Brain Research, 509 (1990) 71-79 Elsevier

71

BRES 15186

Commissural connections between the auditory cortices of the rat Karin R(ittgers, Andreas Aschoff* and Eckhard Friauf** Department of Animal Physiology, University of Tabingen, Tiibingen (E R. G. ) (Accepted 11 July 1989)

Key words: Auditory cortex; Rat; Wheat germ agglutinin conjugated horseradish peroxidase; Fluorescent dye; Double-labeling; Commissural connection; Mapping rule

The pattern of commissural connections of the rat auditory cortex (AC) was investigated with injections of wheat germ agglutinated horseradish peroxidase into the AC. Homotopic and heterotopic patches of neurons were retrogradely labeled in the contralateral hemisphere. Each injection labeled neurons at the corresponding contralateral site, i.e. the homotopic site. In addition, retrogradely labeled neurons were found at non-corresponding locations in contralateral AC, i.e. at heterotopic locations. The pattern of heterotopic labeling changed systematically with the injections. Mapping rules were established that led to the parceUation of areas 41 and 36 into 6 fields. Four fields were defined in Krieg's area 41 (primary AC) and two fields in Krieg's area 36 (secondary AC). In area 41 the heterotopic connection is not reciprocal; in area 36, however, heterotopic projections are organized recfprocally. Contrary to the visual cortex, homotopic and heterotopic projection neurons were equally distributed across the cortical laminae. With double-label experiments it could be shown that a considerable number of the neurons in area 41 bifurcate and project to homotopic as well as to heterotopic sites in the contralateral hemisphere. We conclude that in the AC there are several subtypes of neurons projecting to the contralateral hemisphere; it would be of interest whether these anatomical differences are manifested by physiological differences.

INTRODUCTION In a n t e r o g r a d e d e g e n e r a t i o n and r e t r o g r a d e tracing studies it has been shown that cortical areas differ in several aspects of their commissurai connections 1,1~, 18,22,42. For e x a m p l e a great variability is seen in the density of the commissural connections and in the specific patterns of commissural connectivity (for review see ref. 16), C o m m o n to all commissural connections is the mainly h o m o t o p i c nature of p r o j e c t i o n , i.e, a projection to c o r r e s p o n d i n g sites in the contralateral h e m i s p h e r e (for review see ref. 16). Nevertheless recent p a p e r s r e p o r t m o r e and m o r e h e t e r o t o p i c projections, i.e. projections to n o n - c o r r e s p o n d i n g sites in the contralateral hemisphere. Such h e t e r o t o p i c projections have been found in a wide variety of species ( m o n k e y 3'9'12,2°,36,37, cat ~,8'22, 23.35, tupaia31 and rat27'4t). The commissural connections between the auditory cortices ( A C ) are r a t h e r dense and acommissural regions are lacking 1"4"~1'22. The p a t t e r n of commissural connectivity of the A C underlies species-specific differences. Strong and e l a b o r a t e h e t e r o t o p i c commissural connections originate in the rhesus m o n k e y from the association

areas 28 and in the cat from p r i m a r y AC 6"22. In the rat, both p r i m a r y and s e c o n d a r y A C p r o j e c t h o m o t o p i c a l l y to the contralateral side32; as yet h e t e r o t o p i c connections have not been described in this species. G r a n g e r et al. 11 (rat) and Yorke and Caviness 42 (mouse) r e p o r t a homogeneous distribution of the s o m a t a of commissural p r o j e c t i o n neurons across the A C . In contrast, terminals of commissural p r o j e c t i o n n e u r o n s are r e p o r t e d l y nonh o m o g e n e o u s l y distributed across the A C of the rat, and are c o n c e n t r a t e d in patches or stripes in area 414'3~'43. A s s u m i n g a strict h o m o t o p y , (as it was shown for example by Porter and W h i t e 3°) one would expect the distribution p a t t e r n for s o m a t a and terminals to be the same. The present study aims to analyze the commissural connections of rat A C in further detail. The following specific questions were addressed. (1) A r e the commissural projections b e t w e e n the auditory cortices only h o m o t o p i c or also h e t e r o t o p i c ? (2) If there are heterotopic projections, do h o m o t o p i c and h e t e r o t o p i c projections originate from the same neurons via collaterals or are there different subsets of neurons which project only to the h o m o t o p i c or only to the h e t e r o t o p i c site? (3) A r e there differences in the commissural connections of the primary and secondary A C ?

