Exp. Brain Res. 23, 535--554 (1975) 9 by Springer-Verlag 1975

The Association Connexions of the Suprasylvian Fringe (SF) and Other Areas of the Cat Auditory Cortex M. M. Paula-Barbosa, P. B. Fcyo and A. Sousa-Pinto Anatomical Institute, Medical Faculty, University of Oporto (Portugal) Received April 6, 1974 Summary. The association connexions of the peri-auditory (SF, E a and INS) and auditory (AI, A I I and Ep) areas of the eat cortex were studied in silver impregnated material of 32 experiments with cortical lesions. The cortex of the lateral bank of the rostral part of the middle suprasylvian sulcus (SF) sends m a n y fibres to AI and to the insular cortex (INS), and has scanty projections upon A I I and Ep. I n addition, it sends fibres to the visual area 17 as well as to the ventral bank of the medial part of the cruciate sulcus. I t receives fibres from the three auditory areas AI, A I I and Ep, as well as from E a and INS. The dorsal part of the anterior ectosylvian gyrus (Ea) projects upon SF, AI, and AII. Ea sends few fibres to Ep, and receives relatively dense projections from A I and AII. The anterior sylvian gyrus (INS) projects heavily u p o n A I I as well as upon the superficial part of SF. I t sends few fibres also to Ep. INS receives heavy projections from A I I and relatively lighter connections from SF, AI and Ep. The three auditory areas AI, A I I and Ep are strongly mutually interconnected. A I and Ep have scanty projections upon the visual area 19, and AI also to the lateral suprasylvian visual area, as well as upon the ventral bank of the medial cruciate suleus. Correlations of the association eonnexions with the functions of each area are discussed. Key words: Auditory cortex - - Cat - - Association connexions Introduction Suprasylvian fringe area (SF) is the designation introduced by Rose (1949) for the cortex hidden rostrally in the lateral bank of the horizontal part of the suprasylvian sulcus, where it is close to the dorsal border of the first auditory cortex (AI). Later, Woolsey (1960) proposed t h a t SF might be an additional auditory cortical area containing a complete cochlear representation, rostrodorsally encircling AI. Most of this area is hidden in the lateral bank of the suprasylvian sulcus, but parts of it are situated in the superficial cortex of the middle and anterior ectosylvian gyrus. The cortical association connexions of SF have not yet been studied. Metler (1932) described the association connexions of the cat auditory cortex, using the Marchi method, m a n y years before SF and most of the auditory areas were recognized. I n the recent studies of these connexions published by Diamond et al.

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(1968) a n d K a w a m n r a (1973) lesions of SF were n o t made. To our knowledge, only one lesion of this cortical area has been published, b y H e a t h a n d Jones (1971b) in a n e x p e r i m e n t a l s t u d y of the connexions of the cat s u p r a s y l v i a n gyrus. I t was, therefore, decided to s t u d y the association connexions of SF in experim e n t s with lesions of this cortical area. Since the association fibres originating in some of the other p e r i - a u d i t o r y areas have n o t y e t been studied in detail, it was decided to include experiments with lesions of the i n s u l a r a n d t e m p o r a l cortices, and, i n addition, lesions of all the other a u d i t o r y areas were studied for comparison. The results show t h a t S F has association conncxions which differ from those of the other auditory cortical areas.

Materials and Methods The material for this study was selected from 54 experiments with lesions of the auditory and peri-auditory cortex which have also been used for other studies in this laboratory (Pontes et al., 1975; Paula-Barbosa and Sousa-Pinto, 1973). All lesions were made in adult cats under Nembutal anesthesia, and with asseptic precautions. Most of the lesions were made by transdural termocoagulation using a heated metal rod (Fig. la). In some cases, however, the lesions were traumatic (needle puncture) and in other cases electrolytic lesions (Fig. lb) were made by passing anodal current of 2.5--5 mAmp, for 20--60 sec through a wire electrode inserted into the cortex.

Fig. 1. Photomicrographs of lesions of SF. (a) Cat 120, transdural termocoagulation, section no. 58 (see Fig. 3) stained by the Wiitanen (1969) method and counterstained with thionin X 18. (b) Cat 132, electrolytic lesion, 2.5 mAmp, 30 sec, section no. 70 (see Fig. 5) stained with thionin X 16,2

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Fig. 2. Auditory and visual cortical areas of the cat. The visual areas are delimited according to Otsuka and Hassler (1962). The areas labelled in the upper drawing are shown below by the same symbols After 6 or 7 days the animals were killed under nembutal anesthesia, by intravaseular perfusion of 200 ml of 0.9~ NaC1, followed by 2 liters of 10~ formalin-saline. The brains were fixed at room temperature in the same formalin solution for at least 15 days. Photographs were made of the surface of the brains before they were transversely cut at 2 5 / m l on the freezing mierotome. One section out of each 10 was stained with the Wiitanen (1969) method and counterstained with thionin. When necessary, additional sections were stained only with thionin. The sections were drawn in a projection apparatus. The degeneration, as well as the lesions, were identified under the microscope and entered in the drawings. The lesions and the degeneration were carefully localized in relation to the gyri and sulei with the aid of the photographs of the cerebral surface. The lesions were placed on a topographical basis, but the identification of the damaged areas was helped by careful study of the cortical cytoarchitecture around the lesions, in Nissl stained preparations. However, the usefulness of the eytoarchiteetural criteria was limited by the relatively low quMity of the Nissl preparations based on frozen sections and, in addition, was restricted to the cortical areas whieh have been cytoarehitectonicMly described (Rose, 1949; Sousa-Pinto, 1973a). Therefore, the distribution of degeneration in the opposite hemisphere and in the thalamus, which will be described in detail in other publications (Pontes et al., 1975), was used as an indication for the identification of the damaged areas, and will be referred to where necessary. On the basis of these criteria, 32 experiments were selected with lesions restricted to one of the cortical areas under study, and the other 22 experiments were discarded.

