Visual Cortex in Primates

John Allman and EveLynn McGuinness Division ofBiology, California insntUle of Technology, Pasadena. California 9JJ25

EVOLUOON OF THE VISUAL SYSTEM the contralateral half of the visual field; 8) the IN PRIMATES expansion and functional differentation of primary visual cortex; 9) the expansion of extrastriate cor­ Fossil remains of the earliest primates that bear tical visual areas and the probable elaboration of a close resemblance to living primates have been new visual areas: 10) the shift of the foramen recovered from early Eocene deposits 55 million magnum from a posterior to a more ventral posi­ years old [Simons. 19721. The sb.-ull and cramal tion in the sb.-ull: II) prehensile hands: 12) eye­ endocast of one of these early primates. Tetomus hand coordination: 13) bmocular convergence and homunculus. are illustrated in Figure l. Tetonius accommodative focusing; 14) tine-grained stereop­ possessed large bony orbits that completely encir­ SIS [see reviews. Allman. 1977. 1982). Since most cled its eyes and a cranIUm containing a large brain of these features are characteristic of all living compared with Its similarly sized contemporaries. primates. it is likely that they were present in the The large size and position of the orbits in Tetonius most recent common ancestors of the living closely resemble living nocturnal prosimians (see primates. Fig. 2). The cranial endocasts of Tetonius and Two theories have been advanced to explain this other Eocene primates reveal that their brains pos­ basic set of primate adaptations. In the first. Mar­ sessed a conspicuous enlargement of the neocortex tin [1979) has suggested that the early primates. of the occipital and temporal lobes [Radinsky, like the smaller living prosimians they closely re­ 1967. 1970: Gurche. 1982). The studies in living semble and the small arboreal marsupials of Aus­ primates to be reviewed in this chapter indicate tralia and South America. adapted to a "fine­ that all of the occipital lobe and much of the branch niche": the prehensile hands and feet found temporal lobe are devoted to the processing of in these animals developed to grasp the fine ter­ visual information. minal branches of trees. Most arboreal mammals, The large bony orbits and expanded occipital such as squirrels. run on the trunk and larger and temporal lobes in the early primates probably branches but are unable to grasp the fmer branches. were parts of an adaptive complex that included 1) The second theory is based on the observation tbat, frontally directed eyes; 2) an area of high acuity in outside of the order Primates. animals with large. the central retina; 3) a large-field of binocular frontally directed eyes (owls and felids) are noc­ overlap; 4) a large ipsilateral projection from the turnal. visually directed predators, which led Cart­ retina to the lateral geniculate nucleus and the optic mill [1972) to propose that visually directed tectum: 5) the expansion of the representation of predation was the ecological specialization linked the central visual field in thalamic. tectal. and to this set of developments in the early primates. cortical visual structures: 6) a laminated lateral Cartmill's visual predation hypothesis is supported geniculate nucleus in which the inputs from the by the fact that the tarsier, the living primate that two eyes were segregated in several sets of layers: most closely resembles the early primates of the 7) a representation in the optic tectum restricted to Eocene, is exclusively a predator (see Fig. 3).

Comparative Primare Biology. Volume 4: Neurosciences. pages 279-326 © 1988 Alan R. Liss, Inc. • ~ 1 j

280 Allman and McGuinness

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Fig. 1. Left: dorsal view of the skull of Teronius homunculus. A.M.N.H.No .+\94. Right: dorsal view of Radinsky's cral1lai endocast of Tewnius. From Radinsky [19671. with permission.

Fig. 2. Left: dorsal view of the sku!! of Galago The Vs demarcate the anterior border of visual cor­ senegalensis. Right: dorsal view of the brain of Gal­ tex. OB. olfactory bulbs. From Allman. [1977], with ago senegalensis. The visual cortex corresponds to permission. approximately the posterior half of the neocortex. Visual Cortex in Primates 281

Fig. 3. Tarsier seizing a lizard. The tarsier is exclusively a predator: it eats no fruit or vegetable maner. Of the livmg primates. [he tarsier most closely resembles the early primates living in (he Eocene. Photo by Dr. Johannes Tigges. From Allman [19771. with permission.

