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The organization of connections between the pulvinar and visual area MT in the macaque monkey
288
Brain Research, 262 (1983) 28~294 Elsevier Biomedical Press
The organization of connections between the pulvinar and visual area MT in the macaque monkey G R E G G P. STANDAGE and LOUIS A. BENEVENTO
Department of A natomy, Universityof lllinois, College of Medicine, P.O. Box 6998, Chicago, IL 60680 (U.S.A.) (Accepted October 5th, 1982)
Key words: visual area MT - inferior pulvinar - lateral pulvinar
Injections of horseradish peroxidase were placed in visual area MT which is located in the superior temporal sulcus of the macaque monkey occipital cortex. Overlapping retrogradely filled cells and anterogradely transported terminal grains were found to be located only within a cresent shaped region which traverses the brachium of the superior colliculus to include the inferior pulvinar and dorsal overlying lateral pulvinar. The connections between MT and the pulvinar crescent are reciprocal and topographically organized, with the lower visual field represented dorsally and the upper visual field represented ventrally. There is an expanded representation of cental vision located caudally within the crescent while peripheral vision is represented rostrally. These findings indicate that any functional properties derived from the visual thalamus must arise from this crescent shaped region of the pulvinar.
The thalamic and cortical subdivisions of the primate brain have been traditionally derived from Nissl and myelin architectonics9.~°.2s. A view which has resulted from these studies is that these cytoarchitecturally defined areas also outline functionally distinct areas in the thalamus and cortex which are interconnected. This view has recently been altered beginning with the discovery that there are several anatomically and functionally distinct thalamic and cortical areas located either within one traditional cytoarchitecturally defined area or found crossing adjacent portions of two of these areas t9-2~.26. Functional subdivisions of visual association (i.e. extrastriate or prestriate) cortex receive afferents from essentially two different sources: (i) from the dorsal lateral geniculate nucleus (DLG) directly or via its connections with a r e a 17s.12.29, or (ii) from the pulvinar 2. Like visual cortex, the pulvinar, which was subdivided on the basis of cytoarchitectonic criteria into inferior, lateral and medial subdivisions 2s, has been found to have connectional and functional subdivisions which do not respect these boundaries 6.~9.2°. With the discovery of functionally specialized areas, i.e. V 1, V2, V3, V4, MT, etc. 26, within clas0006-8993/83/0000 0000/$03.00 © 1983 Elsevier Biomedical Press
sically defined regions of visual cortex (i.e. areas 17, 18 and 19 of Brodmanff °) corresponding generally to areas OC, OB and OA of Bonin and Bailey9, it is not unlikely that the pulvinar is also organized in a similar fashion, i.e. containing specialized subdivisions which project primarily to specific functional subdivisions of visual cortex. We report here the discovery of one such region in the macaque monkey pulvinar. The region extends through a major fiber system (the brachium of the superior colliculus) and two classically defined subdivisions, i.e. the inferior pulvinar (PI) and the lateral pulvinar (PL). This region is topographically organized and projects to visual area MT in the superior temporal sulcus (STS). MT is also known as the motion sensitive a r e a 27'3°. Five Macaca fascicularis, weighing 2.5 4 kg, were anesthetized with pentobarbital sodium (32 mg/kg) and received two or three 0.0150.025/zl injections of 30% horseradish peroxidase (HRP, Sigma VI or Worthington) or 5% wheat germ conjugated horseradish peroxidase (WGHRP) in visual area MT (Fig. 1C). MT was located by single unit recording and aspiration of the
289 overlying anterior bank of STS about its junction with the lateral sulcus (Benevento and Standage7). Histological verification of the location of the injection sites was made with myelin stains ~3 as MT has a unique fiber pattern which distinguishes it from adjacent cortical areas (Fig. 1A) 714"25"2v. Following 42 h survival times, the animals were deeply anesthetized and perfused transcardially with 2.5% glutaraldehyde and 1.0% paraformaldehyde in 0.1 M phosphate buffer, followed by a 30% sugar in 0.1 M phosphate buffer rinse at 4 °C. The brains were blocked in the stereotaxic transverse plane (except one which was cut in the horizontal plane) and adjacent 40 t~m frozen sections were reacted according to the