Relationships between interhemispheric cortical connections and visual areas in hooded rats

transcript

214 Brain Research, 417 (1987) 214-224 Elsevier

BRE 12744

Hardy C. Thomas and Sergio G. Espinoza Instituto de Fisiologia, Facultad de Medicina, Universidad Austral de Chile, Valdivia (Chile)

(Accepted 23 December 1986)

Key words: Visual cortex; Visual topography; Striate area; Extrastriate area; Callosal connection; Microelectrode mapping; Horseradish peroxidase; Rat

The correlation between visual topography within striate and lateral extrastriate visual cortex and the pattern of callosal connections to those areas has been studied in gray rats. The procedure was to put multiple injections of horseradish peroxidase (HRP) into the occipital cortex of the right hemisphere. The cortical areas 17 and 18a in the left hemisphere were electrophysiologically mapped upon stimulation of the right eye. Reference lesions were placed at selected recording sites. Horizontal sections of the left cortex were reacted for the demonstration of HRP. This permitted the comparison of the visual and callosal maps in the same animal. Like in other mammals, the callosal projections coincide with the cortical representations of the vertical midline and the more central regions of the visual field. The heavy line of labelled neurons and terminations embedded within the primary callosal band at the 17/18a border coincides with the representation of the vertical meridian. It provides the boundary between V1 and the maps located lateral to it. In area 18a, the anterolateral collosal 'ring' contains two new maps labelled rostrolateral areas. The lateral acallosal 'body' contains 3 maps: area anterolateral is contained in its anterior half, whereas areas lateromedial and laterointermediate are contained in its posterior half. The acallosal 'island', caudal to the acallosal 'body', contains the map known as posterolateral. There are two laterolateral (LL) maps which coincide with the acallosal 'islands' lateral to the acallosal 'body'; laterolateral anterior is more rostral than LL and these are retinotopically organized as mirror images of each other. Lateral to LL, there is a suggestion of an additional map, which could correspond to a pararhinal area. These results may be useful to understand aspects of a basic mammalian plan in the organization of visual cortex.

INTRODUCTION

Anatomical studies 4,22 have shown that the callosal

projection in the occipital cortex of the rat consists of

a complex and reproductible pattern.

There is a dense band of projections which runs

rostrocaudally along the 17/18a border, which ac-

cording to mapping studies 1'7'14'2° contains a repre-

sentation of the vertical midline of the contralateral

visual field (VF). The lateral extrastriate cortex ap-

pears subdivided into callosal and sparcely callosal

regions. They give rise to conspicuous features 4,

namely: an anterolateral ' r ing' , a lateral sparsely cal-

losal 'body' and sparsely callosal ' islands' in lateral

and posterior area 18a. This region of cortex contains

a number of separate visual maps 7'a4,2°. The medial

extrastriate cortex also receives a callosal input con-

sisting of two tongues of projections. This area con-

tains two visual maps of the more peripheral regions

of the VF 7'32.

Area 17 is connected to areas 18a and 18. The pro-

jections are distributed into multiple extrastriate

fields 15, which in turn connect reciprocally with

striate cortex 18. These fields of intrahemispheric pro-

jections are surrounded by strips of callosal cells and

terminations 19.

In the present study we have made a detailed cor-

relation of the interhemispheric corticocortical con-

nections with the visual topography in the rat. We

combined microelectrode mappings in area 17 and

the lateral extrastriate cortex with tracings of the cal-

losal connections in the same animal.

Correspondence: S.G. Espinoza, Instituto de Fisiologia, Facultad de Medicina, Universidad Austral de Chile, Casilla 567, Valdivia, Chile.

Our results define the correspondences between the visual and callosal plans. In addition, the features of the callosal pattern have helped us to further eluci- date the plan of extrastriate visual areas. We describe here new representations of the VF which had passed undetected in previous physiological mapping experiments in rats.

When compared to other species, these results may be useful to understand aspects of a basic mammalian plan concerning visual cortical organization. Also, they provide a framework for further anatomical, physiological and psychophysiological studies on the role of the visual areas in the rat.