* Present address: Institute of Anatomy, University of Lausanne, Lausanne, Switzerland. ** Present address: Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, U.S.A. Correspondence: K. Rfittgers, Department of Animal Physiology, University of Tiibingen, Morgenstelle 28, D-7400 T/Jbingen, F.R.G. 0006-8993/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)

72 MATERIALS AND METHODS The present data were obtained from 45 adult female rats (Sprague-Dawley, 170-250 g). They were anesthetized with ketamine hydrochloride (100 mg/kg; i.m.) and xylazine (2 mg/kg; i.m.). The temporal cortex was exposed and stereotaxic 29 injections of horseradish peroxidase (HRP), wheat germ agglutinated horseradish peroxidase (WGA-HRP) or fluorescent dyes were made into parts of the AC; the injection sites did not reach the white matter. There were 35 cases with single injections of 3-5 nl WGA-HRP (5%); in 4 cases multiple (25-28) injections, each of about 10 nl HRP (10%), were made which covered the whole temporal cortex. In addition 6 double-labeling experiments with Fast blue (FB) and Diamidino yellow (DY) were carried out; in these cases the appropriate location of the injections was estimated according to the data obtained in the HRP experiments. Pressure injections were made with calibrated glass pipettes which had a tip diameter of about 30/~m. Before and after the injection the pipette was left in place for 15 rain in order to reduce backflow of the tracer along the pipette's shaft. After a survival time of 24 h (HRP and WGA-HRP) or 5 days (fluorescent dyes) the animals were transcardially perfused. For animals with HRP or WGA-HRP injections fixation and histochemistry were performed according to the protocol of Mesulam26. Brains with injections of fluorescent dyes were perfused with buffered formaldehyde (8%). Brains with multiple injections of HRP were cut horizontally; all sections were processed for HRP and counterstained with Neutral red. In two brains 6 equidistant sections through AC were drawn with the aid of a camera lucida; labeled neurons within supragranular and infragranular layers were counted. The percentages and means were calculated. All other brains were cut in the transverse plane. The position of labeled neurons as well as the location and extent of the injection site were plotted and reconstructed onto standardized side views using a computer program; all data were projected onto left hemispheres so that corresponding sites of both hemispheres appear at one site in the reconstruction. A Nissl-stain series was made for every brain and the locations of characteristics in the cortex itself and structures associated with it (e.g. caudal begin of the cortex, location of the rhinal fissure, rostrocaudal and dorsoventral extent and location of koniocortex, first appearance of the corpus callosum, first appearance of the granule cells in the dentate gyrus and other characteristic hippocampal cell masses) of the different brains were determined and standardized. This was necessary on the one hand for the precise evaluation of the location of the injection site and the labeled neurons in one animal and on the other hand to be able to directly compare the results between different individuals.

numbers of labeled neurons in supra- and infragranular layers of one brain are listed. Counts in another brain revealed similar percentages (41% supragranular, 59% infragranular). The highest proportion of commissurally projecting cell bodies were found in the infragranular layers (roughly 60%); in the supragranular layers, the n u m b e r of labeled commissural neurons was smaller (roughly 40%). However, there were more weakly stained n e u r o n s in infragranular layers than in supragranular layers. Layer I was always without labeled cell bodies (Fig. 1). Labeled neuropil was seen in all cortical layers, but it was densest in deep layer I. It is likely that anterograde transport contributed mainly to the labeled neuropil in layer I since only few dendrites of rat A C neurons reach into this layer 1°.

