matelli et al., 1998). In this species, area

PE is largely concerned with limb control, especially the



forelimb and fingers (Huffman and Krubitzer, 2001;

Gardner et al., 2007; Krubitzer and Disbrow, 2008;

Chen et al., 2009). While neurons in the expected

location of area PE in all primate species respond pre-

dominantly to high threshold somatosensory or proprio-

ceptive stimuli (Krubitzer and Kaas, 1990; Padberg

et al., 2007; Seelke et al., 2012), in the macaque neu-

rons in adjacent caudal PE (PEC) also have oculomotor

activity (Batista et al., 1999) and respond to visual as

well as somatosensory and proprioceptive stimuli

(Squatrito et al., 2001; Breveglieri et al., 2008; Bakola

et al., 2010). Minor connections that favored area 6DC

and caudal area 6DR originated from the putative PEC

of the marmoset, while labeled cells projecting to ros-

tral 6DR extended more caudally.

Injections in area 6DR labeled neurons in the four

cytoarchitectural subdivisions of the intraparietal region

identified by Paxinos et al. (2012) as likely homologs of

the homonymous macaque areas: AIP, VIP, MIP, and

LIP. These connections varied in density, but generally

favored rostral area 6DR. In particular, area LIP (which,

as in the macaque, is more densely myelinated than

adjacent areas, and has reciprocal connections with

various dorsal stream areas; Rosa et al., 2009) consis-

tently sent rich projections to rostral area 6DR. The

information conveyed from intraparietal areas to rostral

area 6DR is likely to play a role in visual attention and

directing eye movements, and in visually guided reach-

ing and appropriate hand-shaping prior to grasping an

object in peripersonal space, as suggested by studies

in the macaque (Colby, 1998; Anderson and Buneo,

2002; Grefkes and Fink, 2005; Borra et al., 2008). In

contrast, area VIP has been described as a polymodal

association area, in which the majority of cells also

respond to motion stimuli, suggesting possible involve-

ment in the perception of self and object movement in

peripersonal space (Bremmer et al., 2002; reviewed in

Grefkes and Fink, 2005). However, the exact bounda-

ries of AIP, VIP, and MIP in the marmoset need to be

validated by more extensive anatomical and physiologi-

cal studies.

Minor projections from the ventral parietal cortex ori-

ginated in cytoarchitectural areas PF, PFG, PG, and OPt

(Paxinos et al., 2012), in particular from the latter

three. Collectively, these minor connections suggest the

involvement of the marmoset dorsal premotor areas in

reaching and grasping movements in response to tactile

stimuli, based on studies of the presumed homologous

areas in the macaque (Rozzi et al., 2006, 2008; Ferrari

et al., 2003; Yocochi et al., 2003); area 6DR, particu-

larly its rostral region, could also participate in path-

ways controlling oculomotor movements. Our data on

these connections provide a useful guide for design of

experiments to test the homology of cytoarchitecturally

identified area between species.

Other ipsilateral connectionsSparse inputs from sensory areas were present in all

cases. Previous studies have demonstrated that, as well

as their main connections, cortical areas often also

have a range of variable inputs characterized by small

numbers of neurons (Markov et al., 2014; Burman

et al., 2014). Although some of these connections have

not been reported in the macaque, this may reflect pre-

vious observations that suggest that “minor” connec-

tions may be more obvious in smaller brains, which

require further integration across hierarchical levels of

processing (Palmer and Rosa, 2006a).

Area 6DR received minor inputs from visual areas,

which were rarely observed to target 6DC, including the

motion-sensitive superior temporal areas MST, FST, and

MTC (Rosa and Elston, 1998), occipitoparietal area DA

(a likely homolog of V3A; Rosa et al., 2005, 2013), the

peripheral representations of V2 and VLA (V4; Rosa and

Tweedale, 2000), area prostriata (Rockland, 2012; Yu

et al., 2012), and the as yet poorly characterized

medial part of area 19, which also has an emphasis on

peripheral vision (Allman and Kaas, 1976; Rosa and

Schmid, 1995). These inputs highlight a direct pathway

whereby information in peripheral vision could influence

motor planning. The exception appears to be the pro-

jection from the dorsal parts of the inferior temporal

cortex, which was evident following 6DR injections;

thus, information about central vision can also access

the premotor network, albeit only from hierarchically

advanced stages of processing.

Finally, injections in area 6DR consistently labeled STP,

and injections in both 6DR and 6DC labeled, less consis-

tently, area TPt (which, in the macaque, has been shown

to be a site of auditory and somatosensory convergence;

Smiley et al., 2007) and auditory area CM (de la Mothe

et al., 2006). Overall, these sparse projections from sen-

sory association areas could convey information about

the location of objects in space (Reser et al., 2013).

Interhemispheric connectionsOur analysis of interhemispheric connections

revealed that, despite the smaller number of labeled

cells, these originated in many of the same areas that

send ipsilateral connections. As in our previous study of

M1 connections, approximately half of the labeled cells

were located in homotopic regions in the contralateral

hemisphere (Burman et al., 2014). However, the pattern

of interhemispheric projections was not an exact mirror

of the ipsilateral pattern. For example, Table 3 shows

that parietal area PE, which is a major source of

K.J. Burman et al.


projections to area 6DC, contains relatively sparse con-

tralateral label (0.5% of the total); and connections from

parietal visual association areas to area 6DR were also

relatively sparse. These results resemble those of our

earlier studies of the connections of the frontal pole

and M1, which revealed that interhemispheric connec-

tions from areas outside the frontal lobe were compara-

tively less significant (Burman et al., 2011a, 2014).