MATERIALS AND METHODS

Thirteen adult hooded rats of the A x C strain were used in these series. The aim was to correlate the visual topography within the visual cortex with the callosal pattern in the same animal. The procedure was to inject horseradish peroxidase (HRP) into almost the entire occipital cortex in one hemisphere. Cortical areas 17 and 18a in the opposite hemisphere were mapped by microelectrode recordings of single cell action potentials. Reference lesions were placed at selected recording sites. At the end of the recording sessions, the brains were perfused and processed for the demonstration of callosally projecting neurons and terminations.

At the beginning of the experiments, each animal was anesthetized with urethane, with supplements as needed. A wide opening was made in the skull over the occipital cortex of both hemispheres. The dura was left intact. Next, 20-30 injections of HRP (Sig- ma type VI) were distributed 1 mm apart over the occipital cortex in the right hemisphere. The tracer was delivered by pressure through a micropipette about

80/~m tip diameter. For each injection, volumes were about 0.2/zl of a 30% solution of HRP in saline, at a cortical depth of 0.5 mm, during 10 min.

Next, the topography of the VF representations within the left visual cortex was determined. The positions of receptive fields (RFs) for single neurons or clusters of neurons were related to the locations of the corresponding recording sites. The procedures for microelectrode recording were similar to those of a previous study 7. Glass micropipettes filled with 2 M NaC1 were stereotaxicaUy guided. We focused the at-

tention on the lateral extrastriate cortex. Most of the visual maps there lay over the convex surface of the brain, so the recording electrode was tilted laterally by 30 °. This ensured penetrations normal to the pial surface and provided accuracy in the mappings and reconstructions. RF boundaries were delimited by using spots, bars, edges and flashes of light of varying sizes. They were manually lit with a slide projector on the concave side of a perimeter centered over the

right eye. The eye was immobilized by suturing it through the

equator to a metal ring. This was anchored to the head-holder. The adequacy of this technique was as- certained by repeatedly plotting the projection of the optic disk. The vertical meridian was located 60 ° na-

sally to this projection. It usually coincided with the midsagittal plane of the animal. The horizontal meridian was located 30 ° under this projection 1'25.

Upon completion of the recording sessions, the tip

of the microelectrode was painted with India ink and the full width of the cortex was lesioned at selected recording sites. The brain was perfused through the left carotid artery. Horizontal sections of the left cortex were reacted for the demonstration of HRP using tetramethylbenzidine (TMB) as the chro- mogen 12. Survival time was about 24 h.

RESULTS

The central insets of Figs. 1 and 2 show a low-power photomicrograph of a horizontal section of the left cortex, reacted for the demonstration of HRP. It

contains the pattern of callosally projecting neurons and terminations revealed after multiple injections of HRP in the cortex of the right hemisphere in one animal 21'22. To avoid the infragranular layers containing

widespread callosal connections 2x, it was taken at a level above layer V. The recording sites have been reconstructed according to the lesions. The RF for each penetration is depicted in the perimeter charts representing the right eye VF. The RF plots in the charts correspond to cortical sites located within dif- ferent areas of the left cortex, labelled V1, rostrolateral (RE), anterolateral (AL), lateromedial (LM), (Fig. 1); laterolateral anterior (LLA), laterolateral (LL) and laterointermediate (LI), (Fig. 2).

