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The projections of the medial geniculate complex within the sylvian fissure of the rhesus monkey
Brain Research, 60 (1973) 315-333
315
© Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
T H E PROJECTIONS OF T H E M E D I A L G E N I C U L A T E COMPLEX W I T H I N T H E S Y L ¥ I A N FISSURE OF T H E RHESUS M O N K E Y *
MAREK-MARSEL MESULAM AND DEEPAK N. PANDYA Harvard Neurological Unit, Boston City Hospital, and the Aphasia Research Center, Department of Neurology, Boston University School of Medicine, Boston, Mass. 02118 (U.S.A.)
(Accepted March 12th, 1973)
SUMMARY The projection pattern of the medial geniculate complex (GM) of the rhesus monkey is studied using silver impregnation technique. The results are summarized as follows: (1) Only anterior part of the parvocellular subdivision of the medial geniculate (GMpcA) projects to the auditory koniocortex (primary auditory area - - AI). The anterior GMpcA projects posteriorly in koniocortex while the posterior GMpcA projects more anteriorly. The medial portion of GMpcA has connection to medial koniocortex while lateral GMpcA projects more laterally. (2) The posterior portion of the parvocellular medial geniculate (GMpcP) sends projections mainly to the rostral parakoniocortex - - 'auditory association area'. (3) The projections to the second auditory area (An) originate either from medial GMpcA or from GMmc (magnocellular portion of the medial geniculate nucleus). (4) No specific projections from the suprageniculate subdivision (SG) of the medial geniculate complex to either AI and AII or to the remainder of the temporal operculum were found. The possibility of such projections to the insula and the parietal operculum cannot be excluded from the present investigation. (5) GMmc may send projection to the retroinsular parietotemporal cortex (ReIpt), which on anatomical ground can be homologized to the vestibular area of cat. (6) Geniculocortical afferents terminate mainly in and around cortical lamina IV. These terminations reach the greatest density in koniocortex.
* A preliminary report of the present findings was presented at the eighty-fifth annual session of American Association of Anatomists.
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M.-M. MESULAM A N D I). N. P A N D Y A
INTRODUCTION
The projection from the medial geniculate complex to the temporal lobe has been investigated in the past by means of various techniques. Retrograde degeneration studies of Minkowski 20 showed that only ablation of the superior temporal gyrus caused retrograde degeneration in the medial geniculate body. Polyak concluded from his Marchi studies that the fibers from the medial geniculate body reach the temporal lobe by way of the retrolenticular portion of the internal capsule and are distributed almost exclusively to the supratemporal plane, where they terminate mainly in a posteromedial elevation which Polyak homologized with the transverse gyrus of Heschl in man zs. This elevation, according to Walker 40, corresponds to an area of koniocortex, which, according to this author, represents the exclusive recipient of the projection from the medial geniculate body. However, the region from which Ades and Felder 1 recorded acoustic evoked responses in deeply anesthetized monkeys extends slightly beyond the area of koniocortex described by Walker. Within this physiologically defined region Licklider and K r y t e d 4 observed a tonotopic organization with low frequencies eliciting potentials in the anterolateral portion and the higher frequencies in the posteromedial part. The studies by Walzl and Woolsey 4'~ and Walz141 further showed the existence of an additional, more medially located strip of cortex in which the tonotopical organization was reversed. The lateral region was designated as the primary auditory area (AD while the medial strip was called the second auditory area (AH). Thus the cortex responsive to auditory stimulation was found to extend considerably beyond the koniocortical area of Walker. This was further emphasized by the findings of Akert et aI. 2 and Wegener 43 who observed extensive retrograde degeneration in the posterior portion of the medial geniculate after ablation of the temporal cortex rostral to the koniocortex and rostral to the A~ and AII auditory areas of Walzl. This survey demonstrates that there exists a considerable disagreement between previous findings obtained by means of the anatomical and physiological techniques. For this reason an attempt was made to elucidate the organization of the medial geniculate cortical projection by making various lesions in the medial geniculate body and studying the distribution of the terminal degeneration in the temporal lobe, a technique which as yet has not been applied to this problem. MATERIALS A N D M E T H O D S
In 10 experiments electrolytic lesions were made in the area of the medial geniculate body with stereotaxic approach, using the coordinates from the atlas of Snider and Lee 36. Four animals received unilateral lesion, while in an additional 3 animals the lesions were placed bilaterally. On the seventh day following surgery all animals were anesthetized and perfused with normal saline followed by 10 ~ formalin. The brains were removed and stored in 10 ~ formalin for 3-4 weeks. Each hemisphere was then cut into two blocks through the coronal plane and photographed. Each pair of rostral and caudal quadrants was embedded separately in a mixture of gelatin and
317
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Fig. 1. A: lateral view of the cerebral hemisphere of Macaca mulatta, depicting the major sulci. The rectangular area contains the lateral (sylvian fissure). B." the lateral (sylvian) fissure has been opened to display both upper and lower banks as well as the insula. The upper bank is designated as parietotemporal operculum and the lower as temporal operculum with supratemporal plane. C: lateral view of the hemisphere to show the architectonic divisions of the superior temporal gyrus as they continue in the temporal operculum as shown in D. D: the architectonic fields of the temporal operculum as well as the superior temporal gyrus are shown (see text for detailed description). E: coronal section of the cerebral hemisphere to show the superior and inferior sylvian fossae. For abbreviations in this and all subsequent figures see page 331.
egg albumin and cut in frozen coronal sections 26/,m thick. Every twenty-first and twenty-second section was stained using Fink-Heimers and modified Nauta 2a methods, respectively, while each twenty-fifth section was prepared with Nissl stain. The thalamic lesion as well as the electrode track damage were reconstructed from Nissl stained sections using Olszewski's atlas 25 of the monkey thalamus for reference. The distribution of the resulting degeneration within the sylvian fissure and its immediate surroundings was plotted with the aid of an X-Y recorder. The patterns of degenerated terminals were first reconstructed on the tracings of the sylvian fissure. The degeneration on the temporal operculum* was then mapped in greater detail on the architectonic subdivisions (Fig. 1C and D), described by Sanides 3a. According to Sanides, Kam and Kalt designate medial and lateral koniocortex, * The term supratemporal plane refers to an area in the lower bank of the sylvian fissure caudal to the ventral tip of the central sulcus while the entire lower bank of the sylvian fissure is designated as temporal operculum (see Fig. 1).
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Fig. 2. On left, photographs of transverse sections passing through the thalamus (A-E) to show the area of the medial geniculate body involved by the lesions (indicated by arrow) in cases 4, 5 and 7 10. On right, photomicrographs of the representative fields from each cortical layer in case 8 to show the distribution of degenerated terminals from areas proA and Kam ( >~ 400, Fink-Heimer stain).
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Fig. 3. A: diagrammatic representation of the horizontal view of the medial geniculate, showing its subdivisions - - GMpc, GMmc and SG. B: transverse sections of thalamus to indicate the relationship of the electrode track (shown with oblique hatch lines) with thalamic nuclei, and in particular the medial geniculate complex. C: diagrammatic representation of the lateral surface of the hemisphere, in which the sylvian fissure has been opened up. The temporal operculum with cytoarchitectonic subdivisions is shown under the diagram of the hemisphere. Degeneration in the sylvian fissure from electrode passage is depicted by dots.
respectively. Area proA is the auditory prokoniocortex, while paAc, paAlt, paAr are areas of caudal, lateral and rostral auditory parakoniocortex respectively. More medially, relt and reIpt constitute retroinsular temporal and parietotemporal cortex: pal is parainsular cortex. Tpt is at the caudal tip of the supratemporal plane, while Ts3 and Ts2 are situated at its rostral end. Topographically, proA is coextensive with parts of All while Kam and Kalt are included in AI (see ref. 34). Olszewski's 2~ nomenclature has been used for the subdivisions of the medial geniculate body in which 3 components are distinguished: a lateral parvocellular (small celled) division (GMpc); an anterodorsomedial, magnocellular (large celled) division (GMmc); and a dorsomedial suprageniculate (SG) division (Fig. 3A). RESULTS
Only the degeneration within the sylvian fissure will be described. For the inter-
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pretation of the observed degenerations it is essential to rule out the possibility that the degeneration was due to the electrode track damage or due to damage of thalamocortical afferents other than those from the medial geniculate. Control experiments were therefore carried out.
Control lesions (cases 1-3) In case 1 the electrode was inserted through the parietal cortex towards the vicinity of the medial geniculate body, but remained ventral and lateral to it. Electrolytic damage occurred in pre- and parasubicular areas, immediately below the medial geniculate body. Except for patchy areas of terminal degeneration in the parietal operculum and scattered fibers in the insula and temporal operculum, the entire remainder of the sylvian fissure was free of degeneration (Fig. 3B and C). In case 2 the lesion damaged a portion of ventroposterior (VPL and VPI) and ventrolateral (VL) thalamic nuclei. The extensive degeneration was observed in the
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illustration shows degeneration within the sylvian fissure and in the architectonic subdivisions of the temporal operculum. D: transverse sections of the temporal operculum taken from levels 1-4 as indicated in C, to show the distribution of the degeneration in this case. In subsequent Figs. 5-10 the extent of the lesion and the distribution of degeneration are shown in similar manner.