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Figure 2 shows the localization of the auditory areas with the designations that will be used in the present study. For simplicity, the former designation of the anterior ectosylvian area (Ea) is kept for the superficial rostral part of Woolsey's (1960) SF. The term "superficial SF" will be used for the part of that area situated in the superficial cortex dorsocaudally to AI, while "deep SF" refers to the part of this area hidden in the lateral bank of the suprasylvian sulcus. In addition, some other regions, such as the dorso-caudal turn of the ectosylvian gyrus (DCA) and the insular and temporal cortices, were included in this investigation, although their relation to the auditory functions is not clear. For the delimitation of the visual areas, also shown in Fig. 2, the maps of Otsuka and Hassler (1962) were followed.

Results I n the present experiments v e r y h e a v y degeneration was f o u n d i n all the u n d a m a g e d parts of the p a r t i c u l a r cortical area where the lesion was made. This was a feature c o m m o n to almost all the experiments a n d i n the following present a t i o n the degeneration i n the same area of the lesion will be m e n t i o n e d i n the cases where it did n o t follow this general rule. The t e r m i n a l a n d p r e - t e r m i n a l d e g e n e r a t i o n f o u n d i n the different areas was most h e a v y in cortical layer I V a n d i n the deeper p a r t of layer I I I . I n these layers the degenerating fibres r u n n i n g i n all directions a r o u n d the nerve cells, a n d mixed with n u m e r o u s globular particles, assumed the p a t t e r n characteristic of t e r m i n a l or p r e - t e r m i n a l degeneration (see Figs. 5 a n d 8). I n the deeper cortical layers V a n d V I the degenerating fibres, even when a b u n d a n t , did n o t have the characteristics of t e r m i n a l fibres, a n d globular particles were n o t a b u n d a n t . D e g e n e r a t i o n was a b s e n t i n the superficial cortical layers I a n d I I , except i n the i m m e d i a t e v i c i n i t y of the lesions where degenerating axons were present i n the superficial p a r t of layer I. A n a t t e m p t was m a d e to find a correlation of the thickness of the degenerating fibres with the lesions or with the cortical areas where the degeneration was present. No e v i d e n t correlation was found. I n most experim e n t s there was a m i x t u r e of degenerating fibres of different calibres, m o s t l y of m e d i u m thickness.

Lesions o/the Suprasylvian Fringe Auditory Area (SF) Lesions of the suprasylvian fringe cortex were made in 9 experiments. In 4 cats the lesions were very small (Figs. la and 3) and in the other 5 (Figs. lb and 4) relatively extensive lesions were made. Cats 115 and 120 (Fig. 3) had similar very small lesions situated in the lateral lip of the suprasylvian sulcus (Fig. la). These lesions were made by transdural termocoagulation, and did not damage the white matter. In cat 115 only the superficial half of the cortex was destroyed. Since layer III, with many pyramidal ceils, is identifiable at both borders of the lesions it appears that in none of these cases there was damage to the neighbouring AI. The thalamie and commissural degeneration found was also exactly similar in the two experiments. Degenerating fibres were abundant in MGB and IC, while they were very rare in P and LP and absent in LGB. In the contralateral hemisphere degeneration was found in SF as well as in AII. In the ipsilateral hemisphere degeneration was very heavy in the rostral half of the lateral bank of the suprasylvian sulcus as well as in the superficial cortex dorsocaudally to AI. There was dense degeneration in the rostral half of the middle ectosylvian gyrus as well as, dorsally, in the anterior ectosylvian gyrus. There was degeneration in the ventroeaudal bank of the anterior ectosylvian sulcus as well as in the posterior ectosylvian gyrus. In non-auditory areas, scanty but consistent degeneration was found in the lateral and medial surfaces of the caudal 2/3 of the lateral gyrus, in the surface of the middle suprasylvian gyrus, and in the ventral bank of the medial part of the crueiate sulcus. In the eat 115 some

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Fig. 3. Drawings of lesions and degeneration found in experiments with lesions of the superfieial p a r t of the suprasylvian fringe area. I n this and in the following figures the lesions are shown in full black, a n d the " t e r m i n a l " fields of degeneration are shown by dotting. The density of the dotting gives an impression of the density of degeneration found

few degenerating fibres were also found deeply in the splenial sulcus. In these 2 experiments no degeneration was found in the medial bank of the suprasylvian suleus or in the caudal t h i r d of the lateral bank of the horizontal part of the same sulcus. I n eats 81 and 119 (Fig. 3) lesions similar to those of eats 115 and 120 were made in a more caudal situation. However, in experiments 81 and 119 very small associated undesired lesions were found. I n eat 119 there was very slight damage to the tip of the white m a t t e r of the eetosylvian gyrus and in both eats there seems to be very slight damage to a very small area of the medial border of the suprasylvian sulcus where, although no cellular or eytoarchitectural changes were visible, some degenerating fibres were found arising from the superficial cortical layers. I n the ipsi- and contralateral cortex as well as in the thalamus of these two cats degeneration h a d the same distribution and density as described in the experiments 115 and 120 (Fig. 3). The only difference found was the presence of additional degeneration in the medial b a n k of the middle part of the suprasylvian sulcus as well as in the caudal third of the lateral b a n k of the same sulcus. I n the latter situation, very close to the dorsocaudal angle of t h a t sulcus, the degeneration was very h e a v y and extended to the neighbouring cortical convexity (Fig. 3).

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I n 5 experiments extensive deep lesions of the SF area were made. I n eats 131 and 132 (Fig. 4) electrolytic lesions (:Fig. ]b) were made deeply in the rostral p a r t of the lateral b a n k of the suprasylvian sulcus. The lesion in eat 132 appears restricted to SF, b u t in cat 131 a very small necrotic spot, due to vascular damage, was found in the white m a t t e r of the ectosylvian gyrns. Therefore, in cat 131 some few fibres, most probably arising in AI, may have been cut. However, in these two cats thalamie degeneration was exactly similar, being present in :MGB, mMGB, and SG and absent in LGB as well as in the other nuclei of the posterior thalamus. The cortical degeneration had similar distribution in these two experiments (:Fig. &). There was very h e a v y degeneration rostrally in the lateral bank of the snprasyIvian sulcns, around the lesion. The degeneration was dense in the dorsal p a r t of AI as well as rostrally ia the anterior sylvian gyrus and in the ventro-eaudM bank of anterior eetosylvian suleus. Degenerating axons were also present in A I I as well as in the rostral part of the posterior ectosylvi~n gyrus. Furthermore, degenerating fibres (Fig. 5) were found in the mediM and lateral surfaces of the lateral gyrus in these two experiments. I n cat 131, where fibres from AI m a y have been interrupted, scanty degeneration was found additionally in the dorsal p a r t of the anterior ectosylvian gyrus as well as deeply in the splenial sulcus and in the ventral b a n k of the medial part of the cruciate suleus. I n these two experiments no degeneration was found in the mediM bank of the middle suprasylvian suleus or caudally in the lateral b a n k of this suleas.