tetramethylbenzidene and benzidene dihydrochloride methods ~s. Good myelin staining of gluteraldehyde/paraformaldehyde-fixed and TMB-reacted tissue was difficult to achieve, so adjacent unreacted sections through the pulvinat and STS were stored in 10% formalin for two weeks and then stained with the Gallyas method (Fig. 1A) 13. Sections were examined and plotted for anterogradely transported label (terminal grains), retrogradely labeled cells and myeloarchitecture using a Zeiss microscope coupled to an XY plotter. By plotting the myeloarchitecture of the superior temporal sulcus above and below the junction of this sulcus with the lateral sulcus, we were able to confirm that our injection sites were within MT or, as in the case of one injection (injection 1, Fig. I C), also involved cortex posterior to MT. Importantly, we were able to plot the location and laminar distribution of HRP-filled cells in the striate cortex. Since it is only area MT which receives an input from striate layers IVb and VI, we were able to further confirm that our injections were within MT 1727. Fig. 1 illustrates the location of injection sites in MT and the resulting location of HRP-filled cells and overlapping terminal grains in the pulvinar. The region which contained labeled cells and terminal grains in each case was a heavily myelinated crescent shaped region (as seen in transverse sections) which extended, ventral to dorsal, from the ventral border of the inferior pulvinar through the brachium of the superior colliculus,
into the overlying lateral pulvinar. From rostral to caudal, the region extends from the caudal pole of the DLG where it involved the dorsomedial inferior pulvinar to the caudal lateral pulvinar 4,19(Fig. I D). There was always the presence of strong, coextensive retrograde and anterograde labeling in this restricted crescent shaped region of the pulvinar indicating reciprocal connections with MT (Figs. 2 and 3). From case to case, the location of labeled cells and terminal grains varied within this crescent shaped region depending upon the location of the injection site within MT. Injection 1 (Figs. 1C and 2) involved the posterior wall of STS and included the dorso-lateral portion of MT. HRPfilled cells were located in the anterior one-half of the crescent involving the medio-dorsal region of the inferior pulvinar and overlying lateral pulvinar (Fig. 1D and 2B). Injection 2 was located ventral to injection 1 (Fig. 1C) and involved the junction of the wall and floor of STS. This injection was contained entirely within MT. HRP labeled cells and terminal grains were located more caudally in the crescent when compared with injection 1, but the cells remained dorsally within the crescent (Fig. 1D). Injection 4 also involved the j unction of the wall and floor of STS (Fig. 1C), it too involved only MT. Injection 4 while overlapping with injection 3 was placed more ventrally within MT (Fig. 1C). Terminal grains and HRP-filled cells resulting from injection 4 were located caudally within the crescent but the terminal field was located more ventrally within the crescent than for injection 2 (Figs. 1D and 3). Terminal fields and HRP-labeled cells overlapped in the crescent for injections 2 and 4 (Fig. 3C, E). Injection 7 was restricted to the floor of STS within MT (Fig. 1C). HRP-filled cells were located only in the inferior pulvinar in the ventro-anterior portion of the crescent (Fig. 1D). Relating the locations of our injection sites to the known retinotopic organization of MT 14.27 indicates that central vision is represented caudally within the crescent while peripheral vision is represented rostrally, with the lower visual quadrant represented dorsally within the crescent and the upper visual quadrant represent-
290
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Fig. 2. Light-field photomicrographs which illustrate the extent of injection 1 (Fig. IC) and the resulting HRP-filled cells in the inferior pulvinar. A: a low power photomicrograph (5.0 x ) of a transverse section through the superior temporal sulcus showing an HRP injection involving the entire posterior bank of STS including MT (level C, Fig. IC); arrows indicate anterior and posterior border of the injection site. B: the location of HRP-filled cells in the rostro-medial inferior pulvinar (12.5 x ) and corresponds to level 420 in Fig. 1D. The box labeled C is shown at higher power (50.0 x ) in C. The cluster of HRP-filted cells in C labeled D are shown at higher power in D ( 125.0 x ). The two cells in D labeled E are shown in E at high magnification ( 1250 x ) and illustrate the characteristic appearance of HRP-filled cells.