As in previous studies 1'7'14, the boundaries be-

tween any two neighboring areas could be defined on

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Fig. 1. Central inset: low-power photomicrograph of a tangential section, left flattened occipital cortex, reacted for HRP. It shows the pattern of callosal connections demonstrated after multiple injections of HRP into the right cortex. Recording sites, (numbered from right to left and from top to bottom) have been reconstructed according to lesions placed at selected recording sites. The locations of areas containing representations of the right eye VF are indicated: primary visual area (V1), areas rostrolateral (RL), anterolateral (AL), and lateromedial (LM). B regma taken as zero for the reference axes; scale in ram. RFs identically numbered and corresponding to the recording sites in V1, RL, A L and LM, are plotted in the perimeter charts of the right eye VF. HM and VM in upper right chart indicate horizontal and vertical meridians, respectively; scale subdivisions, 20 ° . Asterisk in lower right and subsequent charts is projection of optic disk.

the basis of characteristic changes in the RF progres- sions when recording from one area to the other. It was evident that the layout of these areas was corre- lated with the features of the callosal pattern. The lateral border of V1, which contains the representation of the most nasal VF and the vertical meridian,

was in register with the primary band of labelled cells and terminations which runs rostrocaudally along the 17/18a border (points 3, 16, 29, 41 and 55, Fig. 1).

The sparcely callosal body in lateral extrastriate cortex contained 3 maps: AL was located in its anterior half, whereas LM and LI were contained in its

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Fig. 2. Same animal as in Fig. 1, demonstrating location of areas laterolateral anterior (LLA), laterolateral (LL) and laterointermediate (LI). The location of each area with respect to the callosal map and its visual topography can be deduced by correlating the RF distribution in each chart with the corresponding recording sites. RF plots for recording sites in LLA, LL and LI are shown.

posterior half (Figs. 1 and 2). Areas LL and L L A

were located outside the body, immediately lateral to it. Their location coincided, at least in part, with the

lateral sparcely callosal islands located lateral to the sparcely callosal body (Fig. 2).

In previous mapping studies 7'2°, LL was identified

as a single map and the rostrocaudal displacement in

cortex determined a lower to upper VF progression of RFs. In the present experiment, this was true at

the rostral end (.points 35-37 and 48-50, respectively, Fig. 2, chart LLA). However, a more caudal ex-

ploration (points 63-65, Fig. 2) gave rise to RFs lo-

cated again lower in the VF. Therefore, we could subdivide it into two separate maps.

In this animal, the most rostral mediolateral exploration (points 1-12, Fig. 1) started in V1 and passed

across the caudal end of the anterolateral callosal

ring. Points 1-3 corresponded to V1, giving rise to a

temporal to nasal progression of RFs. Point 3, representing the vertical meridian, was located at the me-

dial border of the ring. Points 3-5 , inside the ring,

gave rise to a nasal to temporal progression of RFs. Point 6, at the lateral border of the ring corresponded

to an RF located again close to the vertical meridian

TEMPORAL

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Fig. 3. Same conventions as in previous figures. A detailed exploration through the rostral end of V1 and the anterolateral callosal ring in another animal. Definition of areas V1, rostrolateral medial (RL-m), rostrolateral lateral (RL-I) and AL.

(chart RL, Fig. 1). Points 6-12 gave rise to a nasal to temporal progression of RFs located in upper VF, thus corresponding to the rostral end of the AL map (chart AL, Fig. 1). This suggested that the anterolateral callosal ring could contain a separate representation which was labelled rostrolateral (RL).

Fig. 3 shows an experiment in another rat. Here there was a more finely grained exploration through the anterolateral callosal ring. Points 2, 6 and 19, representing the vertical meridian at the lateral border of V1, were located in the medial border of the ring.

As in the experiment of Figs. 1 and 2, the mediolateral exploration through the ring gave rise first to a nasal to temporal progression of RFs (points 2-3 and points 6-9, chart RL-m, Fig. 3). Point 9, at about the center of the ring, represented an RF located at the azimuth 60 °. Points 9-12 represented RFs which pro- gressed again from temporal to nasal VF (chart RL-1, Fig. 3). Point 12, at the lateral border of the ring, represented again the vertical meridian. This allowed us to consider the ring as containing two separate representations of the nasal regions of the visual field. We

suggest labeling them rostrolateral areas (RL), with a medial (RL-m) and a lateral (RL-1) subdivision. RL-m appears as a mirror image of V1, with the upper VF located caudally and the lower VF, rostrally. The upper-lower VF topography in RL-I is more difficult to ascertain. As in the previous experiment, the cortex lateral to the ring (points 12-15 and 19-25,

chart AL, Fig. 3) contained the anterolateral (AL) map.