PROJECTIONS OF THE MEDIAL GENICULATE
321
pre- and postcentral gyri (cf. Jones and PowellU). However, around the sylvian fissure only a few degenerated fibers were found in the pericentral and parietal opercula. In case 3 the lesion was confined to the rostromedial portion of the pulvinar nucleus. Degeneration was found in parts of the parietal and, temporal lobes. In contrast to a previous report a the degeneration in the temporal lobe was concentrated in the superior temporal sulcus, extending quite rostrally up to the temporal pole. No degeneration however, was found in the sylvian fissure.
Lesions of the medialgeniculate complex (GM) In case 4 the lesion destroyed mainly the dorsal portion of the parvocellular subdivision (GMpc). In addition, the lateralmost fringes of the magnocellular portion (GMmc) and the suprageniculate nucleus (SG) were also involved. Some damage also occurred in the ventral portion ofVPL, VPI and pulvinar nuclei (Figs. 2A, 4A and B). In striking contrast to the previous 3 cases extensive degeneration occurred in the entire sylvian fissure (Fig. 4C). The heaviest degeneration was found in the temporal operculum sparing its caudal and rostral ends. Very lateral and medial portions of the temporal operculum were likewise free of degeneration. In the upper bank of the fissure a localized area in midportion of the superior sylvian fossa (Fig. 1E) contained a substantial amount of degeneration, while only a few terminations were found in the caudal part of the insula and the parietal operculum. The degeneration within the lower bank of the sylvian fissure was especially concentrated in the koniocortex (Fig. 4C and D). The area Kalt (the lateral koniocortex) contained degenerated boutons throughout its extent, but a circumscribed sector in the caudal part of the area Kam was free of degeneration. In addition, degenerated terminals, in moderate amount, were found in areas surrounding the koniocortex: relt, medial paAc, lateral proA and paAr. Finally, relatively sparse degeneration was observed in medial paAlt and Ts3, paI and Ts2. These findings raised two questions. First, does each point in the medial geniculate project both to the koniocortex and to areas surrounding it, or do circumscribed parts of the medial geniculate project exclusively to the koniocortex? Secondly, is the degeneration-free zone in Kam a function of the size of the lesion in GM or a constant feature of geniculocortical projections? In order to answer these questions small lesions were placed in the different portions of the medial geniculate nucleus. In case 5 the lesion was limited to the rostrolateral and ventral portions of the GMpc. The fiber capsule on the lateral aspect of GM was also involved (Figs. 2B, 5A and B). This lesion was considerably smaller than case 4, more ventrolaterally placed and spared most of the caudal and medial portions of GM. The distribution of the degeneration resembled that of case 4; however, most of the degeneration was located caudal to the ventral tip of the central sulcus (Fig. 5C). The supratemporal plane, the caudal insula and the frontoparietal operculum contained degenerated terminals in different proportions. A small area in the retroinsular portion of the parietal operculum corresponding to the architectonic area relpt (Fig. 1D) showed intense degeneration.
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Both divisions of the koniocortex (Kam and Kalt) contained marked degeneration, as was observed in case 4, though it was more intense in Kalt than in Kam. The areas medial (proA) and caudal (reIt and paAc) to koniocortex also contained substantial amounts of terminations. In contrast to case 4 the lateral (paAlt) and the rostral (paAr) parakoniocortex showed only a few terminals while the rostral temporal operculum (Ts3) was totally free of degeneration. In addition there was no evidence of a circumscribed region in Kam remaining free of degeneration. In this case the degeneration was not uniformly distributed within the supratemporal plane, but certain strips of cortex showed an exceptionally intense collection of terminals which were flanked by relatively less degeneration (Fig. 5D). In case 6 the lesion was in a location similar to case 5, but extended less caudally in GMpc (Fig. 6A and B) and involved also the fiber capsule around GM and the ventroposterior thalamic nuclei (VPL, VPI). As in the preceding case, the degeneration remained predominantly caudal to the ventral tip of the central sulcus (Fig. 6C). Degenerated terminals in moderate amounts were found in the depth of the retroinsular part of the parietal operculum whereas the caudal insula and regions elsewhere in the upper bank contained only sparse terminations.
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The degeneration on the supratemporal plane was concentrated in the koniocortex, with Kalt containing heavier degeneration than Kam (Fig. 6D). Unlike cases 4 and 5, in which the lesions had extended more caudally, degeneration in the koniocortex extended far less rostrally in this case. Several areas in Kalt contained significantly more degeneration than immediately surrounding regions, and seemed to be organized in strips. The entire area Kam, except for its rostralmost part, showed uniform degeneration, leaving once again no circumscribed region free of terminals. In comparison to case 5, degeneration in proA and in areas caudal (reIt, paAc) and lateral (paAlt) to the koniocortex was considerably less. Similar to case 5 and in contrast to case 4, areas rostra1 to the koniocortex (paAr, Ts3) were free of degeneration, suggesting that terminations observed in these regions in case 4 might have originated in the caudal portion of GM. In case 7 the lesion was confined to the caudal one-third of the GMpc and encroached upon the lateral border of the suprageniculate (SG) nucleus (Figs. 2C, 7A and B). Some damage to the lateral portion of the pulvinar was also found. In contrast to all previous cases, the bulk of the degeneration in this case was
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observed in the rostral portion of the temporal operculum including inferior sylvian fossa (Fig. 1). It was heavy in area paAr and moderate in lateral pal, in Ts3 and in rostral paAlt. Degeneration in the koniocortex was limited to its rostralmost tip. In other areas of the STP degeneration was only minimal (Fig. 7C and D). With these 4 medial geniculate nucleus lesions a rostrocaudal topography of projections is clearly established. These lesions, however, involved primarily the lateral portion of the geniculate complex. In the next 3 cases the degeneration pattern originating from the medial portion of GM will be analyzed. In case 8 the lesion damaged the medial part of GMpc, sparing its lateral and caudalmost portions. Only limited damage in VPI and ventral pulvinar was found (Figs. 2D, 8A and B). In this animal, as in cases 5 and 6, degenerated terminals were observed to be concentrated mainly in regions caudal to the tip of the central sulcus (Fig. 8C). Degeneration in moderate quantity occurred in the dorsocaudal insula as well as in the parietal operculum. In the koniocortex the degeneration was quite heavy, as it was in cases 4-6. The patterns of degeneration were, however, reversed so that area Kam contained denser degeneration than Kalt. In fact, the caudolateral portion of
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Kalt remained free of degeneration. The medially located area proA also contained considerably more terminations than in any of the other cases. The remainder of the supratemporal plane relt, paAc, paAlt, and the area paAr contained degenerations comparable to cases 4 and 5. The rostral extent of degeneration of the STP was intermediate between those observed in cases 4 and 5; the same was true for the caudal extent of the lesion. Longitudinal strips of relatively heavier degeneration were observed in this case also: one in Kam adjacent to proA, another between Kam and Kalt, the third in paAlt and a fourth in medial relt (Fig. 8D). In the preceding cases the lesions mainly involved GMpc. In the next two cases the GMmc (the magnocellular division) and SG (the suprageniculate portion) were damaged. In case 9 the lesion damaged the dorsal portion of the GMmc rostrally, and the medialmost part of GMmc and SG more caudally. GMpc involvement was minimal. In addition, the lesion encroached upon VPI and VPM thalamic nuclei (Figs. 2E, 9A and B). The degeneration was chiefly observed in the upper bank of the sylvian fissure while the entire temporal operculum remained free of terminations. There was a circumscribed patch of heavy degeneration in area relpt in the retroinsular portion of
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The findings of this investigation indicate that medial geniculate projections are
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directed to the koniocortical areas in the sylvian fissure (cf. Walker 39,4°) as well as to the para- and prokoniocortical regions and to other cortical areas around the sylvian fissure. It is also found that geniculocortical projections are topographically organized and that they terminate mainly in and around layer IV.
