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Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey
Brain Research, 192 (1980) 339-351 © Elsevier/North-Holland Biomedical Press
339
C O N V E R G I N G VISUAL A N D SOMATIC SENSORY CORTICAL I N P U T TO T H E I N T R A P A R I E T A L SULCUS OF T H E RHESUS M O N K E Y *
BENJAMIN SELTZER** and DEEPAK N. PANDYA **Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Mass. 01730 and Neurological Unit, Beth Israel Hospital, Boston; Departments of Neurology, Harvard Medical School and Boston University School of Medicine, Boston, Mass. (U.S.A.)
(Accepted December 13th, 1979) Key words: intraparietal sulcus - - parietal lobe - - cortical connections
SUMMARY A cyto- and myeloarchitectonic study reveals the presence of a distinct cortical zone ('area POa') in the lower bank of the intraparietal sulcus of the rhesus monkey. Using both autoradiographic and silver impregnation techniques, an analysis of cortical connections shows two overlapping projections to this sulcal zone. These come from (1) the middle portion of the preoccipital gyrus (area OA) and (2) the rostral inferior parietal lobule (area PF).
INTRODUCTION Several recent neuroanatomical studies, using silver impregnation techniques, have identified two sources of cortical input to the intraparietal sulcus of the rhesus monkey. Kuypers et alp and Pandya and Kuypers 14, investigating visual cortical pathways, showed a projection to the lower bank of the intraparietal sulcus from visual-related cortex; and Jones and Powell 8, in a study of the somatic sensory system, demonstrated afferents to the same sulcal area from the parietal lobe. The details of these projections - - the precise sources of afferents and exact sites of termination - remain, however, incompletely known. Furthermore, in terms of architectonics, the lower bank of the intraparietal sulcus is largely undefined and has not been clearly differentiated from the adjacent cortex of the inferior parietal lobule. The present * Preliminary results of this investigation were presented at the Eighth Annual Meeting, Society for Neuroscience, Saint Louis, November, 1978. ** Address for correspondence.
340 study attempts to further clarify the nature of this dual cortical input to the lower bank of the intraparietal sulcus by correlating an architectonic analysis of" that area with a detailed survey of its afferent cortical connections. MATERIALS AND METHODS In 23 rhesus monkeys radiolabeled amino acid ([3H]-Ieucine and/or -proline) was injected at different sites in parietal, temporal, or occipital cortex and the brains prepared for study by autoradiography 3. An additional 22 monkeys received ablations of cortical tissue in the same regions and were processed by the Fink-Heimer technique 5. Serial coronal sections of the ipsilateral intraparietal sulcus were then charted for the presence of terminal label or terminal degeneration. In both sets of monkeys a parallel series of sections, stained with cresyl violet, was also examined in order to locate precisely each injection or ablation and its projection. Finally, coronal sections of three unoperated hemispheres, stained with cresyl violet and by Loyez or Heidenhain technique, were used to study the cyto- and myeloarchitecture of the cortex within the intraparietal sulcus. A diagram of the buried sulcal cortex (Fig. 1) was constructed in order to portray both connectional and architectonic results. In this diagram the upper and lower banks of the intraparietal sulcus were drawn in proportion to the actual dimensions of these surfaces. RESULTS
Architectonic parcellation (Figs. 1 and 2) At its rostral tip, the intraparietal sulcus is occupied by cortex identical to that of the nearby area 2 (ref. 2). At its caudal limit, where it merges with the lunate sulcus and its depth expands to become the annectent gyrus, the cortex of the intraparietal sulcus belongs to type 'OA' of Bonin and Bailey 1 (or area 19 of Brodmann2). Between these two topographical extremes, however, the lower bank of the intraparietal sulcus is composed of a different, and distinct, architectonic zone. This area, termed POa, is a rostrocaudally oriented strip of cortex. In the transverse plane, two subdivisions may be seen (Fig. 1). The internal division (POa-i) has an indistinct second cortical layer. The third layer is broad but only lightly populated with cells. Scattered large globular-shaped IIIc pyramidal cells appear especially prominent against this relatively acellular background. The fourth layer is also broad but sparsely populated with small granular cells. Occasional large pyramidal cells are the only outstanding features of layer five. The sixth cortical layer, while clearly separable from the fifth, is also quite modestly developed (Fig. 2C). The external division (POa-e) is more cellular than the internal division. The third layer is relatively more densely packed with cells. As a result, large IIIc pyramidal cells, though still present in considerable numbers, do not stand out as
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Fig. 1. Above: drawing of the lateral surface of the cerebral hemisphere of Macaca mulatta to show the architectonic parcellation of the lower bank of the intraparietal sulcus. The intraparietal and lunate sulei are opened, and an interrupted line separates the upper and lower banks of the intraparietal sulcus. Areas POa-i and POa-e are cross-hatched for clearer visualization. Below: drawings of coronal sections of the cerebral hemisphere, taken at levels 1-3 indicated on the upper illustration, to show the architectonic parcellation of the lower bank of the intraparietal sulcus. Abbreviations: ann., annectent gyrus; ar., arcuate sulcus; ce., central sulcus; i.p., intraparietal sulcus; 1., lunate sulcus; lat., lateral sulcus (Sylvian fissure); o.i., occipitoinferior sulcus; pr., principal sulcus; s.t., superior temporal sulcus. prominently as they do in the internal division. The fourth layer is a thin ribbon o f closely spaced granular cells. The fifth layer has two discernible sublayers: Va and Vb, The sixth layer is not significantly different from its counterpart in subdivision POa-i (Fig. 2C). In terms o f myelination, area P O a has a moderately dense plexus o f vertically directed myelinated fibers in the deepest cortical layers. Only the external division (POa-e), however, has a distinct outer b a n d o f Baillarger, while in the internal division (POa-i) the inner and outer bands are merged (Fig. 2B).