ed ventrally (Fig. I D). The data also indicate that central visual space is represented in the caudal one-half to two-thirds of the pulvinar crescent. Thus, there is an expansion of the representation of central vision. These findings agree with previous work describing the retino-
topic organization of the macaque inferior pulvinar and adjacent lateral pulvinar 1,3-4.2°. The region of the pulvinar which shows retrograde labeling following injections of MT has its own distinct myeloarchitecture (Fig. 3B, D). Within this crescent shaped strip, a dense net-
Fig. 1. Examples of HRP injections into area MT and the resulting location of terminal grains and HRP-filled cells within the pulvinar. A: transverse myelin-stained section (5.0 x ) through visual area MT; arrowheads indicate the anterior and posterior borders of MT as determined by the dense network of obliquely running fibers which sets MT off from surrounding cortex. Panel A corresponds to level E in C. B: the transverse levels through the superior temporal sulcus from which the summary diagram in panel C was reconstructed. C: an unfolding of the superior temporal sulcus in order to illustrate the location of our injections into MT (stippled). Each injection illustrated is numbered. The locations of terminal grains and HRP-filled cells for injections 1, 2, 4 and 7 are illustrated in D. D: the rostral-caudal and dorsal-ventral extent of the crescent region which projects to MT. Note: the region extends from the caudal lateral pulvinar (upper left) to the rostral inferior pulvinar and overlying lateral pulvinar rostralIv. Abbreviations: B. brachium of the superior colliculus: IOS. inferior occipital sulcus: IPS, inferior parietal sulcus: L, lunate sulcus: LS, lateral sulcus, MD, mediodorsal nucleus: MG, medial geniculate: PI, inferior pulvinar: PL, lateral pulvinar; PM, medial pulvinar; STS, superior temporal sulcus.
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Fig. 3. Light-field (A, B and D) and dark-field photomicrographs (C and E) which illustrate the results of injection 4 (level D, Fig. I C) and the resulting location of overlapping terminal grains and H RP-filled cells in the heavily myelinated crescent region of the pulvinar. A: corresponds to level D (Fig. 1C). Note that the anterior bank of STS has been removed by aspiration allowing visual inspection and access to the floor and posterior wall of STS (5.0 x ). B and C and D and E: adjacent sections stained for myelin (B and D, 12.5 x ) or reacted for HRP reaction product (C and E, 50.0 x ), illustrating the location of overlapping terminal grains and HRP-filled cells within the heavily myelinated region of the caudal lateral pulvinar (B and C) (level 340, Fig. I D) and inferior pulvinar and overlying lateral pulvinar (D and E) (level 380, Fig. ID). The boxes in B and D enclose the heavily myelinated crescent and location of HRP reaction product in the photomicrographs.
work of obliquely running fibers can be seen in sections stained for myelin, with myelination being more prominent in the inferior pulvinar. This fiber network sets the crescent shaped region off from the surrounding portions of the inferior pulvinar and lateral pulvinar. Finally, the results from extensive HRP and W G - H R P studies which involved injections into every specialized functional region of occipital cortex23.24 demonstrate a lack of any significant efferents from the crescent to other areas of visual cortex. Thus, visual area MT is the crescent's primary cortical projection target. These results provide anatomical evidence for the existence of a unique subdivision of the macaque monkey pulvinar whose primary projection target is a functionally specialized zone of extrastriate cortex located in the STS. This pul-
vinar region cannot be assigned to either the inferior pulvinar or lateral pulvinar as it is contained within both of these subdivisions. The fact that the region possesses a unique myelinated fiber pattern is interesting since visual area MT, its cortical projection target, also possesses a unique myelin pattern which distinguishes it from surrounding areas. The myeloarchitectonic organization of both MT and the pulvinar crescent are similar in that each is described as containing a dense network of obliquely running fibers. The strong, monogamous reciprocity of connections and similar myeloarchitectonics between the two regions could mean that both regions share in their functional properties. Indeed recent anatomical and physiological evidence6,~L2~ suggests a segregation of functional properties within the macaque pulvinar. We