Single H R P injections Areal distribution. After single small injections into the A C retrogradely labeled n e u r o n s in the contralateral hemisphere were confined to patches. Homotopic to the injection site always one patch of labeled n e u r o n s was seen. It had the same size as the center of the injection site. In addition to that homotopic patch there was at least one heterotopic patch of retrogradely labeled neurons. The labeled heterotopic neurons were fewer and the labeling was lighter than in the homotopic neurons (Fig. 2). In none of the experiments could we find a continuity of labeling between the homotopic and heterotopic patches of neurons. In other words, there was always an obvious discontinuity in the distribution of cells of origin. Since we always used W G A - H R P in these experiments, which has been shown to be not taken up by intact fibers of passage 2, we thus conclude that neurons of rat A C form heterotopic commissural connections.

TABLE I RESULTS

Multiple H R P injections Areal distribution. Multiple injections of H R P into the A C resulted in labeling of n e u r o n s which were distributed over the whole contralateral AC. The tangential distribution of the commissural n e u r o n s in the temporal cortex within area 41 (primary A C ) and area 36 (seco n d a r y A C ) of Krieg 25 was homogeneous. In the perirhinal and entorhinal regions labeled neurons were seen only occasionally, although the injections reached into these regions. They had the weakest commissural connectivity observed in the regions surr o u n d i n g AC. Laminar distribution. In Table I the percentages and

Percentage (and number) of supragranular and infragranular HRPlabeled neurons after multiple injections into the contralateral hemisphere Labeled neurons in supragranular and infragranular layers are shown. Sections 76 and 176 are the AC's most dorsal and ventral sections, respectively.

Section

76 96 116 136 156 176 mean

% (number) of labeled neurons Supragranular

Infragranular

50(24) 37(28) 33 (157) 36(143) 42(159) 29(52) 38

50(24) 63(48) 67(321) 64(249) 58(219) 71 (130) 62

73

Fig. 1. Horizontal section through the AC after multiple injections of HRP into the contralateral hemisphere (counterstained with Neutral red). Rostral is at the top, medial at the right. Arrowheads indicate caudal and rostral border of the AC. Scale bar: 500 ~m.

The areal distribution showed patterns that are described as follows. There was a topographic relationship between the injection site and the location of the homotopic as well as the heterotopic patch. The topographic relationship for the homotopic patch was naturally very simple: it was congruent and thus always coincided with the injection site. For the heterotopic patch the situation was more complicated. A change of the location of the injection site resulted in a corresponding shift of the location of the heterotopic patch.

However, this shift was not necessarily going into the same direction as the injection site. In other words, if the injection site was displaced some distance towards dorsal from one experiment to another, the corresponding heterotopic patch did not always move dorsal, too, but sometimes moved rostral. We observed systematic differences in the topographic relationships of the heterotopic projections which led us to identify specific mapping rules. Each rule was only valid for a restricted part of the AC. The existence of different mapping rules allowed us to parcellate several fields within the AC. The change of the mapping rule for the heterotopic projection marked the border of a field. If an injection was entirely located within one of the defined fields the labeling was confined to one homotopic and one heterotopic patch (Fig. 3a,b). Injection sites affecting two fields produced one homotopic patch and two heterotopic patches (Fig. 3c,d). If the injection site affected more than two fields, consistently more than two heterotopic patches were labeled (not shown). The number of heterotopic patches thus always equaled the number of fields involved in the injection site. The combination of all data resulted in the definition of 6 fields in the AC. Within each field, one common mapping rule could be identified. Among the 6 fields, however, the mapping rules showed considerable differences. Four fields (fields I - I V Fig. 4a-d) lay in Krieg's area 41 and two (fields V and VI Fig. 4e,f) in area 362s. The fields were exclusively defined by the mapping rules of their heterotopic patches and not by cytological or histochemical criteria. The exact extent of these fields could not be determined, because the injections were not infinitely small. In Fig. 4 the 6 fields and their mapping rules are shown; each part of the figure represents one field with the organization of its homotopic and heterotopic projections. Fig. 4a shows field I; the area shown in outline is the region for which one mapping rule exists. Field I covers the most rostral part of area 41. Injections into this field resulted in homotopic labeling and in heterotopic labeling within a field I" (stippled outline), caudodorsal to field I. The axes show the mapping rule. Field I and field I" have one parallel axis; injection sites located rostroventral (indicated by filled star in Fig. 4a) and caudodorsal (indicated by open star in Fig. 4a) in field I will produce homotopic and heterotopic labelings laying rostroventral or caudodorsal, respectively. The other axis of field I and field I" is rotated by 180 ° and is thus called antiparailel; injection sites located rostrodorsal or caudoventral in field I produce heterotopic patches that are caudoventral and rostrodorsal, respectively. Field II (Fig. 4b) lies in the center of area 41; the