(I) Topography of geniculocortical projections ( A ) Projections of the anterior portion of the parvocellular medial geniculate ( GMpcA ) Only the anterior two-thirds of GMpc was found to project to the temporal operculum (supratemporal plane) caudal to the tip of the central sulcus (cases 4 and 7-9) in accordance with the findings of Clark et al. 5, and Walker 39,4°. It is in this same region that cortical evoked responses to acoustic stimulation are predominantly observed 1. Furthermore, in the cat and in the monkey, the inferior colliculus projects only to the anterior part of GMpc22, 30. These complementary findings suggest that the anterior two-thirds of GMpc (GMpcA) may therefore be regarded as the auditory relay nucleus in the rhesus monkey. (1) Projections to the koniocortex (Kam and Kalt). From human material, Nagino 23 concluded that the transverse gyrus of Heschl received projections from dorsomedial GM and the remainder of STP from the ventral GM, while according to Walker39,40 in the monkey, all of GMpc projected exclusively to the koniocortex. He
328
M.-M. MESULAM AND D. N. PANDYA
concluded that ventral and posterior GMpc projected to the anterior koniocortex that dorsal and anterior GMpc projected to posterior koniocortex; and that, within the koniocortex, lateral GMpc projected more laterally while medial GMpc projected more medially. Our results indicate that only GMpcA projects with great density throughout the koniocortex (cases 5 and 6) in comparison to the projections from other parts of the medial geniculate. The present findings also indicate a topographical order within the projections of GMpcA into the koniocortex. Rostral points in GMpcA are found to project caudally in the koniocortex while caudal points project more rostrally (cases 5-7). Medial parts of GMpcA project more medially in the koniocortex while lateral points in GMpcA project more laterally in the koniocortex (cases 5 and 8). The presence of degeneration within Kam (medial koniocortex) following lateral lesions (cases 4-6) might be the result of the interruption of fibers originating from more medial GMpcA and coursing laterally and dorsally to reach the retrolenticular part of the internal capsule. (2) Projections into prokoniocortex (proA). Area proA of Sanides 34 is probably homologous to area AII of Walz141. In the cat, AII had been said to receive projections from GMpc 6,32 and from GMmc 13,21,46. In the monkey, Rundles and Papez 33, without significant evidence, suggest that AI~ receives projections from GMmc. In our study the densest degeneration in proA occurred after a medial GM lesion (case 8) suggesting that this projection is derived from medial GMpcA, or from lateroventral GMmc, or both. In this respect, it is significant that Moore and Goldberg 22 have traced input from the inferior colliculus to the lateral part of GMmc. The presence of some proA degeneration in more lateral lesions again may be ascribed to interruption of fibers. (3) Projections to the regions posterior and lateral to koniocortex. Minkowski2° and Walker39,4° reported that after destruction of banks of the sylvian fissure caudal to the koniocortex, retrograde degeneration occurred in GMpc as well as GMmc. According to the present investigation the caudal tip of STP (Tpt) receives no significant projection from GM. Projections into the lateral parakoniocortex (paAlt) come primarily from the medial part of GMpcA or, less likely, from ventrolateral GMmc (case 8). Physiologically, a substantial part of this area (relt, paAc, paAlt) has been considered as belonging to A~ and to A I I 1'12'29'41'42, thus implying that the cortical auditory receiving area extends beyond the koniocortical areas into the surrounding parakoniocortical regions. However, anatomically these parakoniocortical areas differ from the koniocortical areas themselves, in that the former have long connections to the other association areas while the latter project strictly to the parakoniocortical regions 26.
(B) Projections of the posterior portion of parvocellular medial geniculate (GMpcP) A lesion in the caudal third of GMpc (GMpcP) caused degeneration in the rostral temporal operculum (paI, Ts3 and in particular in paAr; ef. case 7). This observation is in agreement with the findings of Akert et al.2, as well as those of Wegener4L Behaviorally, ablation of the rostral portion of the temporal operculum results
P R O J E C T I O N S OF T H E MEDIAL G E N I C U L A T E
329
in initially marked but temporary deficits of both auditory and visual discrimination tasks 43. It is of interest that, anatomically, rostral parakoniocortex projects primarily to the prefrontal and orbitofrontal cortex in contrast to the projections of the caudal parakoniocortex and the koniocortexzS. This may suggest that caudal GMpc which projects to rostral parakoniocortex may therefore be functionally distinct from rostral GMpc which projects to the koniocortex and caudal parakoniocortex.
(C) Projection of the magnocellular medial geniculate (GMmc) Some of the evidence for GMmc projections to Air and to the caudal portion of the sylvian fissure has already been mentioned. In cat, the temporal and insular cortex6, 32 and the primary vestibular area in the suprasylvian gyrus16 have been shown to receive 'sustaining' projections from GMmc. In man, the supramarginal gyrus and caudal insula apparently receive projections from GMmc 19 while in the monkey, GMmc cells show degeneration only following very large temporal lobe ablations 17. Our case 8 raised the possibility of a lateral GMmc projection to proA and to paAlt. In case 9 with a lesion in GMmc a circumscribed patch of heavy degeneration occurred in the retroinsular depth of the parietal operculum (relpt), an area which received only little degeneration in the other cases. This area relpt, according to Sanides, is homologous to the suprasylvian vestibular area of the cat 3a. In this respect it is of interest to note that studies in cat, monkey and man have attributed vestibular function to GMmc 16-19. However, further research is required to elucidate the precise functional role and connections of GMmc.
(D) Projections of the suprageniculate nucleus (SG) In the cat, stimulation of SG produces evoked potentials in AII (see ref. 13). In the monkey, hemidecortication leaves SG without retrograde degeneration38. Lesions in Sr, Su and in superior parietal lobule in the monkey have resulted in anterograde degeneration in SG (see ref. 11). SG was involved in our cases 4, 9 and 10. There was no degeneration in the temporal operculum which can be attributed specifically to SG. However, the possibility that SG may project diffusely to the frontoparietal operculum and to the insula cannot be ruled out.
(E) Projections of the medial geniculate outside the superior temporal plane In some of our cases, notable projections were observed in the superior sylvian fossa. There were also some terminals in the parietal operculum and in the insula. This may be in keeping with the fact that auditory evoked responses have been found in these areas 29. Furthermore, Sudakov et al.37 have supplied physiological support for such a projection in the squirrel monkey. However, it has to be kept in mind that the opercular and insular degeneration may in part have resulted by the electrode track damage of VPL, VPI and VPM (see refs. 11 and 31).
(I1) Selective concentration of thalamic input along the STP In 3 cases (5, 6 and 8) the degeneration in STP was concentrated in longitudinal
330
M.-M. MESULAM A N D D. N. P A N D Y A
cortical strips located between proA and Kam (case 8), between Kam and Kalt (cases 5, 6 and 8), in Kalt (case 6), in paAlt (case 8), and between reIt and paAc (case 8). Comparable strips were observed by Pandya and Sanides 27 in callosal projections of the STP. Even though some of the strips in each of these two studies appear to be situated in identical architectonic fields, we cannot as yet determine whether there is precise overlap. Physiological studies, aimed at investigating the meaning of converging inputs of callosal and thalamic origin in the specific part of the auditory cortex, might be quite useful.
(III) Distribution of thalamic input within cortical layers In the opossum, thalamocortical projections from the medial geniculate end primarily in layers IV and I of primary sensory cortex, with layer IV receiving the heaviest projection 7, while in the cat they have been found to terminate in all layers with a strong component in layer I (see ref. 45). In our study the geniculate projections were found to terminate predominantly in layer 1V and deep in layer III, with layer IV containing the overwhelming majority (Fig. 2). The greater the density of terminations in layer IV, the greater was the width of layer III showing degenerations. In areas with heavy degeneration, layers V and VI were full of what we have regarded as preterminal branching of axons. Layers I and II were almost completely free of degeneration. These findings in different species suggests the existence ofa phylogenetic trend in the distribution of thalamocortical connections, in that from the opossum and cat to the monkey thalamic input becomes progressively concentrated in and around a more granularized layer IV.
(IV) Selective distribution of sensory thalamic input in the cat and monkey A comparison of data concerning thalamocortical projections in the cat and in the monkey indicates certain differences. In the somatosensory system ventroposterior nucleus (VPL-VPM) lesions in the cat lead to degeneration in SI and SII (see ref. 10). The density of degeneration is greater in S~, but in S~ the intensity of projection is approximately equal in areas 1, 2 and 3. In the monkey1~, VPL-VPM lesions produce a similar pattern of degeneration with the exception that within S~ the density of degeneration in area 3 is considerably greater than in areas 2 and 1. In the visual system, lateral geniculate (GL) lesions in the cat will lead to degeneration in areas 17-19 (see ref. 44); whereas in the monkey GL lesions lead to degeneration only in area 17 (see refs. 9 and 44). In the auditory system of the cat lesions of GMpc give rise to degeneration in At, A~r, Ep, Ea, SF and I-T cortex, presumably in equal intensity45. In our study area Tpt is shown to receive no significant projection from GM. This area Tpt, according to Sanides 34 is homologous with area Ep in the cat. These data suggest that from the cat to the monkey, fewer cortical areas receive projections from a given sensory relay nucleus. More comparative studies encompass-
PROJECTIONS OF THE MEDIAL GENICULATE
331
i n g a l a r g e r n u m b e r o f selected species w o u l d be d e s i r a b l e to ascribe a n y significance t o this t r e n d .