293 have not recorded sufficiently from this region to make any definite statements, but have found motion sensitive and direction sensitive units in the region of the crescent. It is significant, however, that MT is one of the few occipital extrastriate visual areas which does not receive any input from the D L G 5.7,22, so that any functional properties derived from the visual thalamus must arise from the crescent shaped region traversing the inferior pulvinar and lateral pulvinar. These results also indicate that the macaque inferior pulvinar is not a homogenous structure as previously thought, but rather contains several subdivisions. This interpretation is consistent with results in the New World owl monkey ~5.~6in which PI was shown to receive segregated inputs from the superior colliculus and contain at least 3 separate subdivisions with the one which does not receive collicular input projecting to area MT. In the macaque it has also been shown that there is a similar segregation of superior colliculus projections within PF °. We feel that we must be describing the analagous system for the macaque monkey. Finally, the crescent region which projects to MT in the macaque extends far caudally into PL-gamma as well as dorsally into PL-beta 4-~9-23 so that a major portion of the region is contained within the lateral pulvinar in addition to the in-
1 Bender, D. B., Retinotopic organization of the macaque pulvinar, J. Neurophysiol., 46 ( 1981 ) 672-693. 2 Benevento, L. A. and Rezak, M., The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Maeaca mulatta): an autoradiographic study, Brain Research, 108 (1976) 1-24. 3 Benevento, L. A. and Davis, B., Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: An autoradiographic study, Exp. Brain Res., 30 (1977) 405-424. 4 Benevento, L. A. and Miller, J., Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey, J. Neurosci, 1 (1981) 1268 1278. 5 Benevento, L. A. and Yoshida, K., The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey, J. comp. Neurol., 203 (1981)455 474. 6 Benevento, L. A. and Standage, G. P., A comparison of the projections of the dorsal lateral geniculate nucleus and pulvinar complex to extrastriate visual association
ferior pulvinar. In transverse sections, the crescent region's lateral border and long axis (dorsoventrally oriented) parallels the lateral border of the lateral pulvinar (Fig. 1D). It is interesting that visual area MT has sustaining reciprocal connections with a region of the pulvinar which not only includes within its borders two classically defined subdivisions (i.e. the inferior pulvinar and lateral pulvinar), but also crosses through the brachium of the superior colliculus, a major fiber system which divides the macaque pulvinar into dorsal and ventral sections. Such findings indicate that classically defined subdivisions such as the inferior pulvinar and lateral pulvinar might be somewhat specious and useful only for orientation purposes. In conclusion, these results and our previous findings on brainstem input to the pulvinar lead us to believe that a different organizational scheme, based on connections with functional subdivisions in the cortex24 and brainstem 8,2~ is superimposed upon classically defined regions of the primate pulvinar. This work was supported by N.I.H. Grant EY 2940 and Fellowship NS 7029. We are grateful to Ms. Pamela Brunner for her technical assistance and Dr. Russell Carey of the Barrow Neurological Institute for providing the wheat germ conjugated horseradish peroxidase.
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cortex in the macaque monkey, Anat. Rec., 199 (1981) 25A. Benevento, L. A. and Standage, G. P., Demonstration of lack of dorsal lateral geniculate nucleus input ot extrastriate areas MT and visual 2 in the macaque monkey, Brain Research, in press. Benevento, L. A. and Standage, G. P., The organization of projections of the retinorecipient and non-retinorecipient subdivisions of the pretectal complex and superior colliculus to the lateral pulvinar and medial pulvinar nuclei in macaque monkeys, in preparation. Bonin, G. Von and Bailey, P., The Neocortex of Macaca mulatta, University of Illinois Press, Urbana, IL, 1947. Brodmann, K., Vergleich einer Lokalisationslehre der Grosshirnrinde in ihren Principien dargestellt auf Grund des Zellenbaues, Barth, Leipzig, 1909. Felstein, G., Burman, D., Yoshida, K. and Benevento, L. A., Visual properties of single neurons in the macaque monkey pulvinar, Soc. Neurosci. A bstr., 7 ( 1981 ) 759. Fries, W., The projection from the lateral geniculate nu-