Both hypotheses may be correct. It is probable that Thus natural selection would have especially fa­ the early primates did invade the "fine-branch vored the development of visuo-spatial memory in niche" where they gained access to a rich array of frugivorous primates. insect and small vertebrate prey. Another. even more significant behavioral spe­ The early primates probably were small. noctur­ cialization. is the development of complex systems nal predators living in the fine branches: some of social organization in many primate species. primates have retained this mode of life. but most The neural substrate for the mediation of social have become larger diurnal folivores or frugi­ communication is bound to be an important focus vores. The development of the capacity for color of evolutionary change in the brains of primates. discrimination is probably linked to a selective The order Primates is divided into the strepsirhines adaptation for identifying ripe. and therefore di­ (Iorises. galagos. lemurs), which tend to have rel­ gestible. fruit [Polyak. 19571. Frugivorous diet is atively simple forms of social organization. and correlated positively with brain size [Clutton-Brock the haplorhines (tarsiers. monkeys. apes. humans) and Harvey, 1980J and the amount of neocortex in which social organization tends to be more com­ relative to body size in primates [Stephan and plex. In strepsirhines. as in most mammals. the Andy, 1970). This association between frugivo­ rhinarium (the space between the upper lip and the rous diet and enlarged brain and neocortex may be nostrils) is a furless. moist mucosal tissue that is related to the special demands imposed because a tightly bound to the underlying maxillary bone and fruit eater's food supply is not constant since dif­ is bisected along the midline by a deep cleft (see ferent plants bear fruit at different times and at Fig. 4). Since strepsirhines share this type of rhi­ different locations in the complex matrix of the narium with most other mammals. it is very likely tropical forest. An animal that is guided by the to have been the primitive condition in primates. accurate memory of the locations of fruit-bearing By contrast. haplorhines possess a furry rhinarium trees can more effectively exploit the available and a mobile upper lip that is more capable of fruit resources than would otherwise be possible. participating in facial expression. Strepsirhines. 282 Allman and McGuinness

Fig. 4. Left: a strepsirhine, Gaiago senegalensis. Photo by 1. Allman. Right: a haplor­ hine, Tarsius syrichla. Photo by R. Garrison. Reproduced from Allman, [1977], with permission.

like most pnmitive mammals. have scent glands for the visual mediauon of social signals and mem­ and scent-marking behaviors that playa very im­ ory of past social interactions. portant role in their social ..:ommunicmion. and while hapJorhines use olfactory ..:ues to some ex­ GENICULOSTRIATE PROJECTIONS: tent. they rely much more heavily on the use of PARALLEL ASCENDING SYSTEMS visually perceived facial expressions and gestures. which allow much more rapid and tinely differen­ The parallel ascending systems ansing m the tiated communication. Strepsirhines also tend to retina and projecting to the lateral geniculate nu­ have much larger Olfactory bulbs than do haplo­ cleus of the thalamus are described in the chapters rhines [Stephan and Andy, 1970J. As complex sys­ by Rodieck and Kaas in this volume. In his pi­ tems of social organization evolved in haplorhine oneering study of comparative primate brain anat­ primates. social corrunumcation was increasingly omy, Gratiolet [Leuret and Gratiolet. 18571 mediated by the visual channel at the expense of discovered the system of fibers forming the optic the olfactory channel. One expression of this evo­ radiation that projects from the lateral geniculate lutionary development is the sensory input to the nucleus to the occipital lobe (see Fig. 5).' This amygdala. which is implicated in memory formation projection terminates heavily in layer rv of striate and is linked to the neuroendocrine functions of cortex (= area 17 of Brodmann [1909J = primary the hypothalamus and thus to the emotions. Prim­ visual cortex V-I = VI). There are three dis­ itively, the main input to the amygdala was from tinct parallel ascending fiber systems within the the olfactory bulb, but in haplorhines the amygdala geniculostriate projection; the first of these arises has major reciprocal connections with some of the from the magnocellular laminae. the second arises higher cortical areas [Aggleton et al., 1980; Ama­ from the parvocellular laminae. and the third arises tal and Price. 1984; Turner et al .. 1980; Whitlock from neurons in the interlaminar zones. including and Nauta. 1956]. The role of these structures in the S-Iaminae. and in strepsirhines from the konio­ the visual mediation of social signals is indicated cellular laminae. by the presence of neurons that are selectively Before reviewing these three ascending systems responsive to the images of faces and facial expres­ in detail. some details concerning the structure of sions in the amygdala and inferior temporal cortex layer IV of striate cortex must be considered. [Bruce et al .. 1981; Desimone et al., 1984; Gross Brodmann (1909J subdivided layer IV of area 17 et al., 1972; Leonard et al .. 1985; Perrett et al., in primates into three sublaminae: two cell-rich 1982. 1984. 1985a,b; Sanghera et al., 1979]. The layers. IVa and rvc. separated by a cell-poor layer evolutionary development of this system in higher IVb. which corresponds to the dense fiber plexus primates is thus linked to their expanded capacity known as the stria of Gennari. Brodmann [19091 Visual Cortex in Primates 283