(II) The modality specific association nuclei of the thalamus The observation that GMpcP
p r o j e c t s exclusively to n o n - k o n i o c o r t i c a l ' a u d i -
tory association' cortex permits an analogy among modalities. I n t h e s o m a t o s e n s o r y s y s t e m o f t h e m o n k e y , V P L a n d V P M p r o j e c t to Sr a n d SII (see ref. 11). T h e l a t e r o p o s t e r i o r ( L P ) n u c l e u s , o n the o t h e r h a n d , p r o j e c t s to t h e s u p e r i o r p a r i e t a l l o b u l e w h i c h is a s o m a t o s e n s o r y a s s o c i a t i o n a r e a 11. I n t h e visual s y s t e m o f the m o n k e y , G L p r o j e c t s o n l y t o the striate c o r t e x TM. T h e p u l v i n a r , h o w ever, p r o j e c t s to a r e a s 18 a n d 19, to t h e t e m p o r o - o c c i p i t a l c o r t e x a n d to p a r t o f t h e a n t e r i o r t e m p o r a l lobe3,15,~°,2s,35, 40 all o f w h i c h a r e c o n s i d e r e d v i s u a l a s s o c i a t i o n cortex. I n t h e a u d i t o r y s y s t e m o f t h e m o n k e y , t h e p r e s e n t findings w o u l d i n d i c a t e t h a t G M p c A p r o j e c t s m a i n l y to t h e k o n i o c o r t e x w h i l e G M p c P p r o j e c t s p r e d o m i n a n t l y to t h e ' a u d i t o r y a s s o c i a t i o n ' cortex. T h e s u b c o r t i c a l c o n n e c t i o n s o f LP, p u l v i n a r a n d GMpcP
a r e n o t well k n o w n . O n e o b v i o u s c o n c l u s i o n m i g h t be t h a t t h e s e nuclei
c o n s t i t u t e a r i n g o f ' m o d a l i t y specific a s s o c i a t i o n n u c l e i ' a s s o c i a t e d w i t h p r i m a r y s e n s o r y relay nuclei.
LIST OF ABBREVIATIONS A.S. Caud. C.C. CG CI CM CS Csl FOR GL GM
= = = = = = = = = = =
GMmc
=
GMpc
=
GMpcA = GMpcP = HB I.O.S. I.P.S. LC LD
= : = = =
arcuate sulcus caudate nucleus corpus callosum central gray centralis lateralis nucleus centrum medianum nucleus central sulcus centralis superior nucleus fornix lateral geniculate nucleus medial geniculate nucleus complex magnocellular medial geniculate nucleus parvocellular medial geniculate nucleus anterior parvocellular medial geniculate nucleus posterior parvocellular medial geniculate nucleus habenula inferior occipital sulcus intraparietal sulcus line of cut laterodorsal nucleus
For abbreviations of architectonic areas see text.
L1 Lme LP L.S. MD MLF Pf P.S. Pul. i Pul. 1 Pul. m Pul. o R RN S.F. SG SN STP S.T.S. THI VL VPI VPL VPM
= = = = = = = = = = = = = = = = = = = = = = = =
nucleus limitans lateral medullary lamina lateroposterior nucleus lunate sulcus dorsomedial nucleus medial longitudinal fasciculus parafascicular nucleus principal sulcus inferior pulvinar nucleus lateral pulvinar nucleus medial pulvinar nucleus pulvinar oralis nucleus reticular nucleus red nucleus sylvian (lateral) fissure suprageniculate nucleus substantia nigra supratemporal plane superior temporal sulcus mammillothalamic tract ventrolateral nucleus ventroposterior inferior nucleus ventroposterior lateral nucleus ventroposterior medial nucleus
332
M.-M. MESULAMAND D. N. PANDYA
ACKNOWLEDGEMENTS We are grateful to Dr. N o r m a n G e s c h w i n d for his constant e n c o u r a g e m e n t and advice, to Drs. Frederich Sanides and J o n a t h a n W e g e n e r for kindly p r o v i d i n g us with preprints o f their research material, and to Dr. G a r y Van H o e s e n for helpful suggestions. We extend o u r deep a p p r e c i a t i o n to Mrs. F. Small f o r technical assistance an d to Miss D. Hall for the p r e p a r a t i o n o f illustrations. This investigation was s u p p o r te d in part by N I H G r a n t s N S 09211 and 06209.
REFERENCES 1 ADES, H. W., AND FELDER, R., The acoustic area of the monkey (Maeaca mulatta), J. Neurophysiol., 5 (1942) 49-54. 2 A~ZERT,K., WOOLSEY,C. N., DIAMOND,I. T., AND NEFF, W. T., The cortical projection area of the posterior pole of the medial geniculate body in Macaca mulatta, Anat. Rec., 133 (1959) 242. 3 CHow, K. L., A retrograde cell degeneration study of the cortical projection field of the pulvinar in monkey, J. comp. Neurol., 93 (1950) 313-340. 4 CLARK,W. E. LEGRos, The thalamic connections of the temporal lobe of the brain in monkey, J. Anat. (Lond.), 70 (1936) 447-464. 5 CLARK,W. E. LEGROS,AND NORTHFIELD,D. W. C., The cortical projection of the pulvinar in the macaque monkey, Brain, 60 (1937) 126-142. 6 DIAMOND,I. T., CHOW,K. L., AND NEFF, W. D., Degeneration of caudal medial geniculate body following cortical lesions ventral to auditory area II in the cat, J. comp. Neurol., 109 (1958) 349-362. 7 EBNER, F. F., A comparison of primitive forebrain organization in metatherian and eutherian mammals, Ann. N. Y. Acad. Sci., 167 (1969) 241-257. 8 FINK, R. P., AND HEIMER, L., Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. 9 HUBEL,D. H., AND W~ESEL,T. N., Anatomical demonstration of columns in the monkey striate cortex, Nature (Lond.), 221 (1969) 747-750. 10 JONES,E. G., AND POWELL,T. P. S., The cortical projection of the ventroposterior nucleus of the thalamus in cat, Brain, 13 (1969) 298-318. 11 JONES, E. G., AND POWELL, T. P. S., Connexions of the somatic sensory cortex of the rhesus monkey. III. Thalamic connexions, Brain, 93 (1970) 37-56. 12 KENNEDY,T. K., An Electrophysiological Study of the Auditory Projection Area of the Cortex in Monkey (Maeaca mulatta), Doctoral Dissertation, Univ. of Chicago, 1955. 13 KNIGHTON,R. S., Thalamic relay nucleus for the second somatic sensory area in the cerebral cortex of cat, J. comp. Neurol., 92 (1950) 183-191. 14 LICKLIDER,J. C. R., AND KRYTER, K. D., Frequency localization in the auditory cortex of the monkey, Fed. Proc., 1 (1942) 51. 15 LOCKE,S., The projections of the medial pulvinar of the macaque, J. comp. Neurol., 115 (1960) 155-170. 16 LOCKE, S., The projection of the magnocellular medial geniculate body, J. comp. Neurol., 116 (1961) 179-194. 17 LOCKE,S., Thalamic connection to insular and opercular cortex of monkey, J. comp. Neurol., 129 (1967) 219-240. 18 LOCKE, S., Subcortical projection of the magnocellular medial geniculate body of monkey, J. comp. Neurol., 138 (1970) 321-328. 19 LOCKE, S., ANGEVINE,JR., J. B., AND MARIN, O. S. M., Projection of the magnocellular medial geniculate nucleus in man, Brain, 85 (1962) 319-330. 20 MINKOWSKI, M., Etude sur les connexions anatomiques des circonvolutions rolandiques, pari6tales et frontales, Schweiz. Arch. Neurol. Neurochir. Psychiat., 12 (1923) 227-268. 21 MOGAMI,M., KURUDA,R., HAVAKAWA,T., ANDAKAGI,K., Efferent fibers from the magnocellular
PROJECTIONS OF THE MEDIAL GENICULATE
333
portion of the medial geniculate body. In R. DUBNER AND Y. KAWAMURA(Eds.), Oral-Facial Sensory and Motor Mechanisms, Appleton-Century-Crofts, New York, 1972, pp. 220-228. 22 MOORE, R. Y., AND GOLDRERG,J. M., Projections of the inferior colliculus in the monkey, Exp. Neurol., 14 (1960) 429-438. 23 NAGINO,I., Anatomische Untersuchungen tiber die zentralen akustischen Bahnen beim Menschen aud Grund des Studiums sekund/irer Degenerationen, Schweiz. Arch. NeuroL Neurochir. Psyehiat., 17 (1926) 229-259. 24 NAUTA, W. J. H., Silver impregnation of degenerating axons. In W. F. WINDLE (Ed.), New Research Techniques of Neuroanatomy, Thomas, Springfield, Ill., 1957, pp. 17-26. 25 OLSZEWSKI,J., The Thalamus of the Macaca mulatta, Karger, New York, 1952. 26 PANDYA,D. N., HALLETT,M., AND MUKHERJEE,S. K., Intra- and interhemispheric connections of the neocortical auditory system in the rhesus monkey, Brain Research, 14 (1969) 49-65. 27 PANOYA,D. N., AND SANIDES,F., Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern, Z. Anat. Entwickl.-Gesch., 139 (1973) 127-161. 28 POLYAK,S., The Main Afferent Fiber Systems of the Cerebral Cortex in Primates, VoL 2, Univ. of California Publications in Anatomy, Los Angeles, 1932, 370 pp. 29 PRIBRAM,K. H., BURTON,S. R., AND ROSENBLITH,W. A., Electrical responses to acoustic click in monkey. Extent of neocortex activated, J. Neurophysiol., 17 (1954) 336-344. 30 RASMUSSEN,G. L., Distribution of fibers originating from the inferior colliculus, Anat. Rec., 139 (1961) 266. 31 ROBERTS, T. S., AND AKERT, K., Insular and opercular cortex and its thalamic projection in Macaca mulatta, Schweiz. Arch. Neurol. Neurochir. Psychiat., 92 (1963) 1-43. 32 ROSE,J. E., AND WOOLSEY,C. N., Cortical connections and functional organization of the thalamic auditory system of the cat. In H. F. HARLOWAND C. N. WOOLSEY(Eds.), Biological and Biochemical Bases of Behavior, Univ. of Wisconsin Press, Madison, Wisc., 1958, pp. 127-150. 33 RUNDLES,R. W., AND PAPEZ, J. W., Fiber and cellular degeneration following temporal lobectomy in the monkey, J. comp. Neurol., 68 (1937) 267-296. 34 SANIDES, F., Representation in the cerebral cortex and its areal lamination patterns. In G. H. BOURNE (Ed.), The Structure and Function of Nervous Tissue, 1Iol. 5, Academic Press, New York, 1972, pp. 330-449. 35 SIQUEIRA,E. B., The temporo-pulvinar connections in the rhesus monkey, Arch. NeuroL (Chic.), 13 (1965) 321-330. 36 SNIDER, R. S., AND LEE, J. C., A Stereotaxic Atlas of the Monkey Brain (Macaca mulatta), Univ. of Chicago Press, Chicago, Ill., 1961. 37 SUDAKOV,K., MACLEAN, P. D., REEVES,A., ANt) MARINO, R., Unit study of exteroceptive inputs to claustrocortex in awake, sitting squirrel monkey, Brain Research, 28 (1971) 19-34. 38 WALKER, A. E., The retrograde cell degeneration in the thalamus of Macaca mulatta following hemidecortication, J. comp. Neurol., 62 (1935) 407-419. 39 WALKER,A. E., The projection of the medial geniculate body to the cerebral cortex in the macaque monkey, J. Anat. (Lond.), 71 (1937) 319-331. 40 WALKER, A. E., The Primate Thalamus, Univ. of Chicago Press, Chicago, I11., 1938, pp. 200-237. 41 WALZL, E. M., Representation of cochlea in cerebral cortex, Laryngoscope (St. Louis), 57 (1947) 778-787. 42 WALZL, E. M., AND WOOLSEY, C. N., Cortical auditory areas of the monkey as determined by electrical excitation of nerve fibers in the osseous spiral lamina and by click stimulation, Fed. Proe., 2 (1943) 52. 43 WEGENER,J. G., Unpublished observations. 44 WILSON, M. E., AND CRAGG, B. G., Projections from the lateral geniculate nucleus in cat and monkey, J. Anat. (Lond.), 101 (1967) 67%692. 45 WILSON, M. E., AND CRAGG, B. G., Projections from the medial geniculate body to the cerebral cortex in the cat, Brain Research, 13 (1969) 462-475. 46 WOOLSEY,C. N., AND WALZL, E. M., Topical projection of nerve fibers from local regions of the cochlea to the cerebral cortex of the cat, Bull. Johns Hopk. Hosp., 71 (1942) 315-344.