342 According to the cytoarchitectonic parcellation of Bonin and Bailey 1, the lower bank o f the intraparietal sulcus in this vicinity is composed o f the same ' P G ' - t y p e cortex that invests the inferior parietal lobule. A comparison o f these adjacent regions reveals, however, a striking difference. Area PG has a columnar-appearing cortex with well-developed third and fourth cell layers. In this region, Va pyramidal cells are large and distinct, clearly set off from the prominent sixth layer. The two adjacent regions also differ in terms of myeloarchitecture since area POa is more heavily myelinated than area PG (Fig. 2A, B). In agreement with previous architectonic studies ~,2, the present parcellation assigns much o f the cortex of the posterior part o f the intraparietal sulcus to type ' O A ' o f Bonin and Bailey or area 19 of Brodmann. Like area PG, area O A is also easily distinguishable from area POa, both in terms o f cyto- and myeloarchitecture.
Connectional studies Occipital lobe, peristriate belt, and inferotemporal area Injections. Twelve monkeys had injections o f radiolabeled amino acid in these
Fig. 2. A: photomicrograph of a coronal section of the parietal lobe to show the cytoarchitectonic parcellation of the lower bank of the intraparietal sulcus. Cresyl violet stain. B: photomicrograph of a coronal section of the parietal lobe to show the myeloarchitectonic parcellation of the lower bank of the intraparietal sulcus. I4eidenhain stain. Both A and B are taken at approximately level 2 indicated on Fig. 1. C: higher power view of the lower bank of the intraparietal sulcus in Fig. 2A to illustrate the detailed cytological appearance of each cortical cell layer (i-vi) of areas POa-i and POa-e.
343
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Fig. 3. Diagrammatic representation of the distribution of silver grain (shown by dots) within the lower bank of the intraparietal sulcus in 4 cases with injections of isotope in various parts of the peristriate belt. Injection sites are shown in black. Cross-hatching signifies adjacent spread of isotope. For case 1, a coronal section, taken at level 1, is also shown. Silver grain in areas other than the intraparietal sulcus is not illustrated. Abbreviations as in Fig. 1.
visual-related areas of cerebral cortex. Only those with injections on the lateral aspect of the peristriate belt (area OA) had significant terminal label in the lower bank of the intraparietal sulcus (area POa). Cases 1 and 2 had intracortical injections in the mid-portion of the preoccipital gyrus (area OA). In both cases, silver grain was distributed in a rostrocaudallyoriented band located in the lower bank of the intraparietal sulcus (Figs. 3 and 8). This fell predominantly within the posterior portion of area POa with some extension into the more rostral part of this sulcal zone. Silver grain appeared to be situated within both subdivisions of area POa, and there was a slight interruption at the point of architectonic transition between area POa-e and area POa-i. Cases 3 and 4 also had preoccipital injections, but in a somewhat more ventral location (Fig. 3). Unlike the first two cases, however, these animals had only a scant amount of silver grain in area POa. (Since the present study focuses solely on the projection to area POa, additional label in other cortical zones is not illustrated and will not be further discussed.) Injections in other portions of the peristriate belt did not produce significant terminal label in the lower bank of the intraparietal sulcus (area POa) (Fig. 3). These
344 included injections on the ventral and medial surfaces of the peristriate belt (areas OA and OB; cases 5 9) as well as a portion of the annectent gyrus (case 10). Injections in primary visual cortex (area OC, case 11) and the inferotemporal area (case 12) also gave negative results. Ablations. Cases 13-16 had lesions, of different sizes, on the lateral surface of the peristriate belt in the preoccipital gyrus (area OA). None of these animals had significant destruction of area OB or nearby parietal ( P G or 7) cortex. The resulting terminal degeneration in the lower bank of the intraparietal sulcus is illustrated, using two representative cases, in Fig. 4. Although the amount, and precise location, o t degeneration varied fi'om case to case, the basic pattern was essentially the same in all. Two,'_more or less continuous, parallel bands of terminal degeneration were found. These fell within the posterior portions of the two subdivisions of area POa. There was a clear separation between degeneration in the internal and external divisions. In contrast to the first 4 cases, m o n k e y 17 had a lesion in the most dorsal portion of the preoccipital gyrus (Fig. 4), and m o n k e y 18 (not illustrated) on the medial surface of the peristriate belt. Both lesions chiefly involved area OA, but neither produced significant terminal degeneration in area POa. Lesions in primary visual cortex (area OC, case 19) and the inferotemporal area (case 20) also failed to produce degeneration in area POa. ~ ~!~i
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Fig. 4. Diagrammatic representation of the distribution of terminal degeneration (shown by dots) within the lower bank of the intraparietal sulcus in 3 selected cases with cortical ablations (drawn in black) of portions of the peristriate belt. For case 13, two coronal sections, taken at levels 1 and 2, are also illustrated. Only degeneration within the intraparietal sulcus is shown. Abbreviations as in Fig. 1.