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cleus to the prestriate cortex of the macaque monkey, Proc. roy. Soc. B, 213 (1981) 73-80. Gallyas, E., Silver staining of myelin by means of physical development, Neurol. Res., 1 (1979) 203-209. Gattass, R. and Gross, C. G., Visual topography ofstriate projection zone (MT) in posterior superior temporal sulcus of the macaque, J. Neurophysiol., 46 (1981) 621-638. Lin, C.-S. and Kaas, J. H., The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex, J. comp. Neurol., 187 (1979) 655-678. Lin, C.-S. and Kaas, J. H., Projections from the medial nucleus of the inferior pulvinar complex to the middle temporal area of the visual cortex, Neuroscience, 5 (1980) 2219-2228. Lund, J. S., Lund, R. D., Hendrickson, A. B., Bunt, A. H. and Fuchs, A. F., The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase, J. comp. Neurol., 164 (1975) 287-304. Mesulam, M. M., The blue reaction product in horseradish peroxidase neurochemistry: incubation parameters and visibility, J. Histochem. Cytochem., 24 (1976) 1273 1280. Rezak, M. and Benevento, L. A., A redefinition ofpulvinar subdivisions in the macaque monkey: evidence for three distinct subregions within classically defined lateral pulvinar, Soc. Neurosci. Abstr., 3 (1977) 574. Rezak, M. and Benevento, L. A., A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey, Brain Research, 167 (1979) 19 40. Standage, G. P. and Benevento, L. A., Multiple midbrain input zones within the lateral pulvinar of macaque mon-
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keys with special reference to certain of their cortical targets, Soc. Neurosci. Abstr., 7 (1981) 830. Standage, G. P. and Benevento, L. A., Lack of dorsal lateral geniculate input to extrastriate cortical areas MT and dorsal visual 2 in the macaque monkey, Soc. Neurosci. Abstr., 8 (1982) 680. Standage, G. P. and Benevento, L. A., Relationship of the subdivisions of the pulvinar complex to the various visual areas within the occipital lobe of the macaque monkey, Soc. Neurosci. A bstr., 6 (1980) 481. Standage, G. P. and Benevento, L. A., Parallel thalamic fields in the pulvinar complex of macaque monkeys identified by their connections with functionally specialized regions of occipital and infero-temporal cortex, in preparation. Ungerleider, L. and Mishkin, M., The striate projection zone in the superior temporal sulcus of Macaca mulatta: location and topographic organization, J. comp. Neurol., 188 (1979) 347-366. Van Essen, D. C. and Zeki, S. M., The topographic organization of rhesus monkey prestriate cortex, J. Physiol., (Lond.), 277 (1978) 198 226. Van Essen, D. C., Maunsell, J. H. R. and Bixby, J. L., The middle temporal visual area in the macaque: myeloarchictecture, connections, functional properties and topographic organization, J. comp. Neurol., 199 (1981) 293326. Walker, A. E., The Primate Thalamus, Univ. of Chicago Press, Chicago, IL, 1938. Yukie, M. and Iwai, E., Direct projection from dorsal lateral geniculate nucleus to prestriate cortex in macaque monkeys, J. comp. Neurol., 201 ( 1981 ) 81-97. Zeki, S. M., Functional specialization in the visual cortex of the rhesus monkey, Nature (Lond), 274 (1980) 239248.
Brain Research, 262 (1983) 28~294 Elsevier Biomedical Press
The organization of connections between the pulvinar and visual area MT in the macaque monkey G R E G G P. STANDAGE and LOUIS A. BENEVENTO
Department of A natomy, Universityof lllinois, College of Medicine, P.O. Box 6998, Chicago, IL 60680 (U.S.A.) (Accepted October 5th, 1982)
Key words: visual area MT - inferior pulvinar - lateral pulvinar
Injections of horseradish peroxidase were placed in visual area MT which is located in the superior temporal sulcus of the macaque monkey occipital cortex. Overlapping retrogradely filled cells and anterogradely transported terminal grains were found to be located only within a cresent shaped region which traverses the brachium of the superior colliculus to include the inferior pulvinar and dorsal overlying lateral pulvinar. The connections between MT and the pulvinar crescent are reciprocal and topographically organized, with the lower visual field represented dorsally and the upper visual field represented ventrally. There is an expanded representation of cental vision located caudally within the crescent while peripheral vision is represented rostrally. These findings indicate that any functional properties derived from the visual thalamus must arise from this crescent shaped region of the pulvinar.