74

a

Fig. 2. Transverse section through the injection site (2a) and the contralateral hemisphere with retrogradely labeled commissural neurons (2b). In 2a dorsal is to the top and lateral to the left; in 2b dorsal is to the top and lateral to the right. RF: rhinal fissure. The arrowhead in 2b indicates the location of the homotopic, the arrow the location of the heterotopic patch of labeled neurons. Note that fewer neurons are labeled in the heterotopic patch. Scale bar: 500/~m.

related field of the heterotopic projection (field II') is located ventral to field II. The mapping rule of field II is depicted by two parallel axes; all heterotopic patches after injections into this field lay ventral to the injection site. Field III (Fig. 4c) is located just ventral to field II; the corresponding field of the heterotopic projection (field I I I ' ) is situated dorsal of field III. Like fields II and II" fields III and III" have two parallel axes; in contrast to field II, injections into field III always produced heterotopic patches dorsal to the injection site. Field IV (Fig. 4d) is most caudal in area 41; the field of heterotopic projection (field I V ' ) lies ventral to field IV. Fields IV and IV" have no parallel axis; both axes are rotated by 90 °. Injections along one axis resulted in a shift of the heterotopic patches along an axis that is rotated by 90 ° . Field V (Fig. 4e) is located in the caudal half of area 36; the corresponding field of heterotopic projection (field V ' ) covers the rostral half of area 36. The axes of

these two fields, which show the mapping rule for field V, are not parallel to each other but tilted to the curvature of the rhinal fissure. Field VI (Fig. 4f) is located in the caudal half of area 36, at the same site as field V'; like field V, the heterotopic field VI" covers the caudal part of area 36. The axes of fields VI and VI" are ~aot completely parallel, but slightly tilted to the curvature of the rhinal fissure. Laminar distribution. As in the cases with multiple injections, the majority of the labeled neurons were found in the infragranular layers after almost all injections. In some cases, however, more labeled neurons were found in the supragranular layers. The occurrence of these different patterns of laminar distribution could neither be correlated with the depth of the injection site nor with the location of the injection site in the AC. There was no obvious difference in the laminar distribution of homotopic and heterotopic neurons when the injections were placed within the auditory cortex. After injections into other cortical regions (e.g. part of

75

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Fig. 3. Examples of 4 reconstructions after injections into the AC. Side views of the cortex are shown. For the sake of clarity, ipsilateral and contralateral hemispheres are shown in one schematic drawing. The ventral border of the AC is depicted by the rhinal fissure indicated by the arrowhead in a. Injection sites are shown in outline. Each dot represents one labeled neuron found in the contralateral cortex, a,b: injections into one field result in one heterotopic patch; after injections into different fields the topographic relationships between homotopic and heterotopic patch are different• c,d: injections into two fields resulted in two heterotopic patches•

the secondary visual cortex, area 18a), however, heterotopic n e u r o n s were labeled almost exclusively in infragranular layers.