345
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Fig. 5. Diagrammatic representation of the distribution of silver grain within the lower bank of the intraparietal sulcus in 3 cases with injectionsof isotope at differentsites in the inferior parietal lobule. Abbreviations as in Fig. 1. Thus, combining the results of both autoradiographic and silver impregnation studies, it is apparent that, of all the regions surveyed, only a discrete sector on the lateral surface of the preoccipital gyrus projects to the lower bank of the intraparietal sulcus. Furthermore, this projection is directed to the posterior portions of the two divisions of area POa.
Parietal lobe Injections. Eleven animals received injections of radiolabeled amino acid at various sites in the parietal lobe. Only two, with injections in the rostral inferior parietal lobule (area PF), showed silver grain in the lower bank of the intraparietal sulcus (area POa). In both cases 21 and 22, the injection was situated within area PF in the rostral inferior parietal lobule. Although a small amount of isotope extended into area 2 at the rostral tip of the intraparietal sulcus, it did not spread caudally into area PG or into other portions of the sulcus. As shown in Fig. 5, a band of silver grain in the lower bank of the intraparietal sulcus could be traced caudally from the injection site in both of these animals. Label extended over the rostral portion of area POa (Figs. 5 and 8). Although 6 other monkeys (cases 23-28) had injections in the mid- and caudal inferior parietal lobule (area PG), a region immediately adjacent to area POa, silver grain remained within the confines of area PG and did not extend into area POa (Fig.
346 5). One injection in the caudal superior parietal lobule (case 29) and two on the medial surface of the parietal lobe (cases 30 and 31 ) also failed to show label in the lower bank of the intraparietal sulcus.
Ablations. Fourteen monkeys had ablations in various parts of the parietal lobe.
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Fig. 6. Diagrammatic representation of the distribution of terminal degeneration within the lower bank of the intraparietal sulcus in 5 cases with cortical ablations of the postcentral gyrus or inferior parietal lobule. Abbreviations as in Fig. 1.
347
Fig. 7. Summarydiagram to show the two major sources of cortical input to areas POa-i and POa-e in the lower bank of the intraparietal sulcus. Only those with damage in either the rostral inferior parietal lobule (area PF) or in the lower bank of the intraparietal sulcus had terminal degeneration in area POa. Monkey 32 had a large lesion in the rostral one-third of the inferior parietal lobule (area PF). This case displayed a prominent focus of degeneration in the rostral lower bank of the intraparietal sulcus (Fig. 6). Degeneration was disposed in a more or less continuous band situated within the limits of area POa. An essentially identical pattern of terminal degeneration was seen in the intraparietal sulcus of case 33 (Fig. 6). This animal had a somewhat smaller lesion, situated just in front of the rostral tip of the intraparietal sulcus, that destroyed a portion of area 2 in addition to PF-type cortex. Lesions restricted to the post-central gyrus (areas 3, 1 and 2) and not involving area PF (monkeys 34 and 35), however, did not produce terminal degeneration within area POa (Fig. 6). In case 36, the cortical lesion directly involved the lower bank of the intraparietal sulcus (area POa) (Fig. 6). This produced abundant degeneration in the same cortical zone. Three other cases (monkeys 37-39), with mid-inferior parietal lobule lesions, also had terminal degeneration in area POa. Two of these cases (monkeys 37 and 38), however, had ablations which involved part of the adjacent lower bank of the intraparietal sulcus (area POa), and the third (case 39) had a large lesion that extended rostrally to involve a portion of area PF. Smaller lesions, restricted to PG cortex in the posterior two-thirds of the inferior parietal lobule (cases 40~2), failed to produce degeneration in area POa despite the close proximity of the ablations to that sulcal region (Fig. 6). Finally, lesions of the superior parietal lobule and adjacent upper bank of the intraparietal sulcus (cases 43-45) ¢¢ere also without terminal degeneration in the lower bank of the sulcus. Thus, both autoradiographic and silver impregnation studies reveal that area POa receives extrinsic parietal connections exclusively from a sector in the rostral
348 inferior parietal lobule (area PF). This projection is confined to the rostral portion of area POa. DISCUSSION An architectonic study reveals the presence of a distinct cortical zone - area POa - - in the lower bank of the intraparietal sulcus of the rhesus monkey. An analysis of its cortical connections shows two major sources of input: the middle portion of the preoccipital gyrus (area OA) and the rostral inferior parietal lobule (area PF). The preoccipital projection is mainly to the posterior part of area POa, and the parietal projection to the anterior, but both projections overlap each other to some extent (Fig. 7). Although previous studiesS,9, t4 indicated somewhat similar connections, they did not specify the precise sources of afferents or their exact sites of termination. Furthermore, up to the present time, an architectonic study of this region has been lacking. In the present investigation an architectonically defined zone in the intraparietal sulcus is shown to be the consistent target of two major cortical projections. Furthermore, the morphological division of area POa into two elongated sectors is matched by the distribution of terminals in rostrocaudally oriented bands. In the absence of physiological or behavioral studies specifically addressed to this area of the parietal lobe, one can only speculate on the functional significance of area POa. The pattern of its afferent cortical connections may, however, suggest several possibilities. Numerous anatomical, physiological, and behavioral studies indicate sensoryrelated functions for the two cortical regions that project to area POa. The preoccipital gyrus is a recipient of fibers (by way of area OB) from primary visual cortex4,9,16,zk