Fig. 4 is a reconstruction of an experiment in another rat. There was a detailed exploration of the middle third of areas 17 and 18a. This experiment demonstrated that the representation of the vertical meridian (points 4, 13 and 29, Fig. 4), common to V1

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Fig. 4. A detailed exploration through V1, the posterior half of the acallosal 'body' and the lateral acallosal island, with the locations of V1, LM, LI and LL in another animal.

and LM, coincided exactly with the heavy line of labeled neurons and terminals embedded within the primary callosal band at the 17/18a border. The lower half of the acallosal body contained the LM and LI maps. As in the experiment of Figs. 1 and 2, the points at the LM/LI border, representing RFs 1o-

cated far temporal in the VF, were located in the

sparsely labelled center of the posterior half of the acallosal body in area 18a (points 33, 46 and 60, Figs. 1 and 2; points 18 and 33, Fig. 4). The points representing the LL/LI border, which contain a representation of the vertical meridian of the VF, were lo-

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Fig. 5. A detailed exploration demonstrating locations of V1, LM and posterolateral (PL), another animal.

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Fig. 6. Surface view of whole left hemisphere. Schematic retinotopic map of striate and lateral extrastriate cortex over the callosal pattern (dotted) of a control rat, as derived from Figs. 1-5. The features relevant to the determination of subdivisions of extrastriate cortex were emphasized. Abbreviations: R.E.V.F., right eye visual field; VM and HM, vertical and horizontal meridians, respectively; u., upper field, 1., lower field. Abbreviations for the visual areas as in previous figures.

cated in the heavily labelled lateral border of the acallosal body (points 35, 48 and 63, Fig. 2; points 21

and 36, Fig. 4). As in the experiment of Figs. 1 and 2,

the LL map was located in the more caudal acallosal island immediately lateral to the acallosal body. No-

tice in the animal of Fig. 4 that the border at the caudal end of LL was point 39, which corresponded to an

RF located in the far periphery of the VF. However, point 40, more lateral, gave rise to an RF located

more nasally (chart LL, Fig. 4). This suggests a new possible map, which might be labelled pararhinal

(Pa). In the rat of Fig. 4 it is worth comparing the distri-

bution o¢ label in V1 and LM through the callosal

band across the 17/18a border. In V1, the label could

be seen approximately between points 3-4, 12-13 and 27-29. In the V1 map, this corresponded to the

most nasal aspect of the VF, from approximately the vertical meridian to the azimuth 20 ° (Fig. 4, chart

V1). In LM, the callosal label was present between points 4-5, 13-14 and 29-30, respectively. In the

LM map this corresponded to the same extent of the

VF as in the V1 map, namely, from the vertical meridian to the azimuth 20 ° (Fig. 4, chart LM). In other

words, the distribution of callosal neurons and termi-

nations was the same, in proportion, in V1 and LM.

A similar result seemed true when comparing this for

V1 and AL in the rat of Figs 1 and 2. An exact estima-

tion of this feature for RL, LI and LL was more difficult with the present material, but as a first impres-

sion this may also hold true for these later maps.

Fig. 5 shows an experiment in another rat in which

there was a more caudal exploration through V1 and area 18a. This allowed identification of V1, LM and

posterolateral (PL). It can be seen that in PL, as in LM, the medial to lateral displacement in cortex gave

rise to a nasal to temporal progression of RFs. How-

ever, the rostral to caudal displacement produced an upper to lower progression of RFs (points 41-46,

chart PL, Fig. 5). The boundary between LM and PL

was seen to coincide precisely with the labelled callosal band separating LM and PL (points 32-37, Fig.