The thalamic and cortical subdivisions of the primate brain have been traditionally derived from Nissl and myelin architectonics9.~°.2s. A view which has resulted from these studies is that these cytoarchitecturally defined areas also outline functionally distinct areas in the thalamus and cortex which are interconnected. This view has recently been altered beginning with the discovery that there are several anatomically and functionally distinct thalamic and cortical areas located either within one traditional cytoarchitecturally defined area or found crossing adjacent portions of two of these areas t9-2~.26. Functional subdivisions of visual association (i.e. extrastriate or prestriate) cortex receive afferents from essentially two different sources: (i) from the dorsal lateral geniculate nucleus (DLG) directly or via its connections with a r e a 17s.12.29, or (ii) from the pulvinar 2. Like visual cortex, the pulvinar, which was subdivided on the basis of cytoarchitectonic criteria into inferior, lateral and medial subdivisions 2s, has been found to have connectional and functional subdivisions which do not respect these boundaries 6.~9.2°. With the discovery of functionally specialized areas, i.e. V 1, V2, V3, V4, MT, etc. 26, within clas0006-8993/83/0000 0000/$03.00 © 1983 Elsevier Biomedical Press
sically defined regions of visual cortex (i.e. areas 17, 18 and 19 of Brodmanff °) corresponding generally to areas OC, OB and OA of Bonin and Bailey9, it is not unlikely that the pulvinar is also organized in a similar fashion, i.e. containing specialized subdivisions which project primarily to specific functional subdivisions of visual cortex. We report here the discovery of one such region in the macaque monkey pulvinar. The region extends through a major fiber system (the brachium of the superior colliculus) and two classically defined subdivisions, i.e. the inferior pulvinar (PI) and the lateral pulvinar (PL). This region is topographically organized and projects to visual area MT in the superior temporal sulcus (STS). MT is also known as the motion sensitive a r e a 27'3°. Five Macaca fascicularis, weighing 2.5 4 kg, were anesthetized with pentobarbital sodium (32 mg/kg) and received two or three 0.0150.025/zl injections of 30% horseradish peroxidase (HRP, Sigma VI or Worthington) or 5% wheat germ conjugated horseradish peroxidase (WGHRP) in visual area MT (Fig. 1C). MT was located by single unit recording and aspiration of the
289 overlying anterior bank of STS about its junction with the lateral sulcus (Benevento and Standage7). Histological verification of the location of the injection sites was made with myelin stains ~3 as MT has a unique fiber pattern which distinguishes it from adjacent cortical areas (Fig. 1A) 714"25"2v. Following 42 h survival times, the animals were deeply anesthetized and perfused transcardially with 2.5% glutaraldehyde and 1.0% paraformaldehyde in 0.1 M phosphate buffer, followed by a 30% sugar in 0.1 M phosphate buffer rinse at 4 °C. The brains were blocked in the stereotaxic transverse plane (except one which was cut in the horizontal plane) and adjacent 40 t~m frozen sections were reacted according to the tetramethylbenzidene and benzidene dihydrochloride methods ~s. Good myelin staining of gluteraldehyde/paraformaldehyde-fixed and TMB-reacted tissue was difficult to achieve, so adjacent unreacted sections through the pulvinat and STS were stored in 10% formalin for two weeks and then stained with the Gallyas method (Fig. 1A) 13. Sections were examined and plotted for anterogradely transported label (terminal grains), retrogradely labeled cells and myeloarchitecture using a Zeiss microscope coupled to an XY plotter. By plotting the myeloarchitecture of the superior temporal sulcus above and below the junction of this sulcus with the lateral sulcus, we were able to confirm that our injection sites were within MT or, as in the case of one injection (injection 1, Fig. I C), also involved cortex posterior to MT. Importantly, we were able to plot the location and laminar distribution of HRP-filled cells in the striate cortex. Since it is only area MT which receives an input from striate layers IVb and VI, we were able to further confirm that our injections were within MT 1727. Fig. 1 illustrates the location of injection sites in MT and the resulting location of HRP-filled cells and overlapping terminal grains in the pulvinar. The region which contained labeled cells and terminal grains in each case was a heavily myelinated crescent shaped region (as seen in transverse sections) which extended, ventral to dorsal, from the ventral border of the inferior pulvinar through the brachium of the superior colliculus,