Physiological studies show this region to be responsive to visual stimuli 2z, and lesions of the preoccipital gyrus cause behavioral deficits involving the visual modality 1t. The rostral inferior parietal lobule (area PF of Bonin and Bailey'), the other source of afferents to area POa, receives input from primary somatic sensory cortex of the postcentral gyrus 7,t4,J9 as well as from the second somatic sensory areal4, TM. This region is believed to play a role in somatic sensory-related activity 1°,Ie. In the light of these facts, it is reasonable to propose that the preoccipital gyrus transmits visual information to area POa and that the rostral inferior parietal lobule transmits somatic sensor>' information to that same sulcal area. Furthermore, available evidence allows the nature of these inputs to be more precisely defined. Recent anatomical studies show that the sequence of cortical visual connections is organized in topographical fashion 4,16,21. Thus, the portion of area OA situated in the midpreoccipital gyrus receives input, by way of area OB, from that portion of striate cortex (area OC) sensitive to stimuli in the opposite peripheral visual field 16. The cortical connections of the somatic sensory system are also topographical. Thus, the rostral inferior parietal lobule (area PF) receives fibers from the ventral postcentral gyrus 7,14,19, that portion of primary somatic sensory cortex which relates to the contralateral head and neck 2°. Its other major source of cortical input, the second somatic sensory area ~s, is also largely responsive to stimuli coming from rostral parts
349
Fig. 8. Four photomicrographs to show two sites of intracortical isotope injection and the resulting terminal label within the lower bank of the intraparietal sulcus. A: the injection site in the preoccipital gyrus (area OA) in case 1 (× 8); B: the resulting distribution of terminal label in area POa (x 63); C: the injection site in the rostral inferior parietal lobule (area PF) in case 21 (x 8); D: the resulting distribution of terminal label in area POa ( x 63). of the b o d y 2°. In functional terms, therefore, area P O a appears to receive two highly specific inputs: visual information from the contralateral peripheral visual field, by way of the middle portion o f the preoccipital gyrus, and kinesthetic information from the contralateral head and neck, via area PF. Although an interaction between these two inputs remains to be shown, their convergence in the intraparietal sulcus suggests that area P O a is involved in integrating visual and somatic sensory information and thus relating the position o f the head and neck to the visual environment. In this connection, one other point should be mentioned. The rostral inferior parietal lobule, in addition to its afferent connections with somatic sensory cortex, has also been
350 shown to c o n t a i n cortex responsive to vestibular stimulation 17. Thus, area P O a may also integrate vestibular i n p u t with both visual and somatic sensory i n l b r m a t i o n . In recent years, several studies have investigated the functions o f p o s t e r i o r parietal cortex6,13,1~. A c c o r d i n g to some o f these investigators, the integration o f visual a n d somatic sensory i n f o r m a t i o n is the functional substrate o f certain o f these c o m p l e x behaviors 15. A l t h o u g h these studies have dealt principally with the exposed cortex o f the inferior parietal lobule (area PG), a n d only incidentally with the cortex b u r i e d within the i n t r a p a r i e t a l sulcus, the present study offers a n a t o m i c a l evidence l b r such a m e c h a n i s m in at least a p o r t i o n o f the p o s t e r i o r p a r i e t a l lobe. ACKNOWLEDGEMENTS W e t h a n k Dr. K a t h l e e n S. R o c k l a n d for p r o v i d i n g some o f the a u t o r a d i o g r a p h i c m a t e r i a l a n d Dr. T h o m a s L. K e m p e r for allowing us to examine sections for the architectonic study. W e are also grateful to Miss Valerie Killgren, Miss K a t h l e e n Barry, a n d Ms. Eileen K o t o p o u l i s for p r o v i d i n g technical assistance. This study was s u p p o r t e d by N I H G r a n t N S 09211 a n d V A G r a n t 6901.
REFERENCES 1 Bonin, G. von and Bailey, P., The Neocortex ofMacaca mulatta, University of Illinois Press, Urbana, I11., 1947, pp. 1-163. 2 Brodmann, K., Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien Dargestellt aufGrund des Zellenbaues, Barth, Leipzig, 1909, pp. 1-324. 3 Cowan, W. M., Gottlieb, D. I., Hendrickson, A. E., Price, J. L. and Woolsey, T. A., Autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37 (1972) 21-51. 4 Cragg, B. G. and Ainsworth, A., The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method, Vision Res., 9 (1969) 733-747. 5 Fink, R. P. and I-Ieimer, 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. 6 Hyvarinen, J. and Poranen, A., Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys, Brain, 97 (1974) 673-692. 7 Jones, E. G. and Powell, T. P. S., Connexions of the somatic sensory cortex in the rhesus monkey. I. Ipsilateral cortical connexions, Brain, 92 (1969) 477-502. 8 Jones, E. G. and Powell, T. P. S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 793-820. 9 Kuypers, H. G. J. M., Szwarcbart, M., Mishkin, M. and Rosvold, H. E., Occipitotemporal corticocortical connections in the rhesus monkey, Exp. Neurol., 11 (1965) 245-262. 10 Leinonen, L., Hyv~irinen, J., Nyman, G. and Linnankoski, I., I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys, Exp. Brain Res., 34 (1979) 299-320. 11 Mishkin, M., Visual mechanisms beyond the striate cortex. In R. W. Russell (Ed.), Frontiers in PhysiologicalPsychology, Academic Press, New York, 1966, pp. 93 119. 12 Moffett, A., Ettlinger, G., Morton, H. B. and Piercy, M. F., Tactile discrimination performance in the monkey: the effect of ablation of various subdivisions of posterior parietal cortex, Cortex, 3 (1967) 59-96. 13 Mountcastle, V. B., Lynch, J. C., Georgopoulos, A., Sakata, H. and Acuna, C., Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space, J. NeurophysioL, 38 (1975) 871-908. 14 Pandya, D. N. and Kuypers, H. G. J. M., Cortico-cortical connections in the rhesus monkey, Brain Research, 13 (1969) 13-36.