315
© Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
T H E PROJECTIONS OF T H E M E D I A L G E N I C U L A T E COMPLEX W I T H I N T H E S Y L ¥ I A N FISSURE OF T H E RHESUS M O N K E Y *
MAREK-MARSEL MESULAM AND DEEPAK N. PANDYA Harvard Neurological Unit, Boston City Hospital, and the Aphasia Research Center, Department of Neurology, Boston University School of Medicine, Boston, Mass. 02118 (U.S.A.)
(Accepted March 12th, 1973)
SUMMARY The projection pattern of the medial geniculate complex (GM) of the rhesus monkey is studied using silver impregnation technique. The results are summarized as follows: (1) Only anterior part of the parvocellular subdivision of the medial geniculate (GMpcA) projects to the auditory koniocortex (primary auditory area - - AI). The anterior GMpcA projects posteriorly in koniocortex while the posterior GMpcA projects more anteriorly. The medial portion of GMpcA has connection to medial koniocortex while lateral GMpcA projects more laterally. (2) The posterior portion of the parvocellular medial geniculate (GMpcP) sends projections mainly to the rostral parakoniocortex - - 'auditory association area'. (3) The projections to the second auditory area (An) originate either from medial GMpcA or from GMmc (magnocellular portion of the medial geniculate nucleus). (4) No specific projections from the suprageniculate subdivision (SG) of the medial geniculate complex to either AI and AII or to the remainder of the temporal operculum were found. The possibility of such projections to the insula and the parietal operculum cannot be excluded from the present investigation. (5) GMmc may send projection to the retroinsular parietotemporal cortex (ReIpt), which on anatomical ground can be homologized to the vestibular area of cat. (6) Geniculocortical afferents terminate mainly in and around cortical lamina IV. These terminations reach the greatest density in koniocortex.
* A preliminary report of the present findings was presented at the eighty-fifth annual session of American Association of Anatomists.
316
M.-M. MESULAM A N D I). N. P A N D Y A
INTRODUCTION
The projection from the medial geniculate complex to the temporal lobe has been investigated in the past by means of various techniques. Retrograde degeneration studies of Minkowski 20 showed that only ablation of the superior temporal gyrus caused retrograde degeneration in the medial geniculate body. Polyak concluded from his Marchi studies that the fibers from the medial geniculate body reach the temporal lobe by way of the retrolenticular portion of the internal capsule and are distributed almost exclusively to the supratemporal plane, where they terminate mainly in a posteromedial elevation which Polyak homologized with the transverse gyrus of Heschl in man zs. This elevation, according to Walker 40, corresponds to an area of koniocortex, which, according to this author, represents the exclusive recipient of the projection from the medial geniculate body. However, the region from which Ades and Felder 1 recorded acoustic evoked responses in deeply anesthetized monkeys extends slightly beyond the area of koniocortex described by Walker. Within this physiologically defined region Licklider and K r y t e d 4 observed a tonotopic organization with low frequencies eliciting potentials in the anterolateral portion and the higher frequencies in the posteromedial part. The studies by Walzl and Woolsey 4'~ and Walz141 further showed the existence of an additional, more medially located strip of cortex in which the tonotopical organization was reversed. The lateral region was designated as the primary auditory area (AD while the medial strip was called the second auditory area (AH). Thus the cortex responsive to auditory stimulation was found to extend considerably beyond the koniocortical area of Walker. This was further emphasized by the findings of Akert et aI. 2 and Wegener 43 who observed extensive retrograde degeneration in the posterior portion of the medial geniculate after ablation of the temporal cortex rostral to the koniocortex and rostral to the A~ and AII auditory areas of Walzl. This survey demonstrates that there exists a considerable disagreement between previous findings obtained by means of the anatomical and physiological techniques. For this reason an attempt was made to elucidate the organization of the medial geniculate cortical projection by making various lesions in the medial geniculate body and studying the distribution of the terminal degeneration in the temporal lobe, a technique which as yet has not been applied to this problem. MATERIALS A N D M E T H O D S
In 10 experiments electrolytic lesions were made in the area of the medial geniculate body with stereotaxic approach, using the coordinates from the atlas of Snider and Lee 36. Four animals received unilateral lesion, while in an additional 3 animals the lesions were placed bilaterally. On the seventh day following surgery all animals were anesthetized and perfused with normal saline followed by 10 ~ formalin. The brains were removed and stored in 10 ~ formalin for 3-4 weeks. Each hemisphere was then cut into two blocks through the coronal plane and photographed. Each pair of rostral and caudal quadrants was embedded separately in a mixture of gelatin and
317
PROJECTIONS OF THE MEDIAL GENICULATE
S
.
~0~~O'PAil
A
.@ \
:~
h2
"-.
pnkl! /
itosrltAl,.- " * "
CAUDAL
~ Ot,t,ttc~Jt'
SUPERIOR SYLVIAN FO$.~A
"
Fig. 1. A: lateral view of the cerebral hemisphere of Macaca mulatta, depicting the major sulci. The rectangular area contains the lateral (sylvian fissure). B." the lateral (sylvian) fissure has been opened to display both upper and lower banks as well as the insula. The upper bank is designated as parietotemporal operculum and the lower as temporal operculum with supratemporal plane. C: lateral view of the hemisphere to show the architectonic divisions of the superior temporal gyrus as they continue in the temporal operculum as shown in D. D: the architectonic fields of the temporal operculum as well as the superior temporal gyrus are shown (see text for detailed description). E: coronal section of the cerebral hemisphere to show the superior and inferior sylvian fossae. For abbreviations in this and all subsequent figures see page 331.
egg albumin and cut in frozen coronal sections 26/,m thick. Every twenty-first and twenty-second section was stained using Fink-Heimers and modified Nauta 2a methods, respectively, while each twenty-fifth section was prepared with Nissl stain. The thalamic lesion as well as the electrode track damage were reconstructed from Nissl stained sections using Olszewski's atlas 25 of the monkey thalamus for reference. The distribution of the resulting degeneration within the sylvian fissure and its immediate surroundings was plotted with the aid of an X-Y recorder. The patterns of degenerated terminals were first reconstructed on the tracings of the sylvian fissure. The degeneration on the temporal operculum* was then mapped in greater detail on the architectonic subdivisions (Fig. 1C and D), described by Sanides 3a. According to Sanides, Kam and Kalt designate medial and lateral koniocortex, * The term supratemporal plane refers to an area in the lower bank of the sylvian fissure caudal to the ventral tip of the central sulcus while the entire lower bank of the sylvian fissure is designated as temporal operculum (see Fig. 1).