into the overlying lateral pulvinar. From rostral to caudal, the region extends from the caudal pole of the DLG where it involved the dorsomedial inferior pulvinar to the caudal lateral pulvinar 4,19(Fig. I D). There was always the presence of strong, coextensive retrograde and anterograde labeling in this restricted crescent shaped region of the pulvinar indicating reciprocal connections with MT (Figs. 2 and 3). From case to case, the location of labeled cells and terminal grains varied within this crescent shaped region depending upon the location of the injection site within MT. Injection 1 (Figs. 1C and 2) involved the posterior wall of STS and included the dorso-lateral portion of MT. HRPfilled cells were located in the anterior one-half of the crescent involving the medio-dorsal region of the inferior pulvinar and overlying lateral pulvinar (Fig. 1D and 2B). Injection 2 was located ventral to injection 1 (Fig. 1C) and involved the junction of the wall and floor of STS. This injection was contained entirely within MT. HRP labeled cells and terminal grains were located more caudally in the crescent when compared with injection 1, but the cells remained dorsally within the crescent (Fig. 1D). Injection 4 also involved the j unction of the wall and floor of STS (Fig. 1C), it too involved only MT. Injection 4 while overlapping with injection 3 was placed more ventrally within MT (Fig. 1C). Terminal grains and HRP-filled cells resulting from injection 4 were located caudally within the crescent but the terminal field was located more ventrally within the crescent than for injection 2 (Figs. 1D and 3). Terminal fields and HRP-labeled cells overlapped in the crescent for injections 2 and 4 (Fig. 3C, E). Injection 7 was restricted to the floor of STS within MT (Fig. 1C). HRP-filled cells were located only in the inferior pulvinar in the ventro-anterior portion of the crescent (Fig. 1D). Relating the locations of our injection sites to the known retinotopic organization of MT 14.27 indicates that central vision is represented caudally within the crescent while peripheral vision is represented rostrally, with the lower visual quadrant represented dorsally within the crescent and the upper visual quadrant represent-
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Fig. 2. Light-field photomicrographs which illustrate the extent of injection 1 (Fig. IC) and the resulting HRP-filled cells in the inferior pulvinar. A: a low power photomicrograph (5.0 x ) of a transverse section through the superior temporal sulcus showing an HRP injection involving the entire posterior bank of STS including MT (level C, Fig. IC); arrows indicate anterior and posterior border of the injection site. B: the location of HRP-filled cells in the rostro-medial inferior pulvinar (12.5 x ) and corresponds to level 420 in Fig. 1D. The box labeled C is shown at higher power (50.0 x ) in C. The cluster of HRP-filted cells in C labeled D are shown at higher power in D ( 125.0 x ). The two cells in D labeled E are shown in E at high magnification ( 1250 x ) and illustrate the characteristic appearance of HRP-filled cells.
ed ventrally (Fig. I D). The data also indicate that central visual space is represented in the caudal one-half to two-thirds of the pulvinar crescent. Thus, there is an expansion of the representation of central vision. These findings agree with previous work describing the retino-
topic organization of the macaque inferior pulvinar and adjacent lateral pulvinar 1,3-4.2°. The region of the pulvinar which shows retrograde labeling following injections of MT has its own distinct myeloarchitecture (Fig. 3B, D). Within this crescent shaped strip, a dense net-
Fig. 1. Examples of HRP injections into area MT and the resulting location of terminal grains and HRP-filled cells within the pulvinar. A: transverse myelin-stained section (5.0 x ) through visual area MT; arrowheads indicate the anterior and posterior borders of MT as determined by the dense network of obliquely running fibers which sets MT off from surrounding cortex. Panel A corresponds to level E in C. B: the transverse levels through the superior temporal sulcus from which the summary diagram in panel C was reconstructed. C: an unfolding of the superior temporal sulcus in order to illustrate the location of our injections into MT (stippled). Each injection illustrated is numbered. The locations of terminal grains and HRP-filled cells for injections 1, 2, 4 and 7 are illustrated in D. D: the rostral-caudal and dorsal-ventral extent of the crescent region which projects to MT. Note: the region extends from the caudal lateral pulvinar (upper left) to the rostral inferior pulvinar and overlying lateral pulvinar rostralIv. Abbreviations: B. brachium of the superior colliculus: IOS. inferior occipital sulcus: IPS, inferior parietal sulcus: L, lunate sulcus: LS, lateral sulcus, MD, mediodorsal nucleus: MG, medial geniculate: PI, inferior pulvinar: PL, lateral pulvinar; PM, medial pulvinar; STS, superior temporal sulcus.
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Fig. 3. Light-field (A, B and D) and dark-field photomicrographs (C and E) which illustrate the results of injection 4 (level D, Fig. I C) and the resulting location of overlapping terminal grains and H RP-filled cells in the heavily myelinated crescent region of the pulvinar. A: corresponds to level D (Fig. 1C). Note that the anterior bank of STS has been removed by aspiration allowing visual inspection and access to the floor and posterior wall of STS (5.0 x ). B and C and D and E: adjacent sections stained for myelin (B and D, 12.5 x ) or reacted for HRP reaction product (C and E, 50.0 x ), illustrating the location of overlapping terminal grains and HRP-filled cells within the heavily myelinated region of the caudal lateral pulvinar (B and C) (level 340, Fig. I D) and inferior pulvinar and overlying lateral pulvinar (D and E) (level 380, Fig. ID). The boxes in B and D enclose the heavily myelinated crescent and location of HRP reaction product in the photomicrographs.