Laminar patterns of connectionsAlmost all of the connections to premotor area 6D

showed relatively high %SLN values. According to the

proposal that there is a correspondence between the

percentage of supragranular label and hierarchical level

(Barone et al., 2000), these connections would be classi-

fied as feedforward projections. In light of the cognitive

and motor roles of the two subdivisions this would not be

unexpected, although a feedforward projection to area

6DC from M1 seems surprising. However, this connec-

tion may provide direct ongoing information about the

parameters of movement execution coded for in M1 such

as force production that has a modulatory role on area

6DC activity, since the latter region also projects directly

to the spinal cord (He et al., 1993). The connections from

areas 24a/b, 6M, and possibly area 6DC to 6DR would

be classified as lateral connections between areas on the

same hierarchical level, while the connection from area

6DR to 6DC is clearly feedforward, as would be

expected. Since both 6M and 6DC have a cognitive

aspect to their motor role they may well occupy a similar

hierarchical level as 6DR (see also Dum and Strick,

2005). The correspondence proposed by Barone et al.,

2000 may depend on the specific role of the projection

being examined, rather than there being a rigid hierarchy

between different areas. However, these conclusions

need confirmation, given the differences in tracers used

(dextrans in the present study, versus fast blue and dia-

midino yellow in most previous studies) and the generally

smaller amounts of tracer injected in the marmoset,

which likely led to less homogeneous uptake across cort-

ical layers.

Comparative and functional considerationsIn marmosets, as in other primate species, 6DC and

6DR have distinct patterns of cortical input, indicating

different functional roles. A strong connection with M1

and other premotor areas, in combination with a prepon-

derance of somatosensory inputs, indicates that the inte-

gral role proposed for caudal area 6D in the motor

networks of Old World and other New World monkeys

arose early in primate evolution. Generally, the connec-

tions in the marmoset are very similar to those reported

for the macaque; however, there appear to be some dif-

ferences, particularly regarding inputs from the parietal

lobe. In the marmoset, a robust projection from area PE

originates from much of this cytoarchitectural area,

whereas in the macaque the projection from area PE orig-

inates more laterally in (and adjacent to), the rostral

intraparietal sulcus. Our results also suggest there may

be differences in the projections from the putative homo-

logs of areas V6a and MIP. We found very sparse input

from parietal area V6a; however, this finding could also

be due to the fact that most of our injections were in dor-

sal 6DC, as were those of Johnson et al. (1993), who also

found no projection from area V6a in the macaque. Input

from intraparietal area MIP to area 6DC was also sparse

in the marmoset, whereas a strong projection has been

reported in the macaque (Matelli et al., 1998). Confirma-

tion of these possible differences will require more exten-

sive study of the marmoset parietal cortex, to refine our

understanding of the boundaries of areas and their exact

correspondence with those described in the macaque.

The connections of area 6DR indicate this region

functions at a higher cognitive level, and is similarly

organized in the marmoset as in macaques. It has

recently been proposed that the rostral premotor areas

are the most likely site for the integration of informa-

tion flow between cognitive and motor networks (Hana-

kawa, 2011). Our results support this hypothesis. Area

6DR has connections with prefrontal, parietal, and other

areas involved in the dorsal and ventral visual streams,

especially the former (Kravitz et al., 2011), that place it

in an ideal position to be a site of convergence of

highly processed sensory information transmitted in the

visual pathways with other cognitive input, and to sub-

sequently influence motor preparation via its connec-

tions with caudal premotor areas.

In recent years, human and macaque functional mag-

netic resonance imaging (fMRI) studies have focused atten-

tion on interacting oscillatory networks that appear to form

the underlying intrinsic organization of the brain, and the

results of recent studies suggest that these networks were

already present in the primate lineage over 30 million years

ago (Reser et al., 2013; see also Belcher et al., 2013). The

present results show that area 6DR in the marmoset has

connections with areas involved in two anticorrelated net-

works, described as task-negative (default mode network,

DMN) and task-positive (Fox et al., 2005). Functional MRI

studies led to the proposal that oscillatory interaction

between these two distributed networks representing two

opposing mental states reflects an underlying intrinsic orga-

nization that can be modulated by sensory information (Fox

et al., 2005). The rich connections between area 6DR, and

the area 8 complex and posterior midline areas of the DMN

(Mantini et al., 2011; Reser et al., 2013), in particular, sug-

gest that the former may interact more strongly with this



network than does area 6DC. Since neither task-negative

nor task-positive networks include primary sensory and

motor cortices (Fox et al., 2005), our results provide sup-

port for the proposal by Hanakawa (2011) that area 6DR

may gate information flow between cognitive and motor

networks as required by the ongoing environmental and

behavioral context.

ACKNOWLEDGMENTSThe skilled assistance of Katrina Worthy and Tristan

Chaplin, including support in several phases of this pro-

ject, as well as the technical support by Amanda Worthy

are gratefully acknowledged.

CONFLICT OF INTEREST

The authors declare that there are no conflicts of

interest.

ROLE OF AUTHORS

All authors had full access to all the data in the

study and take responsibility for the integrity of the

data and the accuracy of the data analysis. Study con-

cept and design: KJB, MGPR. Acquisition of data: KJB,

SB, KER. Analysis and interpretation of data: KJB, SB,

KER, DHR, MGPR. Drafting of the article: KJB, MGPR.

Preparation of reconstructions and figures: SB, KJB.

Critical revision of the article for important intellectual

content: SB, DHR. Statistical analysis: DHR. Obtained

funding: KJB, MGPR. Administrative, technical, and

material support: KER. Study supervision: KJB, MGPR.

REFERENCESAllman JM, Kaas JH. 1976. Representation of the visual field

on the medial wall of occipital-parietal cortex in the owlmonkey. Science 191:572–575.