Injections of fluorescent dyes The pattern of retrograde labeling after injections of the fluorescent dyes FB and DY into the A C confirmed our obtained mapping rules. These experiments were carried out to examine whether individual n e u r o n s in one hemisphere bifurcate and project to two sites in the other

hemisphere• Therefore two injections were made into the areas of the homotopic and heterotopic projection originating from one site in the contralateral hemisphere; this was done by injecting appropriate sites of two related fields (e.g. I and I'). The two injection sites never overlapped. The experiments were carried out in area 41 only. In regions where homotopic and heterotopic labeling coincided, clusters of double-labeled n e u r o n s were found (Fig. 5). The exact percentage of the double labeling could not be calculated because the effective size

76 Fields in A r e a 41 a

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Fig. 6. Schematic illustration of the general organization of commissural connections of area 41 and area 36. Every site of the AC projects homotopically and heterotopicatly to the contralateral hemisphere. In area 36 all projections are reciprocal; in area 41, however, the heterotopic projection is not reciprocal. In area 41 there is a considerable number of neurons that bifurcate and terminate at the homotopic as well as the heterotopie site.

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of the injection sites was difficult to judge due to necrosis caused by the toxic fluorescent dyes.

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Fig. 4. Six fields of topographically organized commissural neurons in areas 41 (primary AC) and 36 (secondary AC). Fields were defined by mapping rules which were established by the topography of the heterotopic labeling patterns. For details see text. Solid lines, borders of homotopic fields. Dotted lines, borders of heterotopic fields. Topographic axes are indicated by open and filled stars or circles, respectively.

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Fig. 5. Fluorescent labeled neurons in one transversal section after injection of DY and FB into different sites within primary auditory cortex. Neurons labeled with FB, DY and double-labeled neurons are shown in separate plots. The rhinal fissure is indicated by arrowheads; the thin line depicts layer IV.

is that the whole auditory cortex of the rat is commissurally connected; there are n e i t h e r regions without commissural neurons nor variations in the density of the labeled neurons. This is in a g r e e m e n t with the findings of others in rat 11 and mouse 42 A C and stands in clear contrast to the distribution of commissural neurons described in the visual and s o m a t o s e n s o r y cortices of these rodents 11'42. In the visual cortex only those regions are commissurally connected which r e p r e s e n t the vertical meridian 4"11'42'43. In the s o m a t o s e n s o r y cortex commissural connections exist p r e d o m i n a n t l y in regions of r e p r e s e n t a t i o n of the b o d y midline11'41-43; (note however the contradictory results in ref. 1). The occurrence of commissural neurons all over a r e a s 36 and 41 could be a consequence of a different organization of space representation within the A C as c o m p a r e d to o t h e r cortical areas. It will be interesting to see w h e t h e r there is a functional space m a p in the rat A C . In and b e n e a t h the rhinal fissure no or merely a few neurons were labeled. This is in a c c o r d with previous reports 1'4'11'43 and shows that the phylogenetically older areas of the cortex have only sparse commissural connections c o m p a r e d to the neocortex, Laminar distribution. The commissura~ p r o j e c t i o n neurons were distributed over all l a m i n a e with a p r e p o n d e r ance of cells lying in the infragranular layers (Table I), This result is in a g r e e m e n t with the o u t c o m e of o t h e r investigations of the commissural p r o j e c t i o n in the

77 rat 11'17'19'39. In other species the commissural neurons are

found mainly in supragranular layers (cat) or entirely in supragranular layers (monkey). The difference in rats is interpreted as 'the less distinct lamination of the nonprimate cortex '21.