work of obliquely running fibers can be seen in sections stained for myelin, with myelination being more prominent in the inferior pulvinar. This fiber network sets the crescent shaped region off from the surrounding portions of the inferior pulvinar and lateral pulvinar. Finally, the results from extensive HRP and W G - H R P studies which involved injections into every specialized functional region of occipital cortex23.24 demonstrate a lack of any significant efferents from the crescent to other areas of visual cortex. Thus, visual area MT is the crescent's primary cortical projection target. These results provide anatomical evidence for the existence of a unique subdivision of the macaque monkey pulvinar whose primary projection target is a functionally specialized zone of extrastriate cortex located in the STS. This pul-
vinar region cannot be assigned to either the inferior pulvinar or lateral pulvinar as it is contained within both of these subdivisions. The fact that the region possesses a unique myelinated fiber pattern is interesting since visual area MT, its cortical projection target, also possesses a unique myelin pattern which distinguishes it from surrounding areas. The myeloarchitectonic organization of both MT and the pulvinar crescent are similar in that each is described as containing a dense network of obliquely running fibers. The strong, monogamous reciprocity of connections and similar myeloarchitectonics between the two regions could mean that both regions share in their functional properties. Indeed recent anatomical and physiological evidence6,~L2~ suggests a segregation of functional properties within the macaque pulvinar. We
293 have not recorded sufficiently from this region to make any definite statements, but have found motion sensitive and direction sensitive units in the region of the crescent. It is significant, however, that MT is one of the few occipital extrastriate visual areas which does not receive any input from the D L G 5.7,22, so that any functional properties derived from the visual thalamus must arise from the crescent shaped region traversing the inferior pulvinar and lateral pulvinar. These results also indicate that the macaque inferior pulvinar is not a homogenous structure as previously thought, but rather contains several subdivisions. This interpretation is consistent with results in the New World owl monkey ~5.~6in which PI was shown to receive segregated inputs from the superior colliculus and contain at least 3 separate subdivisions with the one which does not receive collicular input projecting to area MT. In the macaque it has also been shown that there is a similar segregation of superior colliculus projections within PF °. We feel that we must be describing the analagous system for the macaque monkey. Finally, the crescent region which projects to MT in the macaque extends far caudally into PL-gamma as well as dorsally into PL-beta 4-~9-23 so that a major portion of the region is contained within the lateral pulvinar in addition to the in-
1 Bender, D. B., Retinotopic organization of the macaque pulvinar, J. Neurophysiol., 46 ( 1981 ) 672-693. 2 Benevento, L. A. and Rezak, M., The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Maeaca mulatta): an autoradiographic study, Brain Research, 108 (1976) 1-24. 3 Benevento, L. A. and Davis, B., Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: An autoradiographic study, Exp. Brain Res., 30 (1977) 405-424. 4 Benevento, L. A. and Miller, J., Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey, J. Neurosci, 1 (1981) 1268 1278. 5 Benevento, L. A. and Yoshida, K., The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey, J. comp. Neurol., 203 (1981)455 474. 6 Benevento, L. A. and Standage, G. P., A comparison of the projections of the dorsal lateral geniculate nucleus and pulvinar complex to extrastriate visual association
ferior pulvinar. In transverse sections, the crescent region's lateral border and long axis (dorsoventrally oriented) parallels the lateral border of the lateral pulvinar (Fig. 1D). It is interesting that visual area MT has sustaining reciprocal connections with a region of the pulvinar which not only includes within its borders two classically defined subdivisions (i.e. the inferior pulvinar and lateral pulvinar), but also crosses through the brachium of the superior colliculus, a major fiber system which divides the macaque pulvinar into dorsal and ventral sections. Such findings indicate that classically defined subdivisions such as the inferior pulvinar and lateral pulvinar might be somewhat specious and useful only for orientation purposes. In conclusion, these results and our previous findings on brainstem input to the pulvinar lead us to believe that a different organizational scheme, based on connections with functional subdivisions in the cortex24 and brainstem 8,2~ is superimposed upon classically defined regions of the primate pulvinar. This work was supported by N.I.H. Grant EY 2940 and Fellowship NS 7029. We are grateful to Ms. Pamela Brunner for her technical assistance and Dr. Russell Carey of the Barrow Neurological Institute for providing the wheat germ conjugated horseradish peroxidase.
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