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Fig. 5. Visual pathway of baboon Papio and of nerve (i,)}. external or lateral geniculate nucleus (kl. capuchin monkey, dissected by Gratiolet [Leuret and and the apparent continuation of optic nerve as J Gratlolet. 1857]. In this work. for the first time. a "visual radiation" (I) to the occipital lobe: C. medial connection was shown between subcortical visual view of right hemisphere showing. visual pathway centers and cerebral cortex. the so-called "visual or after removal of obstructing parts: the 0ric tract optic radiation of Gratiolet", and the importance of (m), inner and outer root of the same (m ,mil). the the cortex as the uppermost level in the cerebral latter enveloping the external geniculate nucleus. with hierarchy was anatomically demonstrated. Labeling: fiber fan of visual radiation (mill) streaming toward A. view of the brain from below. with a part of the the occipital lobe at right; m1V , anterior fibers of right temporal lobe removed to show the entry of radiation mingling with callosal fibers. From a spec· optic tract 0 into subcortical visual centers: lateral imen "teased" or dissected with needles. after a geniculate nucleus (s) and pulvinar of thalamus (t); preliminary maceration. From Leuret and Gratiolet. B. basal view of the dissected visual system of both AnalOmie comparee du systeme nerveux (arias). 1857. hemispheres showing junction of optic nerves in the PIs. 26 and 27. Reproduced from Polyak. [19571, chiasma (h). external and internal "roots" of optic with permission. I

284 Allman and McGuinness

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Fig. 6. Cell arrangement in the marginal portion of human striate cortex stained with Nissl-toluidine blue method (Lenhossek's modification), showing the merging of the three sUblayers of the inner granular layer of the striate area (4a, 4b, 4c) into a single layer 4 in the parastriate area at the right end of the figure. Reproduced from Polyak, [1957], with permission. and Polyak [1957] noted that layers IVa and IVc This evidence suggests that the parvocellular pro­ fuse at the margin of area 17 and are continuous jection to Brodmann's layer IVa may be a special­ with layer IV in area 18 (see Fig. 6). Other anato­ ization restricted to diurnal primates. However, mists have restricted their definition of layer IV of the cytoarchitecrural distinctiveness of Brod­ primate striate cortex to the layer corresponding to mann's layer IVa is not associated with diurnality. IVc of Brodmann [Hassler, 1967: Diamond et ai, For example. while it is very difficult to distin­ 1985; see also von Bonin. 1942. for discussion]. guish layers corresponding to Brodmann's IVa and The layer corresponding to IVa of Brodmann re­ IVb in Galago [von Bonin. 1945], they can be ceives a projection from the parvocellular laminae seen easily in Aotus. Moreover, Brodmann's layer of the lateral geniculate nucleus in Macaca [Hubel IVa is especially well developed in Tarsius. and it and WieseL 1972] and Saimiri [Fitzpatrick et al, is separated by a cell-poor layer (IVb) from an­ 1983], but there is no evidence of a similar projec­ other dense layer (IVc), as in other haplorhine tion in Galago and Aotus [Diamond et al, 1985]. primates (see Fig. 7). Moreover, layers IVa, IVb. Visual Cortex in Primates 285