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Fig. 5. Photomicrograph of degenerating fibres found in visual area 17 of cat 132 with lesion of SF. Wiitanen (1969) stained section • 720 I n the other 3 experiments with deep lesions of SF, the lesions were more caudally situated and, in addition, small undesired lesions were associated. I n cat 83 (Fig. 4) a n electrolytic lesion was made in the middle of the transverse p a r t of the lateral bank of the suprasylvian suleus and in the neighbouring cortical convexity. I t was found slight damage to the white m a t t e r underlying the lesion. Although no further cortical lesions were found in this case, thMamic degeneration was found in the MGB and SG but, in addition, it was present also in the dorsal and ventral LGB, as well as in P. Furthermore, there was dense fibre degeneration in the visual areas 17 and lateral suprasylvian of the contralateral hemisphere. I n this experiment (Fig. 4) very dense degeneration was found in the whole rostrocaudal e x t e n t of both banks of the middle suprasylvian sulcus, in the middle ectosylvian gyrus, and in the anterior sylvian gyrus. I n addition, heavy degeneration was found in the middle suprasylvian gyrus and in the three visual areas 17, 18 and 19, in the lateral as well as in the medial surface of the hemisphere. Degeneration was found also in the posterior ectosylvian gyrus and in the ventral b a n k of the medial cruciate sulcus. I n 2 cats 116 (Fig. 4) and 118 (not illustrated) traumatic lesions of the middle part of the lateral b a n k of the suprasylvian suleus were made. I n cat 116 there was damage to the white m a t t e r close to the b o t t o m of the sulens, and in cat 118 there was damage deep to the medial b a n k of the suprasylvian sulcus. I n these 2 experiments the degeneration in the cortex and thalamus was similar to t h a t found in eat 83 (Fig. 4).

Lesions o/the Anterior Ectosylvian Area (Ks) I n cats 105 and 130 (Fig. 6) small electrolytic lesions destroyed the cortex of the dorsal part of the anterior ectosylvian gyrus. The cortical cytoarchitecture showed t h a t the lesions were situated in area Ea and t h a t there was no damage to the neighbouring AI. However, in cat 105 there was slight damage to the white m a t t e r underlying the ventral part of the lesion and it is most likely t h a t fibres from the hindlimb region of SmII were interrupted in this experiment,.

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Fig. 6. Drawings of lesions and degeneration found in experiments with lesion of the ectosylvian anterior area (cats 105 and 130) and of the insular cortex (cats 73 and 109)

The findings were similar in the auditory areas of the 2 experiments (Fig. 6). There was dense degeneration in the rostral parts of the middle sylvian and middle ectosylvian gyri and very scanty degeneration widespread in the posterior ectosylvian gyrus. There was very heavy degeneration in the anterior sylvian gyrus. The degeneration was dense rostrally in the lateral bank of the suprasylvian sulcus while it was scanty in the superficial part of SF. In the non.auditory areas of cat 105 the degeneration was dense in the whole extent of SmII, and in the medial surface of the posterior sigmoid gyrus, as well as rostrally in the suprasylvian gyrus and ventrally in the posterior part of this gyrus. In experiment 130 there was no degeneration in the non-auditory cortical areas.

Lesions o/the Insular Cortex (INS) The anterior sylvian gyrus (insular cortex) was damaged in cats 73 and 109 (Fig. 6). Both lesions destroyed all cortical layers, but there was no damage to the underlying white matter. The degeneration found in the auditory cortical areas was exactly similar in these two experiments (Fig. 6). Very heavy degeneration was found only in the contiguous middle sylvian gyrus. There was degeneration superficially in the lateral bank of the suprasylvian sulcus and in the ventral part of the posterior ectosylvian gyrus, while in AI and in Ea only rare degenerating fibres were found. The temporal cortex, the deep part of SF, and DCA were free of degeneration. In non-auditory areas, degeneration was found in a small patch caudally in the lateral hank of the middle suprasylvian sulcus, in the medial aspect of the anterior sigmoid gyrus, and in the dorsal part of the proreate gyrus. The visual, sensorimotor, and suprasylvian areas were entirely free of degenerating fibres. Lesions o/the First Auditory Cortex (AI) Lesions of AI were made in 5 cats. In the experiments 68 (Fig. 7) and 91 the lesions destroyed only the cortical layers I and I I and the absence of an identifiable layer I I I underneath the lesions suggests that the lesions damaged AI exclusively. In the thalamus no degeneration was found, but in the contralateral hemisphere there was abundant degeneration in AI, and in cat 91 degeneration was found also in the contralateral AII and SF. In the ipsilateral auditory areas of the two cats dense degeneration was found rostrally in the lateral bank of the suprasylvian sulcus, in the dorsal part of the anterior ectosylvian gyrus, in the

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ventrocaudal bank of the anterior ectosylvian sulcus and in the anterior sylvian gyrus. Lighter degeneration was found in the middle sylvian gyrus (Fig. 8a). I n the ipsilateral nonauditory areas scanty b u t consistent degeneration was found at caudal levels in the b o t t o m a n d banks of the lateral sulcus and in the convexity of the middle suprasylvian gyrus. There was degeneration also in the medial bank of the middle suprasytvian sulcus (Fig. 8b). In addition, degeneration was present rostrally in the lateral gyrus as well as in the ventral b a n k of the medial aspect of the cruciate snlcus. I n cat 91 there was degeneration in the middle part of the convexity of the lateral gyrus. I n cats 94 (Fig. 7), 98 and 99 electrolytic lesions damaged all cortical layers of AI with, however, only very slight damage to the white m a t t e r in the centre of the lesions. The cytoarchitecture at the borders of the lesions suggests t h a t they are restricted to AI. This appears indeed to be the case in cats 94 and 99 since in these animals contralateral degeneration was restricted to AI a n d in the thalamus degeneration was found only in P L of the MGB. I n eat 98, however, degeneration was found in A I I and in SF of the contralateral hemisphere. I n the ipsilateral auditory areas of these 3 cats degeneration was found in the same parts as in cats 68 a n d 91. However, it was heavier and, furthermore, there was degeneration in the posterior ectosylvian gyrus. I n the non-auditory areas the degeneration was also similar to the cats 68 and 91 but, in addition, there was consistently scanty degeneration in the b o t t o m a n d banks of the splenial suleus, in the medial surface of the hemisphere.