Single W G A - H R P injections Areal distribution. In this study each single injection of W G A - H R P resulted in labeling of one homotopic patch of neurons and one or more heterotopic patches of neurons in the contralateral hemisphere; the homotopic and the heterotopic patch always lay within the same cytoarchitectonic area, i.e. either in area 41 or in area 36. A study by Ryugo 3z reports only homotopic connections between the two hemispheres. In that study complete lesions of either primary or secondary AC were performed and therefore could not identify heterotopic projections within one area. Thus our data do not contradict Ryugo's results. Heterotopic commissural projections from primary areas to secondary areas have been described in the somatosensory 41 cortex and in the visual cortex 27 of the rat. There is also a heterotopic projection within the primary visual area 27. Heterotopic projections are thus a common feature within the cortex of rats, both within one cytoarchitectural area and also across a cytoarchitectural border. The massiveness and equal distribution of the heterotopic projection observed in the AC, however, are exceptional. Mapping rules could be established between both types of patches and the injection site. There are different mapping rules for the heterotopic projections; each rule holds true for a certain part of the AC. On the whole 6 mapping rules were found which led to the definition of 6 fields. The commissural connections of areas 41 and 36 are remarkably different concerning the reciprocity of their projections. The homotopic projections are by definition reciprocal; this is not the case for the heterotopic projections. As shown in Fig. 6 the heterotopic projections of area 36 are reciprocal; one place projects to the same heterotopic site from where it receives its heterotopic input. In contrast there is no reciprocity of the heterotopic projections in area 41; the site where the heterotopic input terminates is totally different from the site of the heterotopic input. The present study in rat AC has established parcellations of areas 41 and 36 in terms of their commissural connections. These parcellations are in complete accordance with the cytoarchitectural studies of Krieg 25 and Zilles 44. Other anatomical tracer studies of thalamocortical or corticocollicular connections in the rat A C 7"13'34'39 also found differences in the connectivity of primary and

secondary auditory areas. We therefore conclude that the cytoarchitectural delimitation of areas 41 and 36 in the AC is generally reflected by the pattern of afferent and efferent projections. As mentioned above heterotopic projections are not uncommon in the cortex of the rat 27m. One fundamental difference between the AC and other cortical regions is that there are heterotopic connections within primary and within secondary auditory regions, which were not observed in visual and somatosensory cortices. Therefore it is unlikely that the fields in the AC are a subpopulation of fields within a much larger mosaic. The commissural terminals in the rat AC are reportedly not homogeneously distributed 4"3s~43but form stripes or columns with more or less dense terminals. The areal distribution of the commissural neurons and their terminals conflicts with the concept of a strict homotopic projection from each AC to the contralateral hemisphere. As shown in this study, commissural somata are distributed homogeneously and there are homotopic as well as heterotopic projections. One could speculate that homotopic terminals are distributed homogeneously, while heterotopic terminals are arranged in stripes or patches 4'43. If this were the case one would expect differences in the strength of the heterotopic labeling according to the location of the injection site. Those differences could not be observed. The distance of the reported stripes 4 is relatively large (about 0.7 ram). Therefore our injections would have been small enough to reveal differences in the distribution of the commissural somata. At present we cannot tell whether the neurons have different degrees of collateralization which could also be the cause of heterogeneous commissural terminals. Laminar distribution. Homotopic and heterotopic neurons have the same laminar distribution, namely 55-60% in infragranular layers and 40-45% in supragranular layers. However, sometimes this ratio was inverted, It has been demonstrated that the supragranular layers project only to supragranular layers in the contralateral cortex18'42; therefore one would predict shallow injections to produce more labeled cells in supragranular layers than deeper ones. We suspect that those cases in which more labeled cells were found in the supragranular layers can be attributed to shallow injections, although we did not find a statistically significant correlation between the laminar distribution of labeled neurons and the depth of injection. Injections into regions adjacent to the AC labeled heterotopic neurons in infragranular neurons only; this feature was also found by Miller and Vogt 27 in the rat visual cortex. The fact that commissural neurons in rat AC are located in all laminae is therefore a unique

78 feature to distinguish the A C from other cortical areas.