summary, the magnocellular system is fast, sensi­ tive to low-oontrast stimuli, and probably sub­ serves the perception of visual motion. The parvocellular laminae occupy a much larger portion of the lateral geniculate nucleus and have a much more complex pattern of sublamination in diurnal. as compared to nocturnal. primates [Hass­ ler, 1967; Kaas et al, 19781. The parvocellular laminae project to the lower half of layer IVc of striate cortex. This has been termed layer IVc-beta in studies in Macaca [Hubel and Wiesel. 1972J and layer IV-beta in studies in Saimiri. Aorus, and Galago [Fitzpatrick et al, 1983; Diamond et al' 1985] .. In contrast to the magnocellular system, the parvocellular system is slower, insensitive to low­ contrast stimuli. and probably 'subserves the per­ ception of fine detail and. in diurnal primates. color [Wiesel and Hubel, 1966; Sherman et al. Fig. 7. Cresyl-violet srained parasagirral section 1976; Dreher et al' 1976; Schiller and Malpeli. through primary visual cortex in the calcarine sulcus 1978: Kaplan and Shapley, 1982: Hicks et al' 1983: In Tarsius bancanus from our collection. Derrington and Lennie. 1984: Derrington et aL 19841. Other parts of the lateral geniculate nucleus and IVc are continuous with layer IV of the adjoin­ project to layers L U. and III of striate cortex. 109 extrastriate cortex in Tarsius. With horseradish peroxidase (HRP) injections re­ The magnocellular laminae project to the upper stricted to cortical layers I and U in Galago. Carey half of layer IVc of striate cortex. This has been et al [1979] found retrograde filling of neurons in termed layer IVc-alpha in studies in Macaca [Hu­ the interlaminar zones including laminae S. which bel and Wiesel. 1972] and layer IV-alpha in studies lies adjacent to the optic tract. as well as in the in Saimiri. Aorus. and Galago [Fitzpatrick et aL koniocellular laminae, which are intercalated be­ 1983: Diamond et at. 1985] (see Fig. 8). The main tween the two pa!""ocellular laminae in strepsirhine ascending connections of the magnocellular sys­ primates. Livingstone and Hubel [19821 demon­ rem are illustrated in Figure 9. Fiber conduction strated in Macaca and Saimiri that the lateral ge­ in the magnocellular system is faster than in other niculate nucleus projects to the cytochrome systems [Sherman et al. 1976: Dreher et al. 1976; oxidase-rich structures, variously known as Schiller and Malpeli. 1978; Mitzdorf and Singer, "puffs." "blobs." or "patches." in striate layer III 1979; Maunsell and Schiller, 1984], which corre­ that were originally discovered by Wong-Riley [see lates with the dense myelination of Brodmann's Livingstone and Hubel, 1982, 1984]. Fitzpatrick layer IVb in striate cortex and the deeper layers of et al [1983] found in Saimiri that the interlaminar the middle temporal visual area (MT). The neu­ zones surrounding the magnocellular laminae. in­ rons in layer IVb of striate cortex are highly sen­ cluding the S laminae, project to the cytochrome sitive to the direction of stimulus motion [Dow, oxidase-rich structures in layer III and to layer I of 1974; Poggio. 1984: Livingstone and Hubel, 1984: striate cortex. Diamond et al [19851 demonstrated Movshon and Newsome. 1984], as are the neurons these projections for the interlaminar zones in in area MT [Zeki. 1974; Baker et al. 1981; Maun­ Aorus and Galago and found in Galago that the sell and Van Essen. 1983a: Albright. 19841. Neu­ koniocellular laminae project to these targets as rons in the magnocellular laminae of the lateral well. The interlaminar zones. the S laminae. and geniculate nucleus are much more sensitive to low­ the koniocellular laminae all receive input from contrast stimuli than are the neurons in the parvo­ the retina [Kaas et aI. 1978]. The optic tectum also cellular laminae [Kaplan and Shapley, 1982; Hicks projects to the interlaminar zones. including the S et al. 1983; Denington and Lennie, 1984]. In laminae in Saimiri [Harting et al, 1980] and inter­ GAlAGO OWL SQUIRREL MONKEY ~KEy

Fig. 8. Diagram to depict the relation between the laminar organization of the striate cortex and the projections of the lateral geniculate nucleus in Gall/go, Aotll~, and SlIimiri. Reproduced from Diamond, ctllll1985 L with permission. Visual Cortex in Primates 287