351 15 Robinson, D. L., Goldberg, M. E. and Stanton, G. B., Parietal association cortex in the primate: sensory mechanisms and behavioral modulations, J. Neurophysiol., 41 (1978) 910-932. 16 Rockland, K. S., Cortical Connections of the OccipitalLobe in the Rhesus Monkey, Doctoral dissertation, Boston University, Boston, 1979. 17 Schwarz, D. W. F. and Frederickson, J. M., Rhesus monkey vestibular cortex, a bimodal primary projection field, Science, 172 (1971) 280-281. 18 Stanton, G. B., Cruce, W. L. R., Goldberg, M. E. and Robinson, D. L., Some ipsilateral projections to areas PF and PG of the inferior parietal lobule in monkeys, Neurosci. Lett., 6 (1977) 243-250. 19 Vogt, B. A. and Pandya, D. N., Cortico-cortical connections of somatic sensory cortex (areas 3, 1, and 2) in the rhesus monkey, J. comp. NeuroL, 177 (1978) 179-192. 20 Woolsey, C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. FIarlow and C. N. Woolsey (Eds.), Biological and Biochemical Bases of Behavior, University of Wisconsin Press, Madison, Wisc., 1958, pp. 63-81. 21 Zeki, S. M., Representation of central visual fields in prestriate cortex of monkey, Brain Research, 14 (1969) 271-291. 22 Zeki, S. M., Functional specialisation in the visual cortex of the rhesus monkey, Nature (Lond.), 274 (1978) 423-428.
339
C O N V E R G I N G VISUAL A N D SOMATIC SENSORY CORTICAL I N P U T TO T H E I N T R A P A R I E T A L SULCUS OF T H E RHESUS M O N K E Y *
BENJAMIN SELTZER** and DEEPAK N. PANDYA **Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Mass. 01730 and Neurological Unit, Beth Israel Hospital, Boston; Departments of Neurology, Harvard Medical School and Boston University School of Medicine, Boston, Mass. (U.S.A.)
(Accepted December 13th, 1979) Key words: intraparietal sulcus - - parietal lobe - - cortical connections
SUMMARY A cyto- and myeloarchitectonic study reveals the presence of a distinct cortical zone ('area POa') in the lower bank of the intraparietal sulcus of the rhesus monkey. Using both autoradiographic and silver impregnation techniques, an analysis of cortical connections shows two overlapping projections to this sulcal zone. These come from (1) the middle portion of the preoccipital gyrus (area OA) and (2) the rostral inferior parietal lobule (area PF).
INTRODUCTION Several recent neuroanatomical studies, using silver impregnation techniques, have identified two sources of cortical input to the intraparietal sulcus of the rhesus monkey. Kuypers et alp and Pandya and Kuypers 14, investigating visual cortical pathways, showed a projection to the lower bank of the intraparietal sulcus from visual-related cortex; and Jones and Powell 8, in a study of the somatic sensory system, demonstrated afferents to the same sulcal area from the parietal lobe. The details of these projections - - the precise sources of afferents and exact sites of termination - remain, however, incompletely known. Furthermore, in terms of architectonics, the lower bank of the intraparietal sulcus is largely undefined and has not been clearly differentiated from the adjacent cortex of the inferior parietal lobule. The present * Preliminary results of this investigation were presented at the Eighth Annual Meeting, Society for Neuroscience, Saint Louis, November, 1978. ** Address for correspondence.
340 study attempts to further clarify the nature of this dual cortical input to the lower bank of the intraparietal sulcus by correlating an architectonic analysis of" that area with a detailed survey of its afferent cortical connections. MATERIALS AND METHODS In 23 rhesus monkeys radiolabeled amino acid ([3H]-Ieucine and/or -proline) was injected at different sites in parietal, temporal, or occipital cortex and the brains prepared for study by autoradiography 3. An additional 22 monkeys received ablations of cortical tissue in the same regions and were processed by the Fink-Heimer technique 5. Serial coronal sections of the ipsilateral intraparietal sulcus were then charted for the presence of terminal label or terminal degeneration. In both sets of monkeys a parallel series of sections, stained with cresyl violet, was also examined in order to locate precisely each injection or ablation and its projection. Finally, coronal sections of three unoperated hemispheres, stained with cresyl violet and by Loyez or Heidenhain technique, were used to study the cyto- and myeloarchitecture of the cortex within the intraparietal sulcus. A diagram of the buried sulcal cortex (Fig. 1) was constructed in order to portray both connectional and architectonic results. In this diagram the upper and lower banks of the intraparietal sulcus were drawn in proportion to the actual dimensions of these surfaces. RESULTS