Lesions o/the Second Auditory Cortex ( A l l ) I n 6 experiments cortical lesions were made within the cytoarchitectonic boundaries of AII. The presence of degeneration restricted to A I I in the contralateral hemisphere as well as to the dorsal nucleus in the MGB shows t h a t these electrolytic lesions were restricted to A I I in cats 96 (not illustrated), 111 and 129 (Fig. 9). I n cats 70 and 90 the presence of degeneration in AI of the contralateral hemisphere suggests t h a t the ventral p a r t of AI m a y have been damaged, a n d in cat 86, most probably the dorsal border of INS has been included in the lesion. I n the 3 experiments 96, 111 and 129 dense degeneration was found (Fig. 9) in the anterior sylvian gyrus and in the neighbouring b a n k of the anterior ectosylvian sulcus, in the most dorsal part of the anterior ectosylvian gyrus and in the rostral half of the lateral b a n k and lip of the middle suprasylvian sulcus. Scanty degeneration was found in the middle and posterior parts of the convexity of the ectosylvian gyrus as well as in the caudal p a r t of the middle suprasylvian gyrus. 38 Exp. Brain Res. Vol. 23

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Fig. 8. Photomicrographs of degenerating fibres in the cortex of cats with lesions of AI. Wiitanen (1969) stained sections eounterstained with thionin, • (a) Cat 91, second auditory cortex. (b) Cat 98, lateral suprasylvian visual area

Fig. 9. Drawings of lesions and degeneration found in two experiments with lesions of the second auditory cortex

I n cats 70, 86 and 90 the distribution of degeneration was similar to t h a t described above. However, the degeneration in the middle suprasylvian gyrns was more abundant, and in eats 70 and 90 degenerating fibres were found in the b o t t o m and lateral bank of the lateral sulcus.

Lesions o/ the Eetosylvian Posterior Auditory Area (Ep) I n 4 experiments electrolytic lesions were restricted to the ectosylvian posterior auditory cortex. I n eats 92 (not illustrated), 103, and 112 (Fig. 10) there was no damage to the white m a t t e r and degeneration in the contralateral hemisphere was restricted to Ep, b u t in cat 7 there was slight damage to the white m a t t e r and the presence of degeneration in contralateral A I I suggests t h a t in this case fibres from A I I may have been damaged. In cat 112 the electrolytic lesion destroyed the b o t t o m a n d both banks of the ventral part of the posterior ectosylvian sulcus. I n these 4 experiments no degeneration was found in the LGB, and there was dense degeneration in the MGB. I n these 4 experiments very heavy fibre degeneration was found (Fig. 10) in the whole ectosylvian posterior gyrus, as well as in the caudal b a n k and b o t t o m of the posterior ectosylvian sulcus. Dense degeneration was found also in the anterior, middle and posterior parts of the sylvian gyrus. Degenerating fibres were also present rostrally in the lateral bank of the suprasylvian suleus and in the ventroeaudal b a n k of the anterior ectosylvian sulcus. In

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non-auditory areas degeneration was consistently found in the 4 experiments deeply in the splenial sulcus, as well as in the lateral bank of the lateral sulcus, and in the ventrocaudal part of the lateral gyrus. Scattered degenerating fibres were found in the middle suprasylvian gyrus. Lesions in the Dorsocaudal Turn o/ the Ectosylvian Gyrus (DCA) In experiment 76 (Fig. i l ) the lesion was situated immediately caudally to the dorsal tip of the posterior ectosylvian sulcus. It destroyed extensively the cortex of the caudal bank of this suleus as well as a small neighbouring area of the superficial cortex. There was only very slight damage to the white matter of the posterior ectosylvian gyrus. l~elatively scanty degeneration was found in this experiment. Degenerating axons were found in small areas caudally in the deep part of the lateral bank of the suprasylvian sulcus, and rostrally in the middle sylvian gyrus. Rare degenerating fibres were found in the Ea area

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and in DCA. Scanty degeneration was found ventrally in the posterior part of the suprasylvian gyrus, and scattered degenerating fibres were present in the medial hank of the suprasylvian sulcus. The auditory regions AI and Ep were intirely free of degeneration. In another experiment (eat 77, Fig. 11) a small lesion was made in the middle of DCA, with only very slight involvement of the underlying white matter. The distribution of degeneration was similar to cat 76, but, in addition, there was dense degeneration in the middle and posterior suprasylvian gyrus, as well as in the medial bank of the suprasylvian sulcus.

Lesion8 o] the Temporal Cortex (T) Lesions of the posterior sylvian gyrus were made in two experiments. In eat 100 (Fig. 11) all the cortical layers in this gyrus were damaged, but the lesion did not encroach on the underlying white matter. In cat 82 (Fig. 11) a double lesion of the posterior sylvian gyrus was made. Its dorsal part probably damaged slightly AII and in its ventral part there was a small lesion of the underlying white matter. In these two experiments dense degeneration was found in the anterior and middle sylvian gyrus, as well as in the rostral part of the lateral bank of the middle suprasylvian sulcus. Degeneration was scanty in the posterior sylvian gyrus around the lesions, and in eat 100, where the lesion may have damaged the ventral tip of area Ep, there was degeneration in the posterior ectosylvian gyrus as well as in the dorsal part of the anterior ectosylvian gyrus. Rare degenerating fibres were found also in the ventral bank of the medial aspect of the cruciate sulcus.