318
M.-M. MESULAM AND I). N. PANDYA
Fig. 2. On left, photographs of transverse sections passing through the thalamus (A-E) to show the area of the medial geniculate body involved by the lesions (indicated by arrow) in cases 4, 5 and 7 10. On right, photomicrographs of the representative fields from each cortical layer in case 8 to show the distribution of degenerated terminals from areas proA and Kam ( >~ 400, Fink-Heimer stain).
319
PROJECTIONS OF THE MEDIAL GENICULATE
CASE I ROSTRAL
° ~
MEDIAL
~
~
I ~
~
co
~
RP cc
b
CAUDAL d
A
Fig. 3. A: diagrammatic representation of the horizontal view of the medial geniculate, showing its subdivisions - - GMpc, GMmc and SG. B: transverse sections of thalamus to indicate the relationship of the electrode track (shown with oblique hatch lines) with thalamic nuclei, and in particular the medial geniculate complex. C: diagrammatic representation of the lateral surface of the hemisphere, in which the sylvian fissure has been opened up. The temporal operculum with cytoarchitectonic subdivisions is shown under the diagram of the hemisphere. Degeneration in the sylvian fissure from electrode passage is depicted by dots.
respectively. Area proA is the auditory prokoniocortex, while paAc, paAlt, paAr are areas of caudal, lateral and rostral auditory parakoniocortex respectively. More medially, relt and reIpt constitute retroinsular temporal and parietotemporal cortex: pal is parainsular cortex. Tpt is at the caudal tip of the supratemporal plane, while Ts3 and Ts2 are situated at its rostral end. Topographically, proA is coextensive with parts of All while Kam and Kalt are included in AI (see ref. 34). Olszewski's 2~ nomenclature has been used for the subdivisions of the medial geniculate body in which 3 components are distinguished: a lateral parvocellular (small celled) division (GMpc); an anterodorsomedial, magnocellular (large celled) division (GMmc); and a dorsomedial suprageniculate (SG) division (Fig. 3A). RESULTS
Only the degeneration within the sylvian fissure will be described. For the inter-
320
M . - M . M E S U L A M A N D D. N. P A N I ) Y A
pretation of the observed degenerations it is essential to rule out the possibility that the degeneration was due to the electrode track damage or due to damage of thalamocortical afferents other than those from the medial geniculate. Control experiments were therefore carried out.
Control lesions (cases 1-3) In case 1 the electrode was inserted through the parietal cortex towards the vicinity of the medial geniculate body, but remained ventral and lateral to it. Electrolytic damage occurred in pre- and parasubicular areas, immediately below the medial geniculate body. Except for patchy areas of terminal degeneration in the parietal operculum and scattered fibers in the insula and temporal operculum, the entire remainder of the sylvian fissure was free of degeneration (Fig. 3B and C). In case 2 the lesion damaged a portion of ventroposterior (VPL and VPI) and ventrolateral (VL) thalamic nuclei. The extensive degeneration was observed in the
CASE 4
ROSTRAL
cc
R
F ] ~ a "'7"' il c i
B e
A
cAuDAL
°
"
I
I~'~4
D
-
-
Fig. 4. A: horizontal view of the medial geniculate complex to illustrate the area encompassed by the lesion (shown in black). B: transverse sections through the thalamus to show the electrode track and the extent of the lesion damage involving the medial geniculate and the other thalamic nuclei. C: this
illustration shows degeneration within the sylvian fissure and in the architectonic subdivisions of the temporal operculum. D: transverse sections of the temporal operculum taken from levels 1-4 as indicated in C, to show the distribution of the degeneration in this case. In subsequent Figs. 5-10 the extent of the lesion and the distribution of degeneration are shown in similar manner.
PROJECTIONS OF THE MEDIAL GENICULATE
321
pre- and postcentral gyri (cf. Jones and PowellU). However, around the sylvian fissure only a few degenerated fibers were found in the pericentral and parietal opercula. In case 3 the lesion was confined to the rostromedial portion of the pulvinar nucleus. Degeneration was found in parts of the parietal and, temporal lobes. In contrast to a previous report a the degeneration in the temporal lobe was concentrated in the superior temporal sulcus, extending quite rostrally up to the temporal pole. No degeneration however, was found in the sylvian fissure.
Lesions of the medialgeniculate complex (GM) In case 4 the lesion destroyed mainly the dorsal portion of the parvocellular subdivision (GMpc). In addition, the lateralmost fringes of the magnocellular portion (GMmc) and the suprageniculate nucleus (SG) were also involved. Some damage also occurred in the ventral portion ofVPL, VPI and pulvinar nuclei (Figs. 2A, 4A and B). In striking contrast to the previous 3 cases extensive degeneration occurred in the entire sylvian fissure (Fig. 4C). The heaviest degeneration was found in the temporal operculum sparing its caudal and rostral ends. Very lateral and medial portions of the temporal operculum were likewise free of degeneration. In the upper bank of the fissure a localized area in midportion of the superior sylvian fossa (Fig. 1E) contained a substantial amount of degeneration, while only a few terminations were found in the caudal part of the insula and the parietal operculum. The degeneration within the lower bank of the sylvian fissure was especially concentrated in the koniocortex (Fig. 4C and D). The area Kalt (the lateral koniocortex) contained degenerated boutons throughout its extent, but a circumscribed sector in the caudal part of the area Kam was free of degeneration. In addition, degenerated terminals, in moderate amount, were found in areas surrounding the koniocortex: relt, medial paAc, lateral proA and paAr. Finally, relatively sparse degeneration was observed in medial paAlt and Ts3, paI and Ts2. These findings raised two questions. First, does each point in the medial geniculate project both to the koniocortex and to areas surrounding it, or do circumscribed parts of the medial geniculate project exclusively to the koniocortex? Secondly, is the degeneration-free zone in Kam a function of the size of the lesion in GM or a constant feature of geniculocortical projections? In order to answer these questions small lesions were placed in the different portions of the medial geniculate nucleus. In case 5 the lesion was limited to the rostrolateral and ventral portions of the GMpc. The fiber capsule on the lateral aspect of GM was also involved (Figs. 2B, 5A and B). This lesion was considerably smaller than case 4, more ventrolaterally placed and spared most of the caudal and medial portions of GM. The distribution of the degeneration resembled that of case 4; however, most of the degeneration was located caudal to the ventral tip of the central sulcus (Fig. 5C). The supratemporal plane, the caudal insula and the frontoparietal operculum contained degenerated terminals in different proportions. A small area in the retroinsular portion of the parietal operculum corresponding to the architectonic area relpt (Fig. 1D) showed intense degeneration.
322
M.-M. MESULAM AND I). N. PANDYA c~3d
~caua
CASE 5
ROSTRAL
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KO
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Fig. 5. See legend for Fig. 4.
Both divisions of the koniocortex (Kam and Kalt) contained marked degeneration, as was observed in case 4, though it was more intense in Kalt than in Kam. The areas medial (proA) and caudal (reIt and paAc) to koniocortex also contained substantial amounts of terminations. In contrast to case 4 the lateral (paAlt) and the rostral (paAr) parakoniocortex showed only a few terminals while the rostral temporal operculum (Ts3) was totally free of degeneration. In addition there was no evidence of a circumscribed region in Kam remaining free of degeneration. In this case the degeneration was not uniformly distributed within the supratemporal plane, but certain strips of cortex showed an exceptionally intense collection of terminals which were flanked by relatively less degeneration (Fig. 5D). In case 6 the lesion was in a location similar to case 5, but extended less caudally in GMpc (Fig. 6A and B) and involved also the fiber capsule around GM and the ventroposterior thalamic nuclei (VPL, VPI). As in the preceding case, the degeneration remained predominantly caudal to the ventral tip of the central sulcus (Fig. 6C). Degenerated terminals in moderate amounts were found in the depth of the retroinsular part of the parietal operculum whereas the caudal insula and regions elsewhere in the upper bank contained only sparse terminations.
PROJECTIONS
CASE
OF THE MEDIAL
GENICULATE
323
0
6 ROSTRAL -
MEDIAL
-
A
CAUDAL
Fig. 6. See legend for Fig. 4.