Architectonic parcellation (Figs. 1 and 2) At its rostral tip, the intraparietal sulcus is occupied by cortex identical to that of the nearby area 2 (ref. 2). At its caudal limit, where it merges with the lunate sulcus and its depth expands to become the annectent gyrus, the cortex of the intraparietal sulcus belongs to type 'OA' of Bonin and Bailey 1 (or area 19 of Brodmann2). Between these two topographical extremes, however, the lower bank of the intraparietal sulcus is composed of a different, and distinct, architectonic zone. This area, termed POa, is a rostrocaudally oriented strip of cortex. In the transverse plane, two subdivisions may be seen (Fig. 1). The internal division (POa-i) has an indistinct second cortical layer. The third layer is broad but only lightly populated with cells. Scattered large globular-shaped IIIc pyramidal cells appear especially prominent against this relatively acellular background. The fourth layer is also broad but sparsely populated with small granular cells. Occasional large pyramidal cells are the only outstanding features of layer five. The sixth cortical layer, while clearly separable from the fifth, is also quite modestly developed (Fig. 2C). The external division (POa-e) is more cellular than the internal division. The third layer is relatively more densely packed with cells. As a result, large IIIc pyramidal cells, though still present in considerable numbers, do not stand out as
341
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3
Fig. 1. Above: drawing of the lateral surface of the cerebral hemisphere of Macaca mulatta to show the architectonic parcellation of the lower bank of the intraparietal sulcus. The intraparietal and lunate sulei are opened, and an interrupted line separates the upper and lower banks of the intraparietal sulcus. Areas POa-i and POa-e are cross-hatched for clearer visualization. Below: drawings of coronal sections of the cerebral hemisphere, taken at levels 1-3 indicated on the upper illustration, to show the architectonic parcellation of the lower bank of the intraparietal sulcus. Abbreviations: ann., annectent gyrus; ar., arcuate sulcus; ce., central sulcus; i.p., intraparietal sulcus; 1., lunate sulcus; lat., lateral sulcus (Sylvian fissure); o.i., occipitoinferior sulcus; pr., principal sulcus; s.t., superior temporal sulcus. prominently as they do in the internal division. The fourth layer is a thin ribbon o f closely spaced granular cells. The fifth layer has two discernible sublayers: Va and Vb, The sixth layer is not significantly different from its counterpart in subdivision POa-i (Fig. 2C). In terms o f myelination, area P O a has a moderately dense plexus o f vertically directed myelinated fibers in the deepest cortical layers. Only the external division (POa-e), however, has a distinct outer b a n d o f Baillarger, while in the internal division (POa-i) the inner and outer bands are merged (Fig. 2B).
342 According to the cytoarchitectonic parcellation of Bonin and Bailey 1, the lower bank o f the intraparietal sulcus in this vicinity is composed o f the same ' P G ' - t y p e cortex that invests the inferior parietal lobule. A comparison o f these adjacent regions reveals, however, a striking difference. Area PG has a columnar-appearing cortex with well-developed third and fourth cell layers. In this region, Va pyramidal cells are large and distinct, clearly set off from the prominent sixth layer. The two adjacent regions also differ in terms of myeloarchitecture since area POa is more heavily myelinated than area PG (Fig. 2A, B). In agreement with previous architectonic studies ~,2, the present parcellation assigns much o f the cortex of the posterior part o f the intraparietal sulcus to type ' O A ' o f Bonin and Bailey or area 19 of Brodmann. Like area PG, area O A is also easily distinguishable from area POa, both in terms o f cyto- and myeloarchitecture.
Connectional studies Occipital lobe, peristriate belt, and inferotemporal area Injections. Twelve monkeys had injections o f radiolabeled amino acid in these
Fig. 2. A: photomicrograph of a coronal section of the parietal lobe to show the cytoarchitectonic parcellation of the lower bank of the intraparietal sulcus. Cresyl violet stain. B: photomicrograph of a coronal section of the parietal lobe to show the myeloarchitectonic parcellation of the lower bank of the intraparietal sulcus. I4eidenhain stain. Both A and B are taken at approximately level 2 indicated on Fig. 1. C: higher power view of the lower bank of the intraparietal sulcus in Fig. 2A to illustrate the detailed cytological appearance of each cortical cell layer (i-vi) of areas POa-i and POa-e.
343
~p
CASE4
CASE 5
Fig. 3. Diagrammatic representation of the distribution of silver grain (shown by dots) within the lower bank of the intraparietal sulcus in 4 cases with injections of isotope in various parts of the peristriate belt. Injection sites are shown in black. Cross-hatching signifies adjacent spread of isotope. For case 1, a coronal section, taken at level 1, is also shown. Silver grain in areas other than the intraparietal sulcus is not illustrated. Abbreviations as in Fig. 1.