Summary of the Results Lesions o] SF. Lesions a p p a r e n t l y r e s t r i c t e d to t h e r o s t r a l p a r t of a r e a S F were m a d e in 4 e x p e r i m e n t s (cats 115 a n d 120, Fig. 3, cats 131 a n d 132, Fig. 5), where no d a m a g e to t h e white m a t t e r was found. T h e lesions were small a n d superficially s i t u a t e d in cats 115 a n d 120 (Fig. l a ) a n d r e l a t i v e l l y large a n d d e e p l y s i t u a t e d in cats 131 a n d 132 (Fig. l b ) . Cortical c y t o a r c h i t e c t u r e as well as t h a l a m i c a n d c o m m i s s u r a l d e g e n e r a t i o n suggests t h a t t h e 4 lesions were r e s t r i c t e d to SF, a l t h o u g h t h e possibility of v e r y small d a m a g e to t h e a r e a A I c a n n o t be i n t i r e l y excluded. T h e findings were similar in t h e 4 cats (Figs. 3 a n d 5). D e g e n e r a t i o n was h e a v y in t h e superficial as well as in t h e deep p a r t s of SF. There was dense d e g e n e r a t i o n in t h e dorsal p a r t s of A I a n d in E a r e l a t i v e l y light in E p a n d I N S . S c a n t y deg e n e r a t i o n was consistently f o u n d w i d e s p r e a d in t h e visual a r e a 17 (Fig. 5) a n d r o s t r a l l y in a r e a 6 a t of Hassler a n d Muhs-Clement (1964).Very s c a n t y degenerat i o n f o u n d also in r e s t r i c t e d p a r t s of visual a r e a 19 m a y be a t r i b u t e d to simult a n e o u s d a m a g e of A I . No d e g e n e r a t i n g fibres were f o u n d in t h e visual a r e a CB. I n 5 o t h e r e x p e r i m e n t s small (eats 81 a n d 119, Fig. 3) a n d large (eats 83, 116, Fig. 5 a n d 118) lesions of S F were s i t u a t e d m o r e caudally. T h a l a m i c as well as commissuraI d e g e n e r a t i o n s t r o n g l y suggests t h a t t h e CB a r e a has been i n v o l v e d in these 5 lesions. D e g e n e r a t i o n h a d essentially t h e same d i s t r i b u t i o n in these 5 cats (Figs. 3 a n d 5). There was similar, b u t h e a v i e r d e g e n e r a t i o n in t h e s a m e areas as in t h e preceeding 4 e x p e r i m e n t s and, in addition, t h e r e was dense d e g e n e r a t i o n in t h e visual areas 18 a n d CB as well as in t h e c o n v e x i t y of t h e m i d d l e s u p r a s y l v i a n gyrus. Lesions o / E a were m a d e in two e x p e r i m e n t s (cats 105, a n d 130, Fig. 6) lesions of this area. I n these animals d e g e n e r a t i o n was v e r y h e a v y in t h e r o s t r a l p a r t s of A I , A I I , a n d I N S , as well as in t h e deep p a r t of SF. S c a n t y d e g e n e r a t i o n was f o u n d in t h e superficial p a r t of S F a n d in Ep.

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Lesions o / I N S in two other animals (cats 73 and 109, Fig. 6) provoked heavy degeneration in AII as well as in the superficial part of SF and ventrally in Ep. Furthermore degeneration was found in the area CB as well as in area 6at of Hassler and Muhs-Clement (1964). Lesions o] AI. Cats 68, 94 (Fig. 7) and 99 had apparently "pure" lesions of AI, whi]e in eats 91 and 98 small adjacent areas of SF and AII were probably damaged. In these 5 experiments dense degeneration was found in AI, SF and INS. There was also degeneration in AII (Fig. 8a) and Ea, and in the cats with lesion of all cortical layers (91, 98 and 99) degeneration was found also in Ep. In these 5 experiments scanty degeneration was consistently found in the visual areas 19 and CB (Fig. 8b) as well as in area 6at of Hassler and Muhs-Clcment (1964) and in the middle suprasylvian gyrus. Lesions o / A I I were made in the experiments 96 (not illustrated), 111 and 129 (Fig. 9). In 3 other animals lesions of AII were, most probably, associated with small lesions of the neighbouring areas AI (cats 70 and 90) and INS (cat 86). In these 6 experiments dense degeneration was found in AII and in the areas SF, Ea and INS. Scanty degeneration was found in AI and Ep, as well as in the suprasylvian cortex. In the cats where AI may have been damaged (cats 70 and 90) degeneration was found also in the visual area 19, and it was heavy in the suprasylvian cortex. Lesions o] Ep were made in 4 experiments. In cats 92 (not illustrated), 103 and 112 (Fig. 10) the lesions were apparently restricted to Ep but in cat 79 there was slight damage to the white matter underlying the lesion. In these 4 experiments very heavy degeneration was found in the whole extent of area Ep, and degeneration was dense also in AII, INS and SF. Degeneration was consistently found also in the visual area 19. In the experiments with lesions of the posterior eetosylvian gyrus at dorsal levels (cats 76 and 77, Fig. 11) degeneration was very scanty but similar to that provoked by the lesions situated at ventral levels in Ep, but it appears that when the lesion aproaehed the suprasylvian suleus (cat 77) additional degeneration occurred in the area CB. Two lesions of the temporal cortex, situated rostrally in the posterior syivian gyrus (cats 82 and 100, Fig. 11) gave origin only to degeneration similar to that following lesion of the neighbouring areas AII and Ep. Degenerating fibres were found in AII, SF, and INS, and in cat 100 also in Ep and Ea. The degeneration was scanty in the posterior sylvian gyrus around these lesions. Discussion The results obtained in the present study show that the auditory and periauditory areas of the cat cortex, in addition to different thalamic connections (see Sousa-Pinto, 1973b) and eytoarchitecture (Rose, 1949; Sousa-Pinto, 1973a), have different association connections. These areas have also different physiological properties (see Woolsey, 196-9) and it seems clear that they must subserve different functions, even if behavioural studies have so far failed to reveal functional differences between them. 39