1985; Tigges and Tigges, 1979; Hitchcock and Hickey, 1980; Horton and Hedley-Whyte. 1984; Glendenning et al,. 1976; Casagrande and Skeen, 1980]. This horizontal segregation of ocular inputs to layer IV of striate cortex is poorly developed or absent in AoIUS, Callithrix. Saimiri. Pithecia. and Cebus, all of which are New World monkeys [Kaas et al, 1976; Spatz, 1979; DeBruyn and Casa­ grande, 1981; Hubel and Wiesel, 1978; Hendrick­ son and Tigges, 1985;' Kaas, personal com­ munication; Rowe et al. 19781. The ocular segre­ gation in input has been found in all Old World primates tested thus far, including the strepsirhine, GaJago, various monkeys, chimpanzees,. and hu- . mans, plus one New World primate, the spider monkey, Ateles. This distribution is strongly neg­ atively correlated with a distinctive visual behav­ ior, "head cocking," which has been studied in 40 primate species by Menzel [1980]. When most New World monkeys look at an object they cock their heads from side to side (see Fig. 10). Head cocking is particularly notable in young animals and follows a definite ontogenetic course [Menzel. SUPERIOR TEMPORAL AREAS ISTI 1980). By contrast. spider monkeys. galagos. all Fig. 9. The mam ascending connections of Lhe Old World monkeys (except Miopicheeus). apes. magnocellular system. The evidence for these con­ and humans rarely head cock when regarding an nections by level comes from (a) Perry et aI. [1984]; object (see Fig. II). Miopithecus. the smallest Old (b) Hubel and Wiesel (1972); (el Fitzpatrick et aL World monkey, various Lemur species. Hapale­ [1985]; Mitzdorf and Singer (1979); (d) Spatz [1977]; rnur, and Propichecus head cock. bUt the input to Lund et aI. (l975] (e) Hubel, personal communica­ layer IV of striate cortex is unknown in these tion; if) DeYoe and Van Essen [1985]; Shipp and primates. Zeki [1985J; (g) Weller et al. [1984]; Ungerleider Did the ocular dominance system evolve inde­ and Desimone [1985]. pendently at least three times in galagos. in spider monkeys, and in Old World monkeys. apes. and laminar zones and koniocellular laminae in Gaiago humans? Or was this system present in the earliest [Fitzpatrick et al, 1980). Thus the interIaminar true primates and lost in most New World mon­ system constitutes a third parallel ascending path­ keys, as has been suggested by Aorence et al [1986]? way whereby retinal and tectal input is relayed to (see Fig. 12). It is an intriguing possibility striate cortex. that head cocking represents a specialized form of visual scanning that is somehow incompatible with the ocular dominance system of primary visual OCULAR DOMINANCE SYSTEMS AND cortex, While ocular dominance systems tend to VISUAL BEHAVIOR occur in larger primates and head cocking occurs In Macaca, Aceles. Cercopichecus. Erychroce­ in snta1Ier ones. it should not be concluded that it bus. Papio. Pan. Homo. and Gaiago. the inputs is necessarily related to interocular distance for from the contralateralIy and ipsilaterally receptive binocular parallax for stereopsis. since the ocular geniculate laminae are horizontally segregated in dominance system is present in small galagos and layer IV. which is the anatomical basis of Hubel head cocking is not. Furthermore, it has some­ and Wiesel's (1968) ocular dominance columns times been suggested that the ocular dominance [Hubel and Wiesel. 1972: Florence et al, 1986: system is required for stereopsis. This appears not Hendrickson et al, 1978; Hendrickson and Tigges. to be true since Aocus readily discriminates ran­ I• ~:

288 Allman and McGniimess.

Fig. 10. Head cocking in Aotus trivirgatus. Reproduced from Menzel, [1980], with pennission. dom-dot stereograrns with no monocular depth linesterase staining in the parvocellular laminae. cues and thus possesses stereoscopic perception However, they found that striate cortex lesions (Miezin and Allman. unpublished observations). greatly reduced the staining in the visuotopica11y corresponding parts of the parvocellular laminae (see Fig. 13). In addition, they found acetylcholin­ CORTICOGENICULATE FEEDBACK: esterase-positive neurons in layer VI of striate cor­ A POSSmLE SPECIALIZATION IN tex. Fitzpatrick and Diamond [19801 also found NIGIIT-ACI'IVE PRIMATES that the parvocellular laminae were more densely Layer VI of striate cortex projects back upon the stained than the magnocellular laminae in Aotus. lateral geniculate nucleus in Macaca, Gaiago, and In contrast, Hess and Rockland [1983] discov­ AOiUS [Lund et al. 1975: Horton. 1984; Diamond ered that acetylcholinesterase staining was denser et al. 1985]. There is evidence in Galago that a in the magnocellular laminae than in the parvocel­ component of this corticogeniculate feedback pro­ lular laminae in Saimiri, and they suggested that jection that terminates in the parvocellular laminae the difference in laminar distribution was relatf!d is rich in acetylcholinesterase. Fitzpatrick and Dia­ to the diurnal activity pattern of Saimiri as com­ mond [1980] found in Galago that the parvocellu­ pared to the nocturnality of Galago and Aotus. In tar laminae are much richer in acetylcholinesterase other diurnal primates as well, including Macaca than are the koniocellular or magnocellular lami­ [Graybiel and Ragsdale, 1982], Callithrix. and nae. In an elegant series of experiments, they dem­ Homo (McGuinness. McDonald. and Allman. onstrated that the dense acetylcholinesterase unpublished observations), the magnoceilular lam­ staining in the parvocellular laminae in Gaiago inae are more densely stained for acetyl­ was not reduced by eliminating the retinal input. cholinesterase than the parvocellular laminae. In Similarly, they found that kainic acid injections in addition to Gaiago and Aotus. the parvocellular the lateral geniculate nucleus. which produced se­ laminae are more densely stained than the magno­ vere cellular destruction, did not reduce acetylcho­ cellular laminae in the nocturnal Tarsius [Mc­ Visual Cortex in Primates 289

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Fig. 11. Distribution of head cocking across 40 primate species. Each point is a single subject (n '= 229); circles, adults; squares. juveniles; triangles. infants carried by adults. Reproduced from Menzel. [1980], with permission.

Guinness and Allman. 1985}. In Lemur fulvus albifrons subspecies is active at night as well and aibifrons. the parvocellular laminae also were more has a "round-the-clock" or diel activity pattern densely stained than the magnocellular laminae [Conley, 1975; Tattersall. 1982], and thus they [McDonald et al. 1985]. which was the fIrst appar­ must use their visual system in conditions of low ent exception to the correlation between dense par­ illumination as do nocturnal animals. It remains to vocellular staining and nocturnality. LelTUl.r fulvus be determined whether the parvocellular laminae has often been considered to be diUrnal. but the are rich in acetylcholinesterase in all strepsirhine It ~

290 Allman and McGuinness NEW WORLD OLD WORLD

HOMINIDAE CEBIDAE 11m . Saimiriinae r.~~ PONGIDAE AoUnae (K~I~=!J Call1cebinae Alollattinae Pllheciinae ISakl i - Cebinae CALLITRICHIDAE IC.bU~1 I ICatHthrht ( HYLOBATIDAE Atelinae \ CA~

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Fig. U. A phylogenetic tree of primates indicating ing et al. [l9731 (Tupaia): Hendrickson and Wilson those genera in which clear ocular segregation [19791 (Macaca. Saimiri); Hendrickson e! al. [1978J (black), no ocular segregation (black outline), or (Macaca) , Cercopllhecus. Erythrocebus. Papio); weak segregation (dorted outline) has been demon­ Hitchcock and Hickey [198OJ (Homo); Hubel [19751 strated in normai adults. Adapted from Hershkovi!Z (Tupaia): Hubel and Wiesel [1968. 19721 (Macaca. [19771. Data for ocular segregation were taken from Ateles); Hubel and Wiesel [19781 (Saimiri); Hube! et the following references: Casagrande and Hanmg al [1976J (Macaca. Gil/ago); Kaas. personal com­ 119751 (Tupaia): Casagrande and Skeen. [1980] munication (Saki): leVay er at. [1975. 1980. 1985] (Ga/ago); Conley ct al. [1984] (Tupaia); DeBruyn (Macacal; Rowe et al. [19781 (Amus); Spa!Z.[1979] and Casagrande [19811 (Callithrix); Florence and (Caliithrix); Tigges and Tigges [\979) (Pan); Wiese! Casagrande [1978], and Florence et al. [19861 et al. [1974) (Macaca). Reproduced from Florence (Aeeies); Glendenning ct ai. [1976] (Gaiago); Han­ ct al [1986J, with permIssion.