5). Two visual maps have been described 7'32 in area 18

for both mouse and rat, namely anteromedial (AM) and posteromedial (PM). With respect to these noth-

ing can be said from the present experiments, since

the cortex medial to V1 was not explored in these se-

ries. Fig. 6 shows a summary diagram of the present re-

suits. Superimposed on the callosal map (dots) of a

control rat, there is a retinotopic map of striate and lateral extrastriate visual cortex of the left hemi-

sphere. It was derived from the experiments shown in Figs. 1-5. The representation of the visual midline

was in register with the heavily labelled landmarks of the callosal pattern, namely: the heavy line era-

bedded in the callosal band at the 17/18a border, the

medial and lateral borders of the anterolateral callosal ring and the lateral border of the acallosal body. The less dense regions of the callosal map corresponded to the representation of more peripheral zones of the VF both in V1 and the lateral extra striate maps.

DISCUSSION

The present study shows that in rats, as in other mammals, the callosal projections in occipital cortex coincide with the representations of the vertical meridian and the more central regions of the VF. By a combination of anatomical and physiological tech- niques, we have directly compared the callosal and

visual maps in the same animal. This demonstrated that the callosal pattern in visual cortex provides an accurate landmark for the layout of the striate and several extrastriate visual areas. In addition, this allowed us to define new visual topographic maps, which had passed undetected in previous physiological explorations in rats.

Callosal inputs and area boundaries in the rat

The callosal band at the 17/18a border overlaps the cortical representation of the more nasal aspects and

the vertical meridian of the VF, common to V1 and the maps located immediately lateral to it (Fig. 6).

In area 18a, the anterolateral callosal 'ring' contains two new mirror image representations of the nasal regions of the VF, which we propose to be named RL-m and RL-1. The lateral sparsely callosal 'body' contains 3 maps: AL is placed in its anterior half, whereas LM and LI are located in its posterior half. The sparsely callosal 'island', caudal to the acallosal body, contains the map known as PL. We have defined two laterolateral maps which are located in the acallosal islands, lateral to the acallosal body. LLA is more rostral than LL, and they are retinotopically organized as mirror images of each other (Fig. 6). Lat- eral to LL there is a suggestion of an additional map, which could correspond to area PR.

The heavy line of labelled callosal neurons and terminals embedded within the primary callosal band at the 17/18a border 4 coincides precisely with the representation of the vertical meridian, providing the boundary between V1/RL-m, V1/AL, V1/LM and

V1/PL. The boundaries between RL-1/AL, LI/LLA, and LI/LL, which correspond again to vertical meridian representations are likewise coincident with cal-

losal densities, namely: the latera| border of the callosal ring and the lateral border of the acallosal body, respectively. The boundaries which correspond to RFs located in the VF periphery are coincident with regions of less dense callosal projections: RL-m/ RL-1, at the center of the anterolateral callosal ring; LM/LI, at the center of the lower half of the acallosal body and possibly LL/PR (Fig. 6).

Mutiple visual areas in the rat

It has been recognized by anatomical 13'aS'1s'19 and physiological mapping experiments 1'7'14'2° that both

lateral and medial extrastriate cortex in rats contain a number of visual representations. The results out- lined above provide further support to this notion. They are in close agreement and fulfill most of the predictions of a previous study 19 which morphologi- cally defined the plan of extrastriate visual areas in the rat. Its relevance to the present findings will be discussed in detail. It was shown that the intrahemispheric striate-extrastriate projections (demonstrated by autoradiography) are distributed precisely into areas of cortex of less dense interhemispheric connections (demonstrated by HRP). By this ap- proach, the various areas and their relation to the callosal pattern were discerned. In general, the present distribution agrees with it. However, we now add the RL areas which were not defined in that or other anatomical 13'15'18'19 or physiological 7'14'2° studies in rats.

Also, the present partition of the laterolateral areas into two mirror images, predicted in the mentioned study, had not been defined in earlier physiological experiments. The same holds for the present suggestion of a possible PR map.

No direct connections from VI were described 19 for the anterolateral callosal ring. This may be due to

the fact that the tracer injections in V1 did not cover the nasal aspects of the VF, which, as we have demonstrated in the present experiments, is just the region represented in the RL areas.