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The Association Connexions o/ the Suprasylvian Fringe ( S F ) and Other PeriAuditory Areas Rose (1949) and Rose and Woolsey (1949) proposed the designation "suprasylvian fringe area" for the rostral half of the lateral bank of the middle suprasylvian sulcus where they found transition in cytoarchitecture from the 6-layered pattern prevalent in the suprasylvian cortex to the cytoarchitecture characteristic of AI. Later, Woolsey (1960) hypothesized that SF might be the middle part of another cortical auditory area, of which the high and low frequency regions had been found by Hind (1953) in the middle ectosylvian gyrus dorsocaudally to AI, and in the dorsal part of the anterior ectosylvian gyrus (Ea), respectively. On this basis and although Rose (1949) had found the cytoarchitecture of Ea to be similar to AII, Woolsey extended the boundaries of SF to include Ea and the superficial cortex dorsocaudal to AI, and suggested that the whole area is related to auditory functions. A more extended delimitation of this auditory fringe area was suggested by the results of Heath (1970), Graybiel (1970a, b, 1973) and Heath and Jones (1971a) who found that an ill-defined thalamic region, including the magnocellular nucleus of the medial geniculate body (mMGB) and the suprageniculate nucleus (SG), sends axons to an extensive cortical band including, in addition to Woolsey's SF, the cortex folded in the banks of the anterior ectosylvian sulcus as well as the surface of the anterior sylvian gyrus (INS). All parts of this extended periauditory band do not receive fibres from the dorsal or from the ventral nuclei of the MGB (Sousa-Pinto, 1973b), and auditory evoked activity has not yet been electrophysiologically demonstrated neither in its parts folded in the anterior ectosylvian sulcus nor in the lateral bank of the suprasylvian sulcus. The present results show that, although sharing the same thalamic afferent connexions, the 3 different regions of the peri-auditory band of Heath and Jones (1971a) do not have the same association connexions. The situation of most of SF deeply in the lateral bank of the suprasylvian sulcus (see Fig. 2) raises difficulties in obtaining "pure" lesions of this cortical area large enough to demonstrate clearly all its efferents with silver impregnation methods. In addition, although its separation from AI is relatively well defined cytoarchitectonically (Rose, 1949; Sousa-Pinto, 1973a), its medial and caudal borders, where it borders on the lateral suprasylvian visual area of Clare and Bishop (1954), are not recognizable in the Nissl preparations used in the present study. On the other hand, attempts to demonstrate the SF efferents with radioactive tracers (Cowan et al., 1972) met with considerable difficulties (Sousa-Pinto and Reis, 1975). However, it appears that the degenerating fibre systems which were mapped in the 9 lesions of SF used in the present study may be taken as the efferent connexions of this cortical area. In all these 9 experiments degeneration was heavy in SF, while it was dense in parts of AI and scanty in Ep, and in INS as well as in the visual area 17 (Fig. 5), and in area 6ai3. Degeneration in these areas was present also in the experiments 115, 120 (Fig. 3), 131 and 132 (Fig. 4) where thalamic and commissural degeneration, as well as cytoarchitecture around the lesion, suggest that they are "pure" lesions of SF. In these 4 experiments no

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degeneration was found in the CB area and this strongly suggests that the lesions did not damage this visual area, since H e a t h and Jones (1970, 1971b) demonstrated t h a t a small lesion of CB provokes degeneration in the whole extent of this area and our own results support this conclusion. Lesions where CB was visibly damaged in the medial bank of the suprasylvian sulcus (cat 118) as well as lesions situated more caudally in the lateral bank of the suprasylvian sulcus (cats 81 and l l 9 , Fig. 3, 83 and 116, Fig. 4) provoked dense degeneration in the medial bank of the suprasylvian gyrus as well as caudally in the lateral bank of this sulcus, and in the immediate cortical convexity. Furthermore, in these more caudally situated lesions heavy degeneration in the three cortical visual areas and in the LGB was found, such as could he expected from lesions of the CB area (Heath and Jones, 1970; Shoumura and Itoh, 1972). These findings suggest, therefore, t h a t the 4 rostrally situated lesions studied here did not damage CB, and, in addition, support the delimitation of the latter visual area as proposed by H e a t h and Jones (1971b) on the basis of its connexions. The projections mapped in these 4 "pure" SF lesions were, however, not completely uniform. I n cat 131 degeneration was found deeply in the splenial sulcus, and in cats 115 and 120 degeneration was found in Ea which was not present in the other SF lesions. Since it is very difficult to exclude the possibility of slight damage to the neighbouring area A I in these lesions, and since this area sends axons to Ea as well as to the visual area 19 in the splenial sulcus (see below), it is not possible to reach a definite conclusion on this point, although the thalamic and commissural degeneration in cats 115, 120, and 131 does not show any evidence of damage to AI. The association connexions of SF mapped in the present study differ in their distribution from those of the other auditory and periauditory areas. This area receives m a n y fibres from AI and receives relatively less dense projections from the other auditory areas. I t sends fairly dense projections onto AI, and lighter projections to INS and Ep, and, in addition, has efferent fibres to some nonauditory areas, namely to the visual area 17, and to the area 6aB of Hassler and Muhs-Clement (1964). I t has, in addition projections upon the superior colliculus (Paula-Barbosa and Sousa-Pinto, 1973). The connexions of SF demonstrated here seem, therefore, to support Woolsey's (1960) suggestion of its association with auditory functions, since it receives projections from the three auditory areas and projects heavily to AI. On the other hand, it receives fibres from the mMGB (Heath, 1970; Graybiel, 1970a, b, 1973; H e a t h and Jones, 1971a) which is not a purely auditory nucleus (Poggio and Mountcastle, 1960), and has projections onto the visual area 17 as well as to the medial surface of the anterior sigmoid gyrus which, probably, is a motor area (see Sousa-Pinto, 1969). Therefore, it appears t h a t SF is an area subserving different sensory modalities, being concerned in the transmission of auditory information to the visual areas, as well as to some of the auditory and motor cortical regions. I t may, therefore, be a link in the pathway mediating the short latency auditory evoked activity which has been recorded in the visual area 17 by Jung et al. (1963) and Spinelli et al. (1968). The association connexions of the area Ea were found in the present study to be different from those of SF, although m a n y similarities were also found. Both 39*