visual-related areas of cerebral cortex. Only those with injections on the lateral aspect of the peristriate belt (area OA) had significant terminal label in the lower bank of the intraparietal sulcus (area POa). Cases 1 and 2 had intracortical injections in the mid-portion of the preoccipital gyrus (area OA). In both cases, silver grain was distributed in a rostrocaudallyoriented band located in the lower bank of the intraparietal sulcus (Figs. 3 and 8). This fell predominantly within the posterior portion of area POa with some extension into the more rostral part of this sulcal zone. Silver grain appeared to be situated within both subdivisions of area POa, and there was a slight interruption at the point of architectonic transition between area POa-e and area POa-i. Cases 3 and 4 also had preoccipital injections, but in a somewhat more ventral location (Fig. 3). Unlike the first two cases, however, these animals had only a scant amount of silver grain in area POa. (Since the present study focuses solely on the projection to area POa, additional label in other cortical zones is not illustrated and will not be further discussed.) Injections in other portions of the peristriate belt did not produce significant terminal label in the lower bank of the intraparietal sulcus (area POa) (Fig. 3). These
344 included injections on the ventral and medial surfaces of the peristriate belt (areas OA and OB; cases 5 9) as well as a portion of the annectent gyrus (case 10). Injections in primary visual cortex (area OC, case 11) and the inferotemporal area (case 12) also gave negative results. Ablations. Cases 13-16 had lesions, of different sizes, on the lateral surface of the peristriate belt in the preoccipital gyrus (area OA). None of these animals had significant destruction of area OB or nearby parietal ( P G or 7) cortex. The resulting terminal degeneration in the lower bank of the intraparietal sulcus is illustrated, using two representative cases, in Fig. 4. Although the amount, and precise location, o t degeneration varied fi'om case to case, the basic pattern was essentially the same in all. Two,'_more or less continuous, parallel bands of terminal degeneration were found. These fell within the posterior portions of the two subdivisions of area POa. There was a clear separation between degeneration in the internal and external divisions. In contrast to the first 4 cases, m o n k e y 17 had a lesion in the most dorsal portion of the preoccipital gyrus (Fig. 4), and m o n k e y 18 (not illustrated) on the medial surface of the peristriate belt. Both lesions chiefly involved area OA, but neither produced significant terminal degeneration in area POa. Lesions in primary visual cortex (area OC, case 19) and the inferotemporal area (case 20) also failed to produce degeneration in area POa. ~ ~!~i
CASE13
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CASE14 ~ . ~ , / J
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Fig. 4. Diagrammatic representation of the distribution of terminal degeneration (shown by dots) within the lower bank of the intraparietal sulcus in 3 selected cases with cortical ablations (drawn in black) of portions of the peristriate belt. For case 13, two coronal sections, taken at levels 1 and 2, are also illustrated. Only degeneration within the intraparietal sulcus is shown. Abbreviations as in Fig. 1.
345
14~ lat, ~s.t, CASE 21
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Fig. 5. Diagrammatic representation of the distribution of silver grain within the lower bank of the intraparietal sulcus in 3 cases with injectionsof isotope at differentsites in the inferior parietal lobule. Abbreviations as in Fig. 1. Thus, combining the results of both autoradiographic and silver impregnation studies, it is apparent that, of all the regions surveyed, only a discrete sector on the lateral surface of the preoccipital gyrus projects to the lower bank of the intraparietal sulcus. Furthermore, this projection is directed to the posterior portions of the two divisions of area POa.
Parietal lobe Injections. Eleven animals received injections of radiolabeled amino acid at various sites in the parietal lobe. Only two, with injections in the rostral inferior parietal lobule (area PF), showed silver grain in the lower bank of the intraparietal sulcus (area POa). In both cases 21 and 22, the injection was situated within area PF in the rostral inferior parietal lobule. Although a small amount of isotope extended into area 2 at the rostral tip of the intraparietal sulcus, it did not spread caudally into area PG or into other portions of the sulcus. As shown in Fig. 5, a band of silver grain in the lower bank of the intraparietal sulcus could be traced caudally from the injection site in both of these animals. Label extended over the rostral portion of area POa (Figs. 5 and 8). Although 6 other monkeys (cases 23-28) had injections in the mid- and caudal inferior parietal lobule (area PG), a region immediately adjacent to area POa, silver grain remained within the confines of area PG and did not extend into area POa (Fig.
346 5). One injection in the caudal superior parietal lobule (case 29) and two on the medial surface of the parietal lobe (cases 30 and 31 ) also failed to show label in the lower bank of the intraparietal sulcus.
Ablations. Fourteen monkeys had ablations in various parts of the parietal lobe.
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Fig. 6. Diagrammatic representation of the distribution of terminal degeneration within the lower bank of the intraparietal sulcus in 5 cases with cortical ablations of the postcentral gyrus or inferior parietal lobule. Abbreviations as in Fig. 1.
347
Fig. 7. Summarydiagram to show the two major sources of cortical input to areas POa-i and POa-e in the lower bank of the intraparietal sulcus. Only those with damage in either the rostral inferior parietal lobule (area PF) or in the lower bank of the intraparietal sulcus had terminal degeneration in area POa. Monkey 32 had a large lesion in the rostral one-third of the inferior parietal lobule (area PF). This case displayed a prominent focus of degeneration in the rostral lower bank of the intraparietal sulcus (Fig. 6). Degeneration was disposed in a more or less continuous band situated within the limits of area POa. An essentially identical pattern of terminal degeneration was seen in the intraparietal sulcus of case 33 (Fig. 6). This animal had a somewhat smaller lesion, situated just in front of the rostral tip of the intraparietal sulcus, that destroyed a portion of area 2 in addition to PF-type cortex. Lesions restricted to the post-central gyrus (areas 3, 1 and 2) and not involving area PF (monkeys 34 and 35), however, did not produce terminal degeneration within area POa (Fig. 6). In case 36, the cortical lesion directly involved the lower bank of the intraparietal sulcus (area POa) (Fig. 6). This produced abundant degeneration in the same cortical zone. Three other cases (monkeys 37-39), with mid-inferior parietal lobule lesions, also had terminal degeneration in area POa. Two of these cases (monkeys 37 and 38), however, had ablations which involved part of the adjacent lower bank of the intraparietal sulcus (area POa), and the third (case 39) had a large lesion that extended rostrally to involve a portion of area PF. Smaller lesions, restricted to PG cortex in the posterior two-thirds of the inferior parietal lobule (cases 40~2), failed to produce degeneration in area POa despite the close proximity of the ablations to that sulcal region (Fig. 6). Finally, lesions of the superior parietal lobule and adjacent upper bank of the intraparietal sulcus (cases 43-45) ¢¢ere also without terminal degeneration in the lower bank of the sulcus. Thus, both autoradiographic and silver impregnation studies reveal that area POa receives extrinsic parietal connections exclusively from a sector in the rostral