The study discussed predicted further visual representations into two additional small fields (P) of corticocortical terminations. These project into two acallosal islands in posterior area 18a close to the caudal pole. Those were not confirmed in the present series,

since that area of cortex was not explored in suffi- cient detail.

Area 18, medial to VI, which according to physiological studies 7'32 contains two maps (AM and PM) of

the temporal aspects of the VF, was not studied in the present experiments.

Relation to other species

It has been pointed out that in a variety of species,

the representation of the vertical meridian makes up the border of the majority of the visual areas 29. Also,

that the callosal fibers terminate selectively at re-

gions where the vertical meridian of the VF is repre- sented3,11, 33.

From this, the usefulness of the callosal pattern for discerning the organization of extrastriate visual cor-

tex has been established in several species besides the rat.

Callosal recipient zones related to area boundaries

were demonstrated for V2, MT, VP and DM in the owl monkey 16. In the macaque monkey it helped to

locate 5 extrastriate areas: V2, V3, V3A, V4 and VP 30'31'34. The comparison of the physiological map-

pings 2s with the distribution of the callosal pathway in cat visual cortex 6'23 gives support to this correlation

in areas 17, 18 and 19. Also, for the V1/V2 boundary in the mouse, rat, hedgehog and rabbit 4'9'27.

In the gray squirrel, the primary callosal band (with its periodic appearance in this species) was cor- related with the V1/V2 reversal of RFs 8. For the rest

of the callosal pattern, the comparison with the avail- able physiological mappings 1° was more difficult in

the squirrel.

A common plan of visual areas in the rodent

The plan of visual areas proposed in the present

study for the rat, while being more elaborate, shows

several features in common with those reported for related species such as guinea pig 2, mouse 5'32, golden hamster 26, grey squirrel 1° and Octodon degus 17. These latter patterns could be regarded as contained

in the more complex one of the rat. However, the plans of callosal connections reported for mice 4 and

grey squirrels s appear as elaborate as that of the rat.

Also, the plan of intrahemispheric corticocortical connections reported for mice 24 and even rabbits a3 is

similar to that of the rat. Moreover, when examined

in retrospect, some of the data from physiological

mappings in mice 32 and grey squirrels 1° could be in-

terpreted similarly as we have done in the present

study with the rat. For example, in the mouse it was reported 32 that in the central part of the lateral ex-

trastriate cortex there was a second reversal in iso-azimuth lines, indicating an additional representation

of the nasal lower VF. This is equivalent to that at the

LM/LI boundary of the present map. Also, it was re-

ported that in the extreme posterior aspect of V2,

there was a reversal in iso-azimuth lines as one pro- ceeds laterally, yielding a partial reduplication of the

upper temporal VF. There was also an indication of a

small additional representation of the lower nasal VF in the extreme posterior aspect of V3. None of these

zones were defined as separate in the mouse. Also, in

the squirrel 1°, two reversals were reported in medial

to lateral explorations in lateral extrastriate cortex, comparable to the present data. Further distinctions

dependent on rostral to caudal explorations were not

reported. From this, it is possible that the lateral extrastriate cortex in mice and squirrels, after pertinent

study, could be divided in the manner we suggest now for the rat. All the above considerations raise the

possibility of a basic plan of visual cortical areas com-

mon to rodents, which could be extended to logo- morphs and even higher mammals, such as cats and

monkeys. Finally, the close correspondence between the in-

ter- and intrahemispheric connections with the VF topography demonstrated in the present study,

should prove useful for further characterizing the vis-

ual areas in rats with respect to their interconnections

and their role in visual behavior.

ACKNOWLEDGEMENTS

This work was supported by D.I.D., U.A.Ch., Proyecto RS-83-43, and FONDECYT, Proyecto

1053-85, to S.E. The authors are grateful to Jorge E.

Subiabre for technical assistance.

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Relationships between interhemispheric cortical connections and visual areas in hooded rats

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