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areas send dense projections to the auditory areas as well as to INS, and give also some fibres to Ep. Projections from Ea to INS and Ep were, however, not found by K a w a m u r a and Otani (1970) in an experiment with a lesion more ventrally situated than those used here which, therefore, m a y have caused only small damage to Ea. These two regions, Ea and SF, receive also a similar set of afferent association fibres arising from the auditory areas A I and AII. However, the two areas differ strinkingly as to their association projections to non-auditory areas, since Ea has apparently no projections to the visual area 17. I n addition, Ea has proiections upon A I I which were not found from SF, while the latter area has thalamic projections to the MGB which Ea does not appear to have (Pontes et al., 1975). These differences in connectivity, as well as the cytoarchitectonic differences (Rose, 1949), suggest t h a t Ea is distinct from SF. The insular cortex has association eonnexions which differ from those of the other areas studied here. I t receives dense projections from all the auditory and peri-auditory areas. I t sends heavy projections only to AII, and has scanty projections to Ep. I t is the only area studied here t h a t has no projections onto the deep part of SF. I n addition, it has only very scanty projections to non-auditory areas, these being restricted to some few fibres to the CB area, and to area 6aB. These results are in close agreement with those of K a w a m u r a (1973) who studied 5 lesions of this area, except that we found a projection from INS to the superficial SF which was not described by Kawamura. I t appears, therefore, t h a t SF, Ea, and INS, which together form the periauditory band of H e a t h and Jones (i971a), m a y be differentiated on the basis of their connexions. As found in the present study, they have different association connexions, and they have also different projections to thalamic nuclei (Pontes et al., 1975). On the other hand, these 3 areas have several features in common. They receive thalamic afferents from the mMGB and from the SG nucleus (Heath, 1970; Graybiel, 1970a, b, 1973; H e a t h and Jones, 1971a) and, in addition, physiologically they appear as polysensory regions. Convergence of somatic sensory and auditory stimuli has been demonstrated in the Ea area by Mickle and Ades (1952), Berman (1961) and Carreras and Anderson (1963), and in the insular cortex visual as well as auditory and somatic sensory evoked activity has been recorded (Desmedt and Meehelse, 1959a; Thompson et al., i963; Loe and Benevento, 1969). The organization of the thalamic afferents as well as physiological data suggest, therefore, t h a t the peri-auditory band of H e a t h and Jones (197Ia) is mostly a polysensory region where integration of different sensory modMities m a y occur. Association connexions suggest, on the other hand, t h a t although the whole peri-auditory band is strongly interconnected with the auditory areas, parts of it m a y have somewhat specialized functions. SF seems concerned with the transmission of auditory information to the visual area 17, while the insular cortex appears to have m a n y connexions with the descending auditory pathway (Desmedt and Mechelse, 1959b). Intrinsic Auditory Connexions Most of the association connexions of the cortical auditory areas AI, A I I and Ep described previously b y Diamond et al, (1968) and K a w a m u r a (1973) were confirmed in the present study. The three areas are strongly interconnected, a

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fact which has also been physiologically demonstrated b y Downman et al. (1960). Lighter association connexions are found between AI and Ep, in both directions. The posterior sylvian gyrus does not receive fibres from the auditory regions, except some fibres from Ep, caudally, close to the ventral tip of the posterior ectosylvian sulcus. Rostral lesions of this gyrus gave origin to scanty degeneration, similar to t h a t caused by lesions of Ep. This suggests that probably only the caudal part of the posterior sylvian gyrus is related to auditory functions. Most probably, this small cortical region represents a rostral extension of the Ep area, as has been suggested by Sindberg and Thompson (1962). The superficial cortex situated in the dorsoeaudal angle of the ectosylvian gyrus (DCA) has been found in the present study to have very scanty connexions with the auditory and peri-auditory regions. I n addition, the occurence of a few efferent fibres arising from this region and passing to SF, and AII, m a y be explained by damage to the adjacent dorsal part of Ep. This suggests t h a t Ep m a y reach more dorsal levels than frequently drawn in maps of the auditory regions and shown in Fig. 1. The lesion in cat 76, in the caudal bank of the dorsal tip of the posterior ectosylvian sulcus shows t h a t this region has projections similar to the adjacent Ep area. Since this cortical part has a cytoarchitecture similar to Ep (Rose, 1949; Sousa-Pinto, 1973a) and receives thalamic afferents from the same nuclei as Ep (Sousa-Pinto, 1973b) it seems t h a t it m a y be considered as a part of the latter area. Extrinsic Connexions o/ the Auditory Areas

I n the present study extrinsic projections from the auditory areas were found which have not been described in the previous studies of Diamond et al. (1968) and K a w a m u r a (1973). These authors did not find projections from the auditory areas AI, A I I and Ep to any regions outside the suprasylvian sulcus, a result which is at variance with those of Metler (1932). I n the present experiments with lesions of the auditory areas AI and Ep, degenerating fibres were found in the visual areas 19 and CB (Fig. 8b) as well as in the suprasylvian cortex and in area 6aB of Hassler and Muhs-Clement (1964). Most of these extrinsic connexions arise from AI and were here demonstrated in 5 experiments with no associated undesired lesions. The presence of these auditoryvisual cortical connexions might afford an alternative explanation for the results of J u n g et al. (1973) and Spinelli et al. (1968). The divergence between our results, and those of Diamond et al. (1968b) and K a w a m u r a (1973) are, most probably, due to methodological differences, since those authors used the Nauta-Gygax (1954) method while we used Wiitanen's (1969) method. Studies of these connexions, with the method of Cowan et al. (1972) using radioactive aminoacids, are in progress in this laboratory and m a y contribute to resolve this conflict. Ael~nowledgements. The authors gratefully acknowledge the technical assistance of Mrs. Cecili~ Pascoal, Miss M.A. Mendes, and Mr. L. Bessa Nunes, as well as 5J[rs. M.G. Rodrigues typing of the manuscript. This work was financed through the Project PMC/5-I from the Instituto de Alta Cultura of the Portuguese Ministry of Education and Culture.