primates or whether there are any strepsirhines diurnal primates. There are likely to be additional that are limited to a diurnal activity pattern. The sources of acetylcholinesterase input to the lateral present evidence does suggest that the parvocellu­ geniculate nucleus that account for the background lar laminae are rich in acetylcholinesterase in pri­ staining throughout the nucleus and perhaps denser mates that are active at night and thus adapted to staining in the magnocellular laminae in diurnal function in a dimly illuminated environment. primates. These may arise from the brainstem re­ In contrast to the findings in Gaiago. Hess and ticular formation and mediate a general enhance­ Rockland [1983] found in Macaca and Saimiri that ment of geniculate responses [Sherman and Koch. striate conex lesions did not affect the pattern of 19851· acetylcholinesterase staining in the lateral genicu­ These fmdings suggest that in night-active pri­ late nucleus. and thus the acetylcholinesterase-rich mates there is an acetylcholinesterase-rich projec­ striate feedback pathway appears to be absent in tion feeding back from the striate conex to the Visual Conex in Primates 291

TIlE REPRESENTATION OF THE VISUAL FIELD IN STRIATE CORTEX Gratiolet's [Leuret and Gratiolet, 1857] dissec­ tion of the optic radiation traced the visual pathway to the occipital lobe. In 1881, Munk confirmed the location of visual conex in the occipital lobe by making a series of selective lesions in Macaca and observing postoperative deficits in behavior. Munk proposed a scheme for the representation of the retina in the occipital lobe, which proved to be incorrect. Schaefer [1888] established that unilat­ eral removal ofthe occipital lobe produced a visual deficit in the contralateral half of the visual field. However, Schaefer [1889] was unable to deter­ mine further aspects of the map because "the dif­ ficulty of arriving at reliable conclusions from localised extirpations of the visual area is enor­ mous. For the animals soon acquire the habit of compensating for local detlcits in the visual field. by rapid movements of the eyes. sO as to baffle all attempts to determine the existence of such de­ tects. I believe. indeed. that to arrive at detailed conclusions we must await the results of perimetnc observations in cases of cerebral lesions in the human subject" [Schaefer, 1889. p. 6]. Schaefer'S Fig. 13. A parasagittal section through the lateral prediction was correct. The first accurate map­ geniculate body of a Galago that had a small piece pings of the representation of the contralateral vi­ of the striate conex; ex;tirpated nine days prior to sual hemifield in striate conex were achieved by death. The chief point of the photomicrograph is the presence of a break or gap in the dark bands corre­ Inouye [1909J and Holmes [1918], who related sponding to layers 3 and 6. These gaps are pointed visual field defects to the sites of visual conex out by arrowheads. x 50, Reproduced from Fitzpa­ lesions in soldiers who had been injured in the trick and Diamond [1980], with permission. Russo-Japanese and First World Wars. respec­ tively (see Fig. 14). The advent of positron emis­ sion tomography (PET scanning) has made possible the study of cortical organization in normal human parvocellular laminae that is not present in diurnal subjects. and initial fIndings with this method have primates. A possible functional role for this system confmned and extended the early observations is suggested by findings in the rabbit retina, where [Kushner et al, 1982; Fox et ai, 1986]. acetylcholine enhances responses to slowly mov­ The development of amplifiers and oscilloscopes ing stimuli [Masland et aI. 1984]. Alternatively, made possible the eJectrophysiological study of the acetylcholinesterase may regulate or amplify the responses of visual conex. By recording visually effects of other neurotransmitter systems [Bnin et evoked potentials, Talbot and Marshall (1941) aI. 1982]. In diurnal primates. the parvoceUular mapped the representation of the central visual laminae are insensitive to low-eontrast stimuli [Ka­ field in the striate cortex on the' lateral aspect of plan and Shapley, 1982; Hicks et aI. 1983; Der­ the occipital lobe in Macaca. Daniel and Whitter­ rington and Lennie. 1984). In primates that are idge [19611 mapped more extensive portions of active in a dimly illuminated environment, the striate conex in Macaca and Papio. as did Cowey acetylcholinesterase-rich feedback projection may [1964) in Saimiri. Using microelectrode recording serve to enhance the neural responses to low-eon­ techniques. Allman and Kaas [l