348 inferior parietal lobule (area PF). This projection is confined to the rostral portion of area POa. DISCUSSION An architectonic study reveals the presence of a distinct cortical zone - area POa - - in the lower bank of the intraparietal sulcus of the rhesus monkey. An analysis of its cortical connections shows two major sources of input: the middle portion of the preoccipital gyrus (area OA) and the rostral inferior parietal lobule (area PF). The preoccipital projection is mainly to the posterior part of area POa, and the parietal projection to the anterior, but both projections overlap each other to some extent (Fig. 7). Although previous studiesS,9, t4 indicated somewhat similar connections, they did not specify the precise sources of afferents or their exact sites of termination. Furthermore, up to the present time, an architectonic study of this region has been lacking. In the present investigation an architectonically defined zone in the intraparietal sulcus is shown to be the consistent target of two major cortical projections. Furthermore, the morphological division of area POa into two elongated sectors is matched by the distribution of terminals in rostrocaudally oriented bands. In the absence of physiological or behavioral studies specifically addressed to this area of the parietal lobe, one can only speculate on the functional significance of area POa. The pattern of its afferent cortical connections may, however, suggest several possibilities. Numerous anatomical, physiological, and behavioral studies indicate sensoryrelated functions for the two cortical regions that project to area POa. The preoccipital gyrus is a recipient of fibers (by way of area OB) from primary visual cortex4,9,16,zk Physiological studies show this region to be responsive to visual stimuli 2z, and lesions of the preoccipital gyrus cause behavioral deficits involving the visual modality 1t. The rostral inferior parietal lobule (area PF of Bonin and Bailey'), the other source of afferents to area POa, receives input from primary somatic sensory cortex of the postcentral gyrus 7,t4,J9 as well as from the second somatic sensory areal4, TM. This region is believed to play a role in somatic sensory-related activity 1°,Ie. In the light of these facts, it is reasonable to propose that the preoccipital gyrus transmits visual information to area POa and that the rostral inferior parietal lobule transmits somatic sensor>' information to that same sulcal area. Furthermore, available evidence allows the nature of these inputs to be more precisely defined. Recent anatomical studies show that the sequence of cortical visual connections is organized in topographical fashion 4,16,21. Thus, the portion of area OA situated in the midpreoccipital gyrus receives input, by way of area OB, from that portion of striate cortex (area OC) sensitive to stimuli in the opposite peripheral visual field 16. The cortical connections of the somatic sensory system are also topographical. Thus, the rostral inferior parietal lobule (area PF) receives fibers from the ventral postcentral gyrus 7,14,19, that portion of primary somatic sensory cortex which relates to the contralateral head and neck 2°. Its other major source of cortical input, the second somatic sensory area ~s, is also largely responsive to stimuli coming from rostral parts
349
Fig. 8. Four photomicrographs to show two sites of intracortical isotope injection and the resulting terminal label within the lower bank of the intraparietal sulcus. A: the injection site in the preoccipital gyrus (area OA) in case 1 (× 8); B: the resulting distribution of terminal label in area POa (x 63); C: the injection site in the rostral inferior parietal lobule (area PF) in case 21 (x 8); D: the resulting distribution of terminal label in area POa ( x 63). of the b o d y 2°. In functional terms, therefore, area P O a appears to receive two highly specific inputs: visual information from the contralateral peripheral visual field, by way of the middle portion o f the preoccipital gyrus, and kinesthetic information from the contralateral head and neck, via area PF. Although an interaction between these two inputs remains to be shown, their convergence in the intraparietal sulcus suggests that area P O a is involved in integrating visual and somatic sensory information and thus relating the position o f the head and neck to the visual environment. In this connection, one other point should be mentioned. The rostral inferior parietal lobule, in addition to its afferent connections with somatic sensory cortex, has also been
350 shown to c o n t a i n cortex responsive to vestibular stimulation 17. Thus, area P O a may also integrate vestibular i n p u t with both visual and somatic sensory i n l b r m a t i o n . In recent years, several studies have investigated the functions o f p o s t e r i o r parietal cortex6,13,1~. A c c o r d i n g to some o f these investigators, the integration o f visual a n d somatic sensory i n f o r m a t i o n is the functional substrate o f certain o f these c o m p l e x behaviors 15. A l t h o u g h these studies have dealt principally with the exposed cortex o f the inferior parietal lobule (area PG), a n d only incidentally with the cortex b u r i e d within the i n t r a p a r i e t a l sulcus, the present study offers a n a t o m i c a l evidence l b r such a m e c h a n i s m in at least a p o r t i o n o f the p o s t e r i o r p a r i e t a l lobe. ACKNOWLEDGEMENTS W e t h a n k Dr. K a t h l e e n S. R o c k l a n d for p r o v i d i n g some o f the a u t o r a d i o g r a p h i c m a t e r i a l a n d Dr. T h o m a s L. K e m p e r for allowing us to examine sections for the architectonic study. W e are also grateful to Miss Valerie Killgren, Miss K a t h l e e n Barry, a n d Ms. Eileen K o t o p o u l i s for p r o v i d i n g technical assistance. This study was s u p p o r t e d by N I H G r a n t N S 09211 a n d V A G r a n t 6901.
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