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Abbreviatures Used in the Text and Figures AI First auditory cortex AII Second auditory cortex CB Lateral suprasylvian visual area (Clare and Bishop, 1954) DCA Dorsocaudal turn of the ectosylvian gyrus Ea Ectosylvian anterior auditory area Ep Ectosylvian posterior auditory area IC Inferior colliculus INS Insular auditory area LGB Lateral geniculate body LP Lateral posterior nucleus of the thalamus MGB Medial geniculatc body mMGB Magnocellular medial geniculate nucleus P Pulvinar PL Lateral part of the ventral nucleus of the medial geniculate body SF Suprasylvian fringe auditory area Suprageniculate nucleus SG SmlI Second sensory area SSS Suprasylvian sulcus T Temporal cortex Area 6aft of HassIer and Muhs-Clement (1964) 6aft 17 Visual area 17 18 Visual area 18 19 Visual area 19

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Heath, C.J., Jones, E. G. : Connexions of area 19 and the lateral suprasylvian area of the visual cortex of the cat. Brain Res. 19, 302--305 (1970) Heath, C.J., Jones, E. G. : An experimental study of ascending connections from the posterior group of thalamic nuclei in the cat. J. comp. Neurol. 141,397--426 (1971a) Heath, C.J., Jones, E.G.: The anatomical organization of the suprasylvian gyrus of the cat. Ergebn. Anat. Entwickh-Gesch. 45, 1--64 (1971b) Hind, J . E . : An electrophysiological determination of tonotopic organization in auditory cortex of the cat. J. Neurophysiol. 16, 475--489 (1953) Jung, R., Kornhuber, H.H., Da Fonseca, J. S. : Multisensory convergence on cortical neurons. Neural effects of visual, acoustic, and vestibular stimuli in the superior convolutions of the cat's cortex. In: Progress in Brain Research. Brain mechanisms. Eds. by Moruzzi, G., Fessard, A. and Jasper, H.H. vol. 1, pp. 207--240. Amsterdam: Elsevier 1963 Kawamura, K. : Cortical fiber connections of the cat cerebrum. I. The temporal region. Brain Res. 51, 1--21 (1973) Kawamura, K., Otani, K. : Cortico-cortical fiber connections in the cat cerebrum. The frontal region. J. comp. Neurol. la9, 423--448 (1970) Lee, P.R., Benevento, L.A.: Auditory-visuM interaction in single units in the orbito-insular cortex of the cat. Electroenceph. elin. Neurophysiol. 26, 395--398 (1969) Metler, F.A.: Connections of the auditory cortex of the cat. J. comp. Neuroh 55, 139--183 (1932) Mickle, W.A., Ades, H.W. : A composite sensory projection area in the cerebral cortex of the eat. Amer. J. Physiol. 170, 682--689 (1952) Nauta, W.J.H., Gygax, P.A.: Silver impregnation of degenerating axons in the central nervous system: a modified technic. Stain Technoh 29, 91--93 (1954) 0tsuka, R., Hassler, R. : Uber Aufbau und Gliederung der cortiealen Sehsph~ire bei der Katze. Arch. Psychiat. 203, 212--234 (1962) Paula-Barbosa. M., Sousa-Pinto, A. : Auditory cortical projections to the superior eolliculus in the cat. Brain Res. 50, 47--61 (1973) Poggio, (9. F., Mounteastle, V. B. :A study of the functional contributions of the lemniscM and spinothalamic system to somatic sensibility. Central nervous mechanisms in pain. Bull. Johns Hopk. Hosp. 1D6, 266--316 (1960) Pontes, C., Reis, F.F., Sousa-Pinto, A.: The auditory cortical projections onto the medial geniculate body in the cat. An experimental anatomical study with silver and autoradiographic methods. Brain Res. 91, 43--63 (1975) Nose, J.E.: The cellular structure of the auditory region of the cat. J. comp. Neurol. 91, 409---440 (1949) Rose, J.E., Woolsey, C.N. : The relations of thalamic connections cellular structure and evecable electrical activity in the auditory region of the eat. J. comp. Neuroh 91, 441M66 (1949) Shoumura, K., Itoh, K.: lntercortical projections from the lateral wall of the suprasylvian gyrus, the Clare-Bishop area, of the cat. Brain Res. 39, 536--539 (1972) Sindberg, R.]VI., Thompson, R.F.: Auditory response fields in ventral temporal and insular cortex of cat. J. Neurophysiol. 25, 21--28 (1962) Sousa-Pinto, A.: Experimental anatomical demonstration of a cortico-olivary projection from area 6 (supplementary motor area ?) in the cat. Brain Res. 16, 73--83 (1969) Sousa-Pinto, A. : The structure of the first auditory cortex (AI) in the cat. I. Light microscopic observations on its organization. Arch. itah Biol. 111, 112--137 (1973a) Sousa-Pinto, A.: Cortical projections of the mediM geniculate body in the cat. Ergebn. Anat. Entwickh-Gesch. 48, 1--42 (1973b) Sousa-Pinto, A., Reis, F.F.: Selective uptake of (3H) leucine by projection neurons of the cat auditory cortex. Brain Res. 85, 331--336 (1975) Spinelli, D.N., Starr, A., Barrett, T.W.: Auditory specificity in unit recordings from c~t's visual cortex. Exp. Neuroh 22, 75--84 (1968)

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Thompson, R.F., Johnson, R.H., Hoops, J.J.: Organization of auditory, somatic sensory and visual projections to association fields of cerebral cortex in the cat. J. Neurophysiol. 26,343--364 (1963) Wiitanen, J.T. : Selective silver impregnation of degenerating axons and axon terminals in the central nervous system of the monkey (Macaca mulatta). Brain Res. 14,546--548 (1969) Woolsey, C.N.: Organization of cortical auditory system: A review and a synthesis. In: Neural mechanisms of the auditory and vestibular systems. Ed. by G.L. Rasmussen and W.F. Windle, pp. 165--180. Springfield: Thomas 1960 M.M. Paula-Barbosa Anatomical Institute Medical Faculty University of Oporto Oporto Portugal