Injections o f fluorescent dyes Two spatially separated injections of two fluorescent dyes (FB and DY) into one cortical hemisphere led to double-labeled n e u r o n s on the contralateral side (Fig. 1). Some commissural n e u r o n s bifurcate to make terminations at two distinct sites. The feature of the commissural connections of the A C is reflected in Fig. 6. The two sites receive the same information and may be isofrequent. H o w e v e r could we neither derive isofrequency contours nor any other kind of frequency organization from our data. As yet, there are only two electrophysiological studies of the rat A C 24'33. According to their results in primary A C there is only one frequency representation with high frequencies represented rostral and low frequencies caudal. Cells of the same binaural response type are grouped together and sometimes extend across isofrequency contours. This organization corresponds to that in the primary cortex of the cat TM. In parallel to the cat data 15 one would expect that heterotopic projections of rat A C connect sites of similar frequency too. In accordance with the data of Sally and Kelly33 showing a singular frequency representation, heterotopic neurons must lie ventral or dorsal to the homotopic neurons. In the present study this was not always the case. The REFERENCES 1 Akers, R.M. and Killackey, H.P., Organization of corticocortical connections in the parietal cortex of the rat, J. Comp. Neurol., 181 (1978) 513-538. 2 Brodal, P., Dietrichs, E., Bjaalie, J.G., Nordby, T. and Walberg, E, Is lectin-coupled horseradish peroxidase taken up and transported by undamaged as well as by damaged fibers in the central nervous system?, Brain Research, 278 (1983) 1-9. 3 Caminiti, R. and Sbriccoli, A., The caliosal system of the superior parietal lobule in the monkey, J. Comp. Neurol., 237 (1985) 85-99. 4 Cippoloni, P.B. and Peters, A., The bilaminar and banded distribution of the callosal terminals in the posterior neocortex of the rat, Brain Research, 176 (1979) 33-47. 5 Code, R.A. and Winer, J.A., Columnar organization and reciprocity of commissural connections in cat primary auditory cortex (AI), Hear. Res., 23 (1986) 205-222. 6 Diamond, I.T., Jones, E.G. and Powell, T.P.S., Interhemispheric fiber connections of the auditory cortex of the cat, Brain Research, 11 (1968) 177-193. 7 Faye-Lund, H., The neocortical projections to the inferior colliculus in the rat, Anat. Embryol., 171 (1985) 1-20. 8 Feng, J.Z. and Brugge, J.E, Postnatal development of auditory callosal connections in the kitten, J. Comp. Neurol., 214 (1983) 416-426. 9 Fitzpatrick, K.A. and Imig, T.J., Auditory cortico-cortical connections in the owl monkey, J. Comp. Neurol., 192 (1980) 589-610. 10 Games, K.D. and Winer, J.A., Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex, Hear. Res., 34 (1988) 1-26. 11 Granger, E.M., Masteron, R.B. and Glendenning, K.K., Origin of interhemispheric fibers in acallosal opossum (with a compar-

difference could m e a n that there is not always a hetero topic connection between sites of isofrequency and tha the organization in the rat A C differs from that in the cat F u n d a m e n t a l differences between the organization of th~ commissural connections of the A C in rat and cat hav~ been described in some other aspects. In the cat, primar 3 A C of one side projects to secondary A C of the contralateral sideS'6'22"4°; however, these studies do nol report heterotopic projections within one auditory area. F u r t h e r m o r e the secondary A C of the cat is only homotopically connected with the contralateral hemisphere. Thus it seems to be of little effect to compare anatomical data from the rat A C with physiological data gained in cat AC. Only a better understanding of the functional organization of the rat A C will therefore enable us to interpret our anatomical data more thoroughly, particularly to determine their relevance to the computational functions performed by the auditory system in rodents.

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Commissural connections between the auditory cortices of the rat.

The pattern of commissural connections of the rat auditory cortex (AC) was investigated with injections of wheat germ agglutinated horseradish peroxid...
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