The degeneration on the supratemporal plane was concentrated in the koniocortex, with Kalt containing heavier degeneration than Kam (Fig. 6D). Unlike cases 4 and 5, in which the lesions had extended more caudally, degeneration in the koniocortex extended far less rostrally in this case. Several areas in Kalt contained significantly more degeneration than immediately surrounding regions, and seemed to be organized in strips. The entire area Kam, except for its rostralmost part, showed uniform degeneration, leaving once again no circumscribed region free of terminals. In comparison to case 5, degeneration in proA and in areas caudal (reIt, paAc) and lateral (paAlt) to the koniocortex was considerably less. Similar to case 5 and in contrast to case 4, areas rostra1 to the koniocortex (paAr, Ts3) were free of degeneration, suggesting that terminations observed in these regions in case 4 might have originated in the caudal portion of GM. In case 7 the lesion was confined to the caudal one-third of the GMpc and encroached upon the lateral border of the suprageniculate (SG) nucleus (Figs. 2C, 7A and B). Some damage to the lateral portion of the pulvinar was also found. In contrast to all previous cases, the bulk of the degeneration in this case was
324
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D. N . P A N D Y A
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~
Fig. 7. See legendfor Fig. 4.
observed in the rostral portion of the temporal operculum including inferior sylvian fossa (Fig. 1). It was heavy in area paAr and moderate in lateral pal, in Ts3 and in rostral paAlt. Degeneration in the koniocortex was limited to its rostralmost tip. In other areas of the STP degeneration was only minimal (Fig. 7C and D). With these 4 medial geniculate nucleus lesions a rostrocaudal topography of projections is clearly established. These lesions, however, involved primarily the lateral portion of the geniculate complex. In the next 3 cases the degeneration pattern originating from the medial portion of GM will be analyzed. In case 8 the lesion damaged the medial part of GMpc, sparing its lateral and caudalmost portions. Only limited damage in VPI and ventral pulvinar was found (Figs. 2D, 8A and B). In this animal, as in cases 5 and 6, degenerated terminals were observed to be concentrated mainly in regions caudal to the tip of the central sulcus (Fig. 8C). Degeneration in moderate quantity occurred in the dorsocaudal insula as well as in the parietal operculum. In the koniocortex the degeneration was quite heavy, as it was in cases 4-6. The patterns of degeneration were, however, reversed so that area Kam contained denser degeneration than Kalt. In fact, the caudolateral portion of
325
PROJECTIONS OF THE MEDIAL GENICULATE CASE 8
ROSTRAL
2
b
VL
\
A
CAUDAL , ~
aua
oud
d R Pul m
~
R
:'x
t:
LC
Fig. 8. See legend for Fig. 4.
Kalt remained free of degeneration. The medially located area proA also contained considerably more terminations than in any of the other cases. The remainder of the supratemporal plane relt, paAc, paAlt, and the area paAr contained degenerations comparable to cases 4 and 5. The rostral extent of degeneration of the STP was intermediate between those observed in cases 4 and 5; the same was true for the caudal extent of the lesion. Longitudinal strips of relatively heavier degeneration were observed in this case also: one in Kam adjacent to proA, another between Kam and Kalt, the third in paAlt and a fourth in medial relt (Fig. 8D). In the preceding cases the lesions mainly involved GMpc. In the next two cases the GMmc (the magnocellular division) and SG (the suprageniculate portion) were damaged. In case 9 the lesion damaged the dorsal portion of the GMmc rostrally, and the medialmost part of GMmc and SG more caudally. GMpc involvement was minimal. In addition, the lesion encroached upon VPI and VPM thalamic nuclei (Figs. 2E, 9A and B). The degeneration was chiefly observed in the upper bank of the sylvian fissure while the entire temporal operculum remained free of terminations. There was a circumscribed patch of heavy degeneration in area relpt in the retroinsular portion of
326
M . - M . MESULAM A N D D. N. P A N D Y A
ROSTRAL
CASE 9
~
b
CNC--•
~u a
¢
MD
~
A CAUDAL ,
,
B ILC
~~S-IPS ~ V / ~ C . SPIlS. 1
,
Fig. 9. See legendfor Fig. 4. the parietal operculum. Sparse degeneration also occurred in other areas of the posterior operculum as well as in the caudal insula (Fig. 9C). In case 10 the lesion was primarily confined to the suprageniculate subdivision (SG) but damaged more caudally, a narrow strip of medioventral GMpc (Figs. 2F, 10A and B). Patchy areas with moderate amounts of degeneration were found in the insula and in the upper bank of the sylvian fissure including the retroinsular part. The koniocortex did not show any degeneration, while a portion of area paAc displayed only a minimal amount of degenerated terminals (Fig. 10C). In all these cases with medial geniculate lesions, degenerated terminals were selectively distributed to the deeper part of layer III, the entire layer IV and the superficial part of layer V. However, layer IV always contained the overwhelming majority of these degenerated terminals. In addition, among the geniculocortical projections, that projecting to the koniocortex consistently showed the heaviest degeneration (Fig. 2). DISCUSSION
The findings of this investigation indicate that medial geniculate projections are
327
PROJECTIONS OF THE MEDIAL GENICULATE
CASE I0
ROSTRAL
GMpC
B
t_,,.._~,~j p'lt~
CAUDAL
A
ud
@ Fig. 10. See legend for Fig. 4.
directed to the koniocortical areas in the sylvian fissure (cf. Walker 39,4°) as well as to the para- and prokoniocortical regions and to other cortical areas around the sylvian fissure. It is also found that geniculocortical projections are topographically organized and that they terminate mainly in and around layer IV.
(I) Topography of geniculocortical projections ( A ) Projections of the anterior portion of the parvocellular medial geniculate ( GMpcA ) Only the anterior two-thirds of GMpc was found to project to the temporal operculum (supratemporal plane) caudal to the tip of the central sulcus (cases 4 and 7-9) in accordance with the findings of Clark et al. 5, and Walker 39,4°. It is in this same region that cortical evoked responses to acoustic stimulation are predominantly observed 1. Furthermore, in the cat and in the monkey, the inferior colliculus projects only to the anterior part of GMpc22, 30. These complementary findings suggest that the anterior two-thirds of GMpc (GMpcA) may therefore be regarded as the auditory relay nucleus in the rhesus monkey. (1) Projections to the koniocortex (Kam and Kalt). From human material, Nagino 23 concluded that the transverse gyrus of Heschl received projections from dorsomedial GM and the remainder of STP from the ventral GM, while according to Walker39,40 in the monkey, all of GMpc projected exclusively to the koniocortex. He
328
M.-M. MESULAM AND D. N. PANDYA
concluded that ventral and posterior GMpc projected to the anterior koniocortex that dorsal and anterior GMpc projected to posterior koniocortex; and that, within the koniocortex, lateral GMpc projected more laterally while medial GMpc projected more medially. Our results indicate that only GMpcA projects with great density throughout the koniocortex (cases 5 and 6) in comparison to the projections from other parts of the medial geniculate. The present findings also indicate a topographical order within the projections of GMpcA into the koniocortex. Rostral points in GMpcA are found to project caudally in the koniocortex while caudal points project more rostrally (cases 5-7). Medial parts of GMpcA project more medially in the koniocortex while lateral points in GMpcA project more laterally in the koniocortex (cases 5 and 8). The presence of degeneration within Kam (medial koniocortex) following lateral lesions (cases 4-6) might be the result of the interruption of fibers originating from more medial GMpcA and coursing laterally and dorsally to reach the retrolenticular part of the internal capsule. (2) Projections into prokoniocortex (proA). Area proA of Sanides 34 is probably homologous to area AII of Walz141. In the cat, AII had been said to receive projections from GMpc 6,32 and from GMmc 13,21,46. In the monkey, Rundles and Papez 33, without significant evidence, suggest that AI~ receives projections from GMmc. In our study the densest degeneration in proA occurred after a medial GM lesion (case 8) suggesting that this projection is derived from medial GMpcA, or from lateroventral GMmc, or both. In this respect, it is significant that Moore and Goldberg 22 have traced input from the inferior colliculus to the lateral part of GMmc. The presence of some proA degeneration in more lateral lesions again may be ascribed to interruption of fibers. (3) Projections to the regions posterior and lateral to koniocortex. Minkowski2° and Walker39,4° reported that after destruction of banks of the sylvian fissure caudal to the koniocortex, retrograde degeneration occurred in GMpc as well as GMmc. According to the present investigation the caudal tip of STP (Tpt) receives no significant projection from GM. Projections into the lateral parakoniocortex (paAlt) come primarily from the medial part of GMpcA or, less likely, from ventrolateral GMmc (case 8). Physiologically, a substantial part of this area (relt, paAc, paAlt) has been considered as belonging to A~ and to A I I 1'12'29'41'42, thus implying that the cortical auditory receiving area extends beyond the koniocortical areas into the surrounding parakoniocortical regions. However, anatomically these parakoniocortical areas differ from the koniocortical areas themselves, in that the former have long connections to the other association areas while the latter project strictly to the parakoniocortical regions 26.
(B) Projections of the posterior portion of parvocellular medial geniculate (GMpcP) A lesion in the caudal third of GMpc (GMpcP) caused degeneration in the rostral temporal operculum (paI, Ts3 and in particular in paAr; ef. case 7). This observation is in agreement with the findings of Akert et al.2, as well as those of Wegener4L Behaviorally, ablation of the rostral portion of the temporal operculum results
P R O J E C T I O N S OF T H E MEDIAL G E N I C U L A T E
329
in initially marked but temporary deficits of both auditory and visual discrimination tasks 43. It is of interest that, anatomically, rostral parakoniocortex projects primarily to the prefrontal and orbitofrontal cortex in contrast to the projections of the caudal parakoniocortex and the koniocortexzS. This may suggest that caudal GMpc which projects to rostral parakoniocortex may therefore be functionally distinct from rostral GMpc which projects to the koniocortex and caudal parakoniocortex.