Andersen RA, Buneo C. 2002. Intentional maps in posteriorparietal cortex. Annu Rev Neurosci 25:189–220.

Bakola S, Gamberini M, Passarelli L, Fattori P, Galletti C.2010. Cortical connections of parietal field PEc in themacaque: linking vision and somatic sensation for thecontrol of limb action. Cereb Cortex 20:2592–2604.

Bakola S, Passarelli L, Gamberini M, Fattori P, Galletti C.2013. Cortical connectivity suggests a role in limb coor-dination for macaque area PE of the superior parietalcortex. J Neurosci 33:6648–6658.

Barbas H, Pandya DN. 1987. Architecture and frontal corticalconnections of the premotor cortex (area 6) in the rhe-sus monkey. J Comp Neurol 256:211–228.

Barone P, Batardiere A, Knoblauch K, Kennedy H. 2000. Lami-nar distribution of neurons in extrastriate areas projec-ting to visual areas V1 and V4 correlates with thehierarchical rank and indicates the operation of a dis-tance rule. J Neurosci 20:3263–3281.

Batista AP, Buneo CA, Snyder LH, Anderson RA. 1999. Reachplans in eye-centered coordinates. Science 285:257–260.

Belcher AM, Yen CC, Stepp H, Gu H, Lu H, Yang Y, Silva AC, SteinEA. 2013. Large-scale brain networks in the awake, trulyresting marmoset monkey. J Neurosci 33:16796–16804.

Blum B, Kulikowski JJ, Carden D, Harwood D. 1982. Eye move-ments induced by electrical stimulation of the frontal eyefields of marmosets and squirrel monkeys. Brain BehavEvol 21:34–41.

Borra E, Belmalih A, Calzavara R, Gerbella M, Murata A, RozziS, Luppino G. 2008. Cortical connections of the maca-que anterior intraparietal (AIP) area. Cereb Cortex 18:1094–1111.

Bortoff GA, Strick PL. 1993. Corticospinal terminations in twonew-world primates: further evidence that corticomoto-neuronal connections provide part of the neural sub-strate for manual dexterity. J Neurosci 13:5105–5118.

Brasted PJ, Wise SP. 2004. Comparison of learning-relatedneuronal activity in the dorsal premotor cortex and stria-tum. Eur J Neurosci 19:721–740.

Bremmer F, Duhamel J-R, Hamed SB, Graf W. 2002. Headingencoding in the macaque ventral intraparietal area (VIP).Eur J Neurosci 16:1554–1568.

Breveglieri R, Galletti C, Monaco S, Fattori P. 2008. Visual,somatosensory, and bimodal activities in the macaqueparietal area PEc. Cereb Cortex 18:806–816.

Burish MJ, Stepniewska I, Kaas JH. 2008. Microstimulationand architectonics of frontoparietal cortex in commonmarmosets (Callithrix jacchus). J Comp Neurol 507:1151–1168.

Burman KJ, Rosa MGP. 2009. Architectural subdivisions ofmedial and orbital frontal cortices in the marmoset mon-key (Callithrix jacchus). J Comp Neurol 514:11–29.

Burman KJ, Palmer SM, Gamberini M, Rosa MGP. 2006.Cytoarchitectonic subdivisions of the dorsolateral frontalcortex of the marmoset monkey (Callithrix jacchus), andtheir projections to dorsal visual areas. J Comp Neurol495:149–172.

Burman KJ, Palmer SM, Gamberini M, Spitzer MW, Rosa MGP.2008. Anatomical and physiological definition of themotor cortex of the marmoset monkey. J Comp Neurol506:860–876.

Burman KJ, Reser DH, Yu HH, Rosa MGP. 2011a. Corticalinput to the frontal pole of the marmoset monkey. CerebCortex 21:1712–1737.

Burman KJ, Reser DH, Richardson KE, Gaulke H, Worthy KH,Rosa MGP. 2011b. Subcortical projections to the frontalpole in the marmoset monkey. Eur J Neurosci 34:303–319.

Burman KJ, Bakola, S, Richardson, KE, Reser DH, Rosa MGP.2014. Patterns of cortical input to the primary motorcortex in the marmoset monkey. J Comp Neurol 522:811–843.

Cerri G, Shimazu H, Maier MA, Lemon RN. 2003. Facilitationfrom ventral premotor cortex of primary motor cortexoutputs to macaque hand muscles. J Neurophysiol 90:832–842.

Chaplin TA, Yu HH, Soares JG, Gattass R, Rosa MGP. 2013. Aconserved pattern of differential expansion of corticalareas in simian primates. J Neurosci 33:15120–15125.

Chen J, Reitzen SD, Kohlenstein JB, Gardner EP. 2009. Neuralrepresentation of hand kinematics during prehension inposterior parietal cortex of the macaque monkey. J Neu-rophysiol 102:3310–3328.

Cisek P, Kalaska JF. 2005. Neural correlates of reaching decisionsin dorsal premotor cortex: specification of multiple directionchoices and final selection of action. Neuron 45:801–814.

Colby CL. 1998. Action-oriented spatial reference frames incortex. Neuron 20:15–24.

Darian-Smith C, Darian-Smith I, Cheema SS. 1990. Thalamicprojections to sensorimotor cortex in the macaque mon-key: use of multiple retrograde fluorescent tracers. JComp Neurol 299:17–46.

K.J. Burman et al.


de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA. 2006.Cortical connections of the auditory cortex in marmosetmonkeys: core and medial belt regions. J Comp Neurol496:27–71.

di Pelligrino G, Wise SP. 1991. A neurophysiological compari-son of three distinct regions of the primate frontal lobe.Brain 114:951–978.