(C) Projection of the magnocellular medial geniculate (GMmc) Some of the evidence for GMmc projections to Air and to the caudal portion of the sylvian fissure has already been mentioned. In cat, the temporal and insular cortex6, 32 and the primary vestibular area in the suprasylvian gyrus16 have been shown to receive 'sustaining' projections from GMmc. In man, the supramarginal gyrus and caudal insula apparently receive projections from GMmc 19 while in the monkey, GMmc cells show degeneration only following very large temporal lobe ablations 17. Our case 8 raised the possibility of a lateral GMmc projection to proA and to paAlt. In case 9 with a lesion in GMmc a circumscribed patch of heavy degeneration occurred in the retroinsular depth of the parietal operculum (relpt), an area which received only little degeneration in the other cases. This area relpt, according to Sanides, is homologous to the suprasylvian vestibular area of the cat 3a. In this respect it is of interest to note that studies in cat, monkey and man have attributed vestibular function to GMmc 16-19. However, further research is required to elucidate the precise functional role and connections of GMmc.
(D) Projections of the suprageniculate nucleus (SG) In the cat, stimulation of SG produces evoked potentials in AII (see ref. 13). In the monkey, hemidecortication leaves SG without retrograde degeneration38. Lesions in Sr, Su and in superior parietal lobule in the monkey have resulted in anterograde degeneration in SG (see ref. 11). SG was involved in our cases 4, 9 and 10. There was no degeneration in the temporal operculum which can be attributed specifically to SG. However, the possibility that SG may project diffusely to the frontoparietal operculum and to the insula cannot be ruled out.
(E) Projections of the medial geniculate outside the superior temporal plane In some of our cases, notable projections were observed in the superior sylvian fossa. There were also some terminals in the parietal operculum and in the insula. This may be in keeping with the fact that auditory evoked responses have been found in these areas 29. Furthermore, Sudakov et al.37 have supplied physiological support for such a projection in the squirrel monkey. However, it has to be kept in mind that the opercular and insular degeneration may in part have resulted by the electrode track damage of VPL, VPI and VPM (see refs. 11 and 31).
(I1) Selective concentration of thalamic input along the STP In 3 cases (5, 6 and 8) the degeneration in STP was concentrated in longitudinal
330
M.-M. MESULAM A N D D. N. P A N D Y A
cortical strips located between proA and Kam (case 8), between Kam and Kalt (cases 5, 6 and 8), in Kalt (case 6), in paAlt (case 8), and between reIt and paAc (case 8). Comparable strips were observed by Pandya and Sanides 27 in callosal projections of the STP. Even though some of the strips in each of these two studies appear to be situated in identical architectonic fields, we cannot as yet determine whether there is precise overlap. Physiological studies, aimed at investigating the meaning of converging inputs of callosal and thalamic origin in the specific part of the auditory cortex, might be quite useful.
(III) Distribution of thalamic input within cortical layers In the opossum, thalamocortical projections from the medial geniculate end primarily in layers IV and I of primary sensory cortex, with layer IV receiving the heaviest projection 7, while in the cat they have been found to terminate in all layers with a strong component in layer I (see ref. 45). In our study the geniculate projections were found to terminate predominantly in layer 1V and deep in layer III, with layer IV containing the overwhelming majority (Fig. 2). The greater the density of terminations in layer IV, the greater was the width of layer III showing degenerations. In areas with heavy degeneration, layers V and VI were full of what we have regarded as preterminal branching of axons. Layers I and II were almost completely free of degeneration. These findings in different species suggests the existence ofa phylogenetic trend in the distribution of thalamocortical connections, in that from the opossum and cat to the monkey thalamic input becomes progressively concentrated in and around a more granularized layer IV.
(IV) Selective distribution of sensory thalamic input in the cat and monkey A comparison of data concerning thalamocortical projections in the cat and in the monkey indicates certain differences. In the somatosensory system ventroposterior nucleus (VPL-VPM) lesions in the cat lead to degeneration in SI and SII (see ref. 10). The density of degeneration is greater in S~, but in S~ the intensity of projection is approximately equal in areas 1, 2 and 3. In the monkey1~, VPL-VPM lesions produce a similar pattern of degeneration with the exception that within S~ the density of degeneration in area 3 is considerably greater than in areas 2 and 1. In the visual system, lateral geniculate (GL) lesions in the cat will lead to degeneration in areas 17-19 (see ref. 44); whereas in the monkey GL lesions lead to degeneration only in area 17 (see refs. 9 and 44). In the auditory system of the cat lesions of GMpc give rise to degeneration in At, A~r, Ep, Ea, SF and I-T cortex, presumably in equal intensity45. In our study area Tpt is shown to receive no significant projection from GM. This area Tpt, according to Sanides 34 is homologous with area Ep in the cat. These data suggest that from the cat to the monkey, fewer cortical areas receive projections from a given sensory relay nucleus. More comparative studies encompass-
PROJECTIONS OF THE MEDIAL GENICULATE
331
i n g a l a r g e r n u m b e r o f selected species w o u l d be d e s i r a b l e to ascribe a n y significance t o this t r e n d .
(II) The modality specific association nuclei of the thalamus The observation that GMpcP
p r o j e c t s exclusively to n o n - k o n i o c o r t i c a l ' a u d i -
tory association' cortex permits an analogy among modalities. I n t h e s o m a t o s e n s o r y s y s t e m o f t h e m o n k e y , V P L a n d V P M p r o j e c t to Sr a n d SII (see ref. 11). T h e l a t e r o p o s t e r i o r ( L P ) n u c l e u s , o n the o t h e r h a n d , p r o j e c t s to t h e s u p e r i o r p a r i e t a l l o b u l e w h i c h is a s o m a t o s e n s o r y a s s o c i a t i o n a r e a 11. I n t h e visual s y s t e m o f the m o n k e y , G L p r o j e c t s o n l y t o the striate c o r t e x TM. T h e p u l v i n a r , h o w ever, p r o j e c t s to a r e a s 18 a n d 19, to t h e t e m p o r o - o c c i p i t a l c o r t e x a n d to p a r t o f t h e a n t e r i o r t e m p o r a l lobe3,15,~°,2s,35, 40 all o f w h i c h a r e c o n s i d e r e d v i s u a l a s s o c i a t i o n cortex. I n t h e a u d i t o r y s y s t e m o f t h e m o n k e y , t h e p r e s e n t findings w o u l d i n d i c a t e t h a t G M p c A p r o j e c t s m a i n l y to t h e k o n i o c o r t e x w h i l e G M p c P p r o j e c t s p r e d o m i n a n t l y to t h e ' a u d i t o r y a s s o c i a t i o n ' cortex. T h e s u b c o r t i c a l c o n n e c t i o n s o f LP, p u l v i n a r a n d GMpcP
a r e n o t well k n o w n . O n e o b v i o u s c o n c l u s i o n m i g h t be t h a t t h e s e nuclei
c o n s t i t u t e a r i n g o f ' m o d a l i t y specific a s s o c i a t i o n n u c l e i ' a s s o c i a t e d w i t h p r i m a r y s e n s o r y relay nuclei.
LIST OF ABBREVIATIONS A.S. Caud. C.C. CG CI CM CS Csl FOR GL GM
= = = = = = = = = = =
GMmc
=
GMpc
=
GMpcA = GMpcP = HB I.O.S. I.P.S. LC LD
= : = = =
arcuate sulcus caudate nucleus corpus callosum central gray centralis lateralis nucleus centrum medianum nucleus central sulcus centralis superior nucleus fornix lateral geniculate nucleus medial geniculate nucleus complex magnocellular medial geniculate nucleus parvocellular medial geniculate nucleus anterior parvocellular medial geniculate nucleus posterior parvocellular medial geniculate nucleus habenula inferior occipital sulcus intraparietal sulcus line of cut laterodorsal nucleus
For abbreviations of architectonic areas see text.
L1 Lme LP L.S. MD MLF Pf P.S. Pul. i Pul. 1 Pul. m Pul. o R RN S.F. SG SN STP S.T.S. THI VL VPI VPL VPM
= = = = = = = = = = = = = = = = = = = = = = = =
nucleus limitans lateral medullary lamina lateroposterior nucleus lunate sulcus dorsomedial nucleus medial longitudinal fasciculus parafascicular nucleus principal sulcus inferior pulvinar nucleus lateral pulvinar nucleus medial pulvinar nucleus pulvinar oralis nucleus reticular nucleus red nucleus sylvian (lateral) fissure suprageniculate nucleus substantia nigra supratemporal plane superior temporal sulcus mammillothalamic tract ventrolateral nucleus ventroposterior inferior nucleus ventroposterior lateral nucleus ventroposterior medial nucleus
332
M.-M. MESULAMAND D. N. PANDYA
ACKNOWLEDGEMENTS We are grateful to Dr. N o r m a n G e s c h w i n d for his constant e n c o u r a g e m e n t and advice, to Drs. Frederich Sanides and J o n a t h a n W e g e n e r for kindly p r o v i d i n g us with preprints o f their research material, and to Dr. G a r y Van H o e s e n for helpful suggestions. We extend o u r deep a p p r e c i a t i o n to Mrs. F. Small f o r technical assistance an d to Miss D. Hall for the p r e p a r a t i o n o f illustrations. This investigation was s u p p o r te d in part by N I H G r a n t s N S 09211 and 06209.
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