Dum RP, Strick PL. 1991. The origin of corticospinal projec-tions from the premotor areas in the frontal lobe. J Neu-rosci 11:667–689.

Dum RP, Strick PL. 1996. Spinal cord terminations of themedial wall motor areas in macaque monkeys. J Neurosci16:6513–6525.

Dum RP, Strick PL. 2002. Motor areas in the frontal lobe ofthe primate. Physiol Behav 77:677–682.

Dum RP, Strick PL. 2005. Frontal lobe inputs to the digit rep-resentations of the motor areas on the lateral surface ofthe hemisphere. J Neurosci 25:1375–1386.

Fang P-C, Stepniewska I, Kaas, JH. 2005. Ipsilateral corticalconnections of motor, premotor, frontal eye, and poste-rior parietal fields in a prosimian primate, Otolemur gar-netti. J Comp Neurol 490:305–333.

Ferraina S, Johnson PB, Garasto MR, Battaglia-Mayer A,Ercolani L, Bianchi L, Lacquaniti F, Caminiti R. 1997.Combination of hand and gaze signals during reaching:activity in parietal area 7m of the monkey. J Neurophy-siol 77:1034–1038.

Ferrari PF, Gallese V, Rizzolatti G, Fogassi L. 2003. Mirrorneurons responding to the observation of ingestive andcommunicative mouth actions in the monkey ventral pre-motor cortex. Eur J Neurosci 17:1703–1714.

Fluet MC, Baumann MA, Scherberger H. 2010. Context-spe-cific grasp movement representation in macaque ventralpremotor cortex. J Neurosci 30:15175–15184.

Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L,Rizzolatti G. 2001. Cortical mechanism for the visualguidance of hand grasping movements in the monkey: areversible inactivation study. Brain 124:571–586.

Fouad K, Klusman I, Schwab ME. 2004. Regenerating cortico-spinal fibers in the marmoset (Callitrix jacchus) after spi-nal cord lesion and treatment with the anti-Nogo-Aantibody IN-1. Eur J Neurosci 20:2479–2482.

Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC,Raichle ME. 2005. The human brain is intrinsically organ-ized into dynamic, anticorrelated functional networks.Proc Natl Acad Sci U S A 102:9673–9678.

Freret T, Bouet V, Toutain J, Saulnier R, Pro-Sistiaga P, Bihel E,Mackenzie ET, Roussel S, Schumann-Bard P, Touzani O.2008. Intraluminal thread model of focal stroke in the non-human primate. J Cereb Blood Flow Metab. 28:786–796.

Friedman DP, Murray EA, O’Neill JB, Mishkin M. 1986. Corticalconnections of the somatosensory fields of the lateralsulcus of macaques: evidence for a corticolimbic path-way for touch. J Comp Neurol 252:323–347.

Galea MP, Darian-Smith I. 1994. Multiple corticospinal neuronpopulations in the macaque monkey are specified bytheir unique cortical origins, spinal terminations, andconnections. Cereb Cortex 4:166–194.

Gallyas F. 1979. Silver staining of myelin by means of physi-cal development. Neurol Res 1:203–209.

Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S,Luppino G, Galletti C. 2009. Cortical connections of thevisuomotor parietooccipital area V6Ad of the macaquemonkey. J Comp Neurol 513:622–642.

Gardner EP, Babu KS, Reitzen SD, Ghosh S, Brown AS, ChenJ, Hall AL, Herzlinger MD, Kohlenstein JB, Ro JY. 2007.Neurophysiology of prehension. I. Posterior parietal cor-

tex and object oriented hand behaviors. J Neurophysiol97:387–406.

Geyer S, Matelli M, Luppino G, Zilles K. 2000. Functional neu-roanatomy of the primate isocortical motor system. AnatEmbryol (Berl) 202:443–474.

Gharbawie OA, Stepniewska I, Qi H, Kaas JH. 2011a. Multipleparietal-frontal pathways mediate grasping in macaquemonkeys. J Neurosci 31:11660–11677.

Gharbawie OA, Stepniewska I, Kaas JH. 2011b. Cortical con-nections of functional zones in posterior parietal cortexand frontal cortex motor regions in New World monkeys.Cereb Cortex 21:1981–2002.

Ghosh S, Gattera R. 1995. A comparison of the ipsilateralcortical projections to the dorsal and ventral subdivisionsof the macaque premotor cortex. Somatosens Mot Res12:359–378.

Godschalk M, Mitz AR, van Duin B, van der Burg H. 1995.Somatotopy of monkey premotor cortex examined withmicrostimulation. Neurosci Res 23:269–279.

Grant S, Hilgetag CC. 2005. Graded classes of cortical con-nections: quantitative analyses of laminar projections tomotion areas of cat extrastriate cortex. Eur J Neurosci22:681–696.

Grefkes C, Fink GR. 2005. The functional organization of theintraparietal sulcus in humans and monkeys. J Anat 207:3–17.

Greicius MD, Krasnow B, Reiss AL, Menon V. 2003. Functionalconnectivity in the resting brain: a network analysis ofthe default mode hypothesis. Proc Natl Acad Sci U S A100:253–258.

Hanakawa T. 2011. Rostral premotor cortex as a gatewaybetween motor and cognitive networks. Neurosci Res70:144–154.

Hanakawa T, Hopnda M, Sawamoto N, Okada T, Yonekura Y,Fukuyama H, Shibasaki H. 2002. The role of rostral Brod-mann area 6 in mental-operation tasks: an integrativeneuroimaging approach. Cereb Cortex 12:1157–1170.

Hatanaka N, Nambu A, Yamashita A, Takada M, Tokuno H.2001. Somatotopic arrangement and corticospinal inputsof the hindlimb region of the primary motor cortex in themacaque monkey. Neurosci Res 40:9–22.

He SQ, Dum RP, Strick PL. 1993. Topographic organization ofcorticospinal projections from the frontal lobe: motorareas on the lateral surface of the hemisphere. J Neuro-sci 13:952–980.

He SQ, Dum RP, Strick PL. 1995. Topographic organization ofcorticospinal projections from the frontal lobe: motorareas on the medial surface of the hemisphere. J Neuro-sci 15:3284–3306.

Hoshi E, Tanji J. 2007. Distinctions between dorsal and ventralpremotor areas: anatomical connectivity and functionalproperties. Curr Opin Neurobiol 17:234–242.

Huffman KJ, Krubitzer L. 2001. Area 3a: topographic organiza-tion and cortical connections in marmoset monkeys.Cereb Cortex 11:849–867.

Hutchins KD, Martino AM, Strick PL. 1988. Corticospinal pro-jections from the medial wall of the hemisphere. ExpBrain Res 71:667–672.

Isoda M, Tanji J. 2004. Participation of the primate presupple-mentary motor area in sequencing multiple saccades. JNeurophysiol 92:653–659.

Iyengar S, Qi HX, Jain N, Kaas JH. 2007. Cortical and thalamicconnections of the representations of the teeth andtongue in somatosensory cortex of new world monkeys.J Comp Neurol 501:95–120.

Johnson PB, Ferraina S, Caminiti R. 1993. Cortical networksfor visual reaching. Exp Brain Res 97:361–365.



Kaas JH. 2004. Evolution of somatosensory and motor cortexin primates. Anat Rec A Discov Mol Cell Evol Biol 281:1148–1156.

Kaas JH. 2005. The future of mapping sensory cortex in pri-mates: three of many remaining issues. Philos Trans RSoc Lond B Biol Sci 360:653–664.

Kaas JH, Gharbawie OA, Stepniewska I. 2011. The organiza-tion and evolution of dorsal stream multisensory path-ways in primates. Front Neuroanat 5:34.

Konomi T, Fujiyoshi K, Hikishima K, Komaki Y, Tsuji O, OkanoHJ, Toyama Y, Okano H, Nakamura M. 2012. Conditionsfor quantitative evaluation of injured spinal cord by invivo diffusion tensor imaging and tractography: preclini-cal longitudinal study in common marmosets. Neuro-image 63:1841–1853.

Kravitz DJ, Saleem KS, Baker CI, Mishkin M. 2011. A new neu-ral framework for visuospatial processing. Nat Rev Neu-rosci 12:217–230.

Krubitzer L, Disbrow E. 2008. The evolution of parietal areasinvolved in hand use in primates. In: Kaas JH, Gardner EP,editors. The senses: a comprehensive reference. Volume6, Somatosensation. Oxford, UK: Elsevier. p 183–214.

Krubitzer LA, Kaas JH. 1990. The organization and connec-tions of somatosensory cortex in marmosets. J Neurosci10:952–974.

Kurata K. 1991. Corticocortical inputs to the dorsal and ven-tral aspects of the premotor cortex of macaque mon-keys. Neurosci Res 12:263–280.

Legendre P. 2005. Species associations: the Kendall coeffi-cient of concordance revisited. J Agric Biol Environ Stat10:226–245.

Leichnetz GR. 2001. Connections of the medial posterior pari-etal cortex (area 7m) in the monkey. Anat Record 263:215–236.

Lemon RN, Griffiths J. 2005. Comparing the function of thecorticospinal system in different species: organizationaldifferences for motor specialization? Muscle Nerve 32:261–279.

Lemon RN, Kirkwood PA, Maier MA, Nakajima K, Nathan P.2004. Direct and indirect pathways for corticospinal con-trol of upper limb motoneurons in the primate. ProgBrain Res 143:263–279.

Lewis JW, Van Essen DC. 2002. Mapping of architectonic sub-divisions in the macaque monkey, with emphasis onparieto-occipital cortex. J Comp Neurol 428:79–111.

Lu MT, Preston JB, Strick PL. 1994. Interconnections betweenthe prefrontal cortex and the motor areas in the frontallobe. J Comp Neurol 341:375–392.

Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G.1991. Multiple representations of body movements inmesial area 6 and the adjacent cingulate cortex: anintracortical microstimulation study in the macaque mon-key. J Comp Neurol 311:463–482.

Luppino G, Rozzi S, Calzavara R, Matelli M. 2003. Prefrontaland agranular cingulate projections to the dorsal premo-tor areas F2 and F7 in the macaque monkey. Eur J Neu-rosci 17:559–578.

Mantini D, Gerits A, Nelissen K, Durand JB, Joly O, Simone L,Sawamura H, Wardak C, Orban GA, Buckner RL,Vanduffel W. 2011. Default mode of brain function inmonkeys. J Neurosci 31:12954–12962.

Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S,Squatrito S, Molinari M, Lacquaniti F, Caminiti R. 2001.Eye-hand coordination during reaching. I. Anatomicalrelationships between parietal and frontal cortex. CerebCortex 11:513–527.

Markov NT, Ercsey-Ravasz M, Lamy C, Ribieiro Gomes AR,Magrou L, Misery P, Giroud P, Barone P, Dehay C,

Toroczkai Z, Knoblauch K, Van Essen DC, Kennedy H.2013. The role of long-range connections on the specific-ity of the macaque interareal cortical network. Proc NatlAcad Sci U S A 110:5187–5192.

Markov NT, Ercsey-Ravasz MM, Ribeiro Gomes AR, Lamy C,Magrou L, Vezoli J, Misery P, Falchier A, Quilodran R,Gariel MA, Sallet J, Gamanut R, Huissoud C, ClavagnierS, Giroud P, Sappey-Marinier D, Barone P, Dehay C,Toroczkai Z, Knoblauch K, Van Essen DC, Kennedy H.2014. A weighted and directed interareal connectivitymatrix for macaque cerebral cortex. Cereb Cortex 24:17–36.

Marshall JW, Ridley RM. 2003. Assessment of cognitive andmotor deficits in a marmoset model of stroke. ILAR J 44:153–160.

Matelli M, Luppino G. 1996. Thalamic input to mesial andsuperior area 6 in the macaque monkey. J Comp Neurol372:59–87.

Matelli M, Luppino G, Rizzolatti G. 1985. Patterns of cyto-chrome oxidase activity in the frontal agranular cortex ofthe macaque monkey. Behav Brain Res 18:125–136.

Matelli M, Govoni P, Galletti C, Kutz DF, Luppino G. 1998.Superior area 6 afferents from the superior parietal lobulein the macaque monkey. J Comp Neurol 402:327–352.

Matsuzaka Y, Aizawa H, Tanji J. 1992. A motor area rostral tothe supplementary motor area (presupplementary motorarea) in the monkey: neuronal activity during a learnedmotor task. J Neurophysiol 68:653–662.

Mirabella G, Pani P, Ferraina S. 2011. Neural correlates ofcognitive control of reaching movements in the dorsalpremotor cortex of rhesus monkeys. J Neurophysiol 106:1454–1466.

Mitchell DG. 2011. The nexus between decision making andemotion regulation: a review of convergent neurocogni-tive substrates. Behav Brain Res 217:215–231.

Morecraft RJ, van Hoesen GW. 1992. Cingulate input to theprimary and supplementary motor cortices in the rhesusmonkey: evidence for somatotopy in areas 24c and 23c.J Comp Neurol 322:471–489.

Morecraft RJ, van Hoesen GW. 1998. Convergence of limbicinput to the cingulate motor cortex in the rhesus mon-key. Brain Res Bull 45:209–232.

Morecraft RJ, Cipolloni PB, Stilwell-Morecraft KS, Gedney MT,Pandya DN. 2004. Cytoarchitecture and cortical connec-tions of the posterior cingulate and adjacent somatosen-sory fields in the rhesus monkey. J Comp Neurol 469:37–69.

Morecraft RJ, Stilwell-Morecraft KS, Cipolloni PB, Ge J, McNealDW, Pandya DN. 2012. Cytoarchitecture and corticalconnections of the anterior cingulate and adjacent soma-tomotor fields in the rhesus monkey. Brain Res Bull 87:457–497.

Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W,Guldin W, Hadji Dimitrakis K, Savaki HE. 2004. Oculomo-tor areas of the primate frontal lobes: a transneuronaltransfer of rabies virus and [14C]-2-deoxyglucose func-tional imaging study. J Neurosci 24:5726–5740.

Muhammad R, Wallis JD, Miller EK. 2006. A comparison ofabstract rules in the prefrontal cortex, premotor cortex,inferior temporal cortex, and striatum. J Cogn Neurosci18:974–989.

Nachev P, Wydell H, O’Neill K, Husain M, Kennard C. 2007.The role of the pre-supplementary motor area in the con-trol of action. Neuroimage 36(Suppl 2):T155–T163.

Nimchinsky EA, Hof PR, Young WG, Morrison JH. 1996. Neuro-chemical, morphologic, and laminar characterization ofcortical projection neurons in the cingulate motor areasof the macaque monkey. J Comp Neurol 374:136–160.

K.J. Burman et al.


Ogawa H. 1994. Gustatory cortex of primates: anatomy andphysiology. Neurosci Res 20:1–13.

Padberg J, Franca JG, Cooke DF, Soares JG, Rosa MGP,Fiorani M Jr, Gattass R, Krubitzer L. 2007. Parallel evolu-tion of cortical areas involved in skilled hand use. J Neu-rosci 27:10106–10115.

Palmer SM, Rosa MGP. 2006a. Quantitative analysis of thecorticocortical projections to the middle temporal area inthe marmoset monkey: evolutionary and functional impli-cations. Cereb Cortex 16:1361–1375.

Palmer SM, Rosa MGP. 2006b. A distinct anatomical networkof cortical areas for analysis of motion in far peripheralvision. Eur J Neurosci 24:2389–2405.

Parvizi J, van Hoesen GW, Buckwalter J, Damasio A. 2006.Neural connections of the posteromedial cortex in themacaque. Proc Natl Acad Sci U S A 103:1563–1568.

Paxinos G, Huang XF, Petrides M, Toga AW. 2009. The rhesusmonkey brain in stereotaxic coordinates. San Diego: Aca-demic Press.

Paxinos G, Watson C, Petrides M, Rosa M, Tokuno H. 2012.The marmoset brain in stereotaxic coordinates. SanDiego: Academic Press.

Petrides M. 1996. Specialized systems for the processing ofmnemonic information within the primate frontal cortex.Philos Trans R Soc Lond B 351:1455–1462.

Petrides M. 2005. lateral prefrontal cortex: architectonic andfunctional organisation. Philos Trans R Soc B 360:781–795.

Petrides M, Pandya DN. 1999. Dorsolateral prefrontal cortex:comparative cytoarchitectonic analysis in the human andthe macaque brain and corticocortical connection pat-terns. Eur J Neurosci 11:1011–1036.

Petrides M, Pandya DN. 2002. Comparative cytoarchitectonicanalysis of the human and the macaque ventrolateralprefrontal cortex and corticocortical connection patternsin the monkey. Eur J Neurosci 16:291–310.

Pohlmeyer EA, Mahmoudi B, Geng S, Prins N, Sanchez JC.2012. Brain-machine interface control of a robot armusing actor-critic rainforcement learning. Conf Proc IEEEEng Med Biol Soc 2012:4108–4111.

Pohlmeyer EA, Mahmoudi B, Geng S, Prins N, Sanchez JC.2014. Using reinforcement learning to provide stablebrain-machine interface control despite neural input reor-ganization. PLoS One 9:e87253.

Preuss TM, Stepniewska I, Kaas JH. 1996. Movement repre-sentation in the dorsal and ventral premotor areas of owlmonkeys: a microstimulation study. J Comp Neurol 371:649–676.

Purvis A, Nee S, Harvey PH. 1995. Macroevolutionary inferencesfrom primate phylogeny. Proc Biol Sci 260:329–333.

Qi H-X, Lyon DC, Kaas JH. 2002. Cortical and thalamic connec-tions of the parietal somatosensory area in marmosetmonkeys (Callithrix jacchus). J Comp Neurol 443:168–182.

Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, GusnardDA, Shulman GL. 2001. A default mode of brain function.Proc Natl Acad Sci U S A 98:676–682.

Raos V, Franchi G, Gallesi V, Fogassi L. 2003. Somatotopic orga-nization of the lateral part of area f2 (dorsal premotor cor-tex) of the macaque monkey. J Neurophysiol 89:1503–1518.

Ray RD, Zald DH. 2012. Anatomical insights into the interac-tion of emotion and cognition in the prefrontal cortex.Neurosci Biobehav Rev 36:479–501.

Reser DH, Burman KJ, Richardson KE, Spitzer MW, Rosa MGP.2009. Connections of the marmoset rostrotemporal audi-tory area: express pathways for analysis of affective con-tent in hearing. Eur J Neurosci 30:578–592.

Reser DH, Burman KJ, Yu HH, Chaplin TA, Richardson KE,Worthy KH, Rosa MGP. 2013. Contrasting patterns of

cortical input to architectural subdivisions of the area 8complex: a retrograde tracing study in marmoset mon-keys. Cereb Cortex 23:1901–1922.

Ringo JL. 1991. Neuronal interconnection as a function ofbrain size. Brain Behav Evol 38:1–6.

Rizzolatti G, Luppino G, Matelli M. 1998. The organization ofthe cortical motor system: new concepts. Electroence-phalogr Clin Neurophysiol 106:283–296.

Rizzolatti G, Fabbri-Destro M. 2009. Premotor cortex in prima-tes: dorsal and ventral. Encycl Neurosci 935–945.

Rockland KS. 2012. Visual system: prostriata—a visual areaoff the beaten path. Curr Biol 22:R571–573.

Rosa MGP. 2002. Visual maps in the adult primate cerebralcortex: some implications for brain development andevolution. Braz J Med Biol Res 35:1485–1498.

Rosa MGP, Elston GN. 1998. Visuotopic organisation and neu-ronal response selectivity for direction of motion in visualareas of the caudal temporal lobe of the marmoset mon-key (Callithrix jacchus): middle temporal area, middletemporal crescent, and surrounding cortex. J Comp Neu-rol 393:505–527.

Rosa MGP, Schmid LM. 1995. Visual areas in the dorsal andmedial extrastriate cortices of the marmoset. J CompNeurol 359:272–299.

Rosa MGP, Tweedale R. 2000. Visual areas in lateral and ven-tral extrastriate cortices of the marmoset monkey. JComp Neurol 422:621–651.

Rosa MGP, Tweedale R. 2005. Brain maps, great and small: les-sons from comparative studies of primate visual cortical orga-nization. Philos Trans R Soc Lond B Biol Sci 360:665–691.

Rosa MGP, Palmer SM, Gamberini M, Tweedale R, Pinon MC,Bourne JA. 2005. Resolving the organization of the NewWorld monkey third visual complex: the dorsal extrastri-ate cortex of the marmoset (Callithrix jacchus). J CompNeurol 483:164–191.

Rosa MGP, Palmer SM, Gamberini M, Burman KJ, Yu HH,Reser DH, Bourne JA, Tweedale R, Galletti C. 2009. Con-nections of the dorsomedial visual area: pathways forearly integration of dorsal and ventral streams in extras-triate cortex. J Neurosci 29:4548–4563.

Rosa MGP, Angelucci A, Jeffs J, Pettigrew JD. 2013. The casefor a dorsomedial area in the primate ’third-tier’ visualcortex. Proc Biol Sci 280:20121372.

Roullier EM, Babalian, A, Kazennikov O, Moret V, Yu XH,Wiesendanger M. 1994. Transcallosal connections of thedistal forelimb representations of the primary and sup-plementary motor cortical areas in macaque monkeys.Exp Brain Res 102:227–243.

Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG,Matelli M, Luppino G. 2006. Cortical connections of theinferior parietal cortical convexity of the macaque mon-key. Cereb Cortex 16:1389–1417.

Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L. 2008.Functional organization of inferior parietal lobule convex-ity in the macaque monkey: electrophysiological charac-terization of motor, sensory and mirror responses andtheir correlation with cytoarchitectonic areas. Eur J Neu-rosci 28:1569–1588.

Sallet J, Mars RB, Noonan MP, Neubert F-X, Jbabdi S, O’ReillyJX, Filippini N, Thomas AG, Rushworth MF. 2013. Theorganization of dorsal frontal cortex in humans and mac-aques. J Neurosci 33:12255–12274.

Schmued L, Kyriakidis K, Heimer L. 1990. In vivo anterogradeand retrograde axonal transport of the fluorescent rhodami-nedextranamine, Fluoro-Ruby, within the CNS. Brain Res526:127–134.

Seelke AMH, Padberg JJ, Disbrow E, Purnell SM, Recanzone G,Krubitzer L. 2012. Topographic maps within Brodmann’s



area 5 of macaque monkeys. Cereb Cortex 22:1834–1850.

Shima K, Tanji J. 2000. Neuronal activity in the supplementaryand presupplementary motor areas for temporal organi-zation of multiple movements. J Neurophysiol 84:2148–2160.

Shima K, Mushiake H, Saito N, Tanji J. 1996. Role for cells inthe presupplementary motor area in updating motorplans. Proc Natl Acad Sci U S A 93:8694–8698.

Siegel S. 1956. Nonparametric statistics for the behavioralsciences. New York: McGraw-Hill.

Smiley JF, Hackett TA, Ulbert I, Karma G, Lakatos P, Javitt DC,Schroeder CE. 2007. Multisensory convergence in audi-tory cortex. I. Cortical connections of the caudal superiortemporal plane in macaque monkeys. J Comp Neurol502:894–923.

Squatrito S, Raffi M, Maioli MG, Battaglia-Mayer A. 2001. Vis-ual motion responses of neurons in the caudal area PEof macaque monkeys. J Neurosci 21:RC130.

Stepniewska I, Preuss TM, Kaas JH. 1993. Architectonics,somatotopic organization, and ipsilateral cortical connec-tions of the primary motor area (M1) of owl monkeys. JComp Neurol 330:238–271.

Stepniewska I, Preuss TM, Kaas JH. 2006. Ipsilateral corticalconnections of dorsal and ventral premotor areas in newworld owl monkeys. J Comp Neurol 495:691–708.

Stepniewska I, Preuss TM, Kaas JH. 2007. Thalamic connec-tions of the dorsal and ventral premotor areas in NewWorld owl monkeys. Neuroscience 147:727–745.

Striedter GF. 2005. Principles of brain evolution. Sunderland,MA: Sinauer Associates.

Stuphorn V, Brown JW, Schall JD. 2010. Role of supplemen-tary eye field in saccade initiation: executive, not direct,control. J Neurophysiol 103:801–816.

Tanne-Gariepy J, Rouiller EM, Boussaoud D. 2002. Parietalinputs to dorsal versus ventral premotor areas in themacaque monkey: evidence for largely segregated visuo-motor pathways. Exp Brain Res 145:91–103.

Tian JR, Lynch JC. 1996. Functionally defined smooth and sac-cadic eye movement subregions in the frontal eye fieldof Cebus monkeys. J Neurophysiol 76:2740–2753.

Tokuno H, Tanji J. 1993. Input organization of distal and proxi-mal forelimb areas in the monkey primary motor cortex:a retrograde double labeling study. J Comp Neurol 333:199–209.

Tsujimoto S, Genovesio A, Wise SP. 2010. Evaluating self-generated decisions in frontal pole cortex of monkeys.Nat Neurosci 13:120–126.

Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D,Anderson CH. 2001. An integrated software suite forsurface-based analyses of cerebral cortex. J Am MedInform Assoc 8:443–459.

Vann SD, Aggleton JP, Maguire EA. 2009. What does the ret-rosplenial cortex do? Nat Rev Neurosci 10:792–803.

Virley D, Hadingham SJ, Roberts JC, Farnfield B, Elliott H,Whelan G, Golder J, David C, Parsons AA, Hunter AJ.2004. A new primate model of focal stroke: endothelin-1-induced middle cerebral artery occlusion and reperfu-sion in the common marmoset. J Cereb Blood FlowMetab 24:24–41.

Vogt BA, Laureys S. 2005. Posterior cingulate, precuneal &retrosplenial cortices: cytology & components of the neu-ral network correlates of consciousness. Prog Brain Res150:205–217.

Vogt C, Vogt O. 1919. Allegmeinere Ergebnisse unserer Hirn-forschung. J Psychol Neurol (Leipzig) 25:279–439.

Wang W, Isoda M, Matsuzaka Y, Shima K, Tanji J. 2005. Pre-frontal cortical cells projecting to the supplementary eyefield and presupplementary motor area in the monkey.Neurosci Res 53:1–7.

Wise SP, Boussaoud D, Johnson PB, Caminiti R. 1997. Premotorand parietal cortex: corticocortical connectivity and combi-natorial computations. Annu Rev Neurosci 20:25–42.

Wong-Riley M. 1979. Changes in the visual system of monoc-ularly sutured or enucleated cats demonstrable withcytochrome oxidase histochemistry. Brain Res 171:11–28.

Yamane J, Nakamura M, Iwanami A, Sakaguchi M, Katoh H,Yamada M, Momoshima S, Miyao S, Ishii K, Tamaoki N,Nomura T, Okano HJ, Kanemura Y, Toyama Y, Okano H.2010. Transplantation of galectin-1-expressing humanneural stem cells into the injured spinal cord of adultcommon marmosets. J Neurosci Res 88:1394–405.

Yokochi H, Tanaka M, Kumashiro M, Iriki A. 2003. Inferiorparietal somatosensory neurons coding face-hand coordi-nation in Japanese macaques. Somatosens Mot Res 20:115–125.

Yu HH, Chaplin TA, Davies AJ, Verma R, Rosa MGP. 2012. Aspecialized area in limbic cortex for fast analysis ofperipheral vision. Curr Biol 22:1351–1357.


K.J. Burman et al.

Date post:	09-Mar-2021
Category:	Documents
Upload:	others
View:	2 times
Download:	0 times

Patterns of Afferent Input to the Caudal and Rostral Areas of ......Patterns of Afferent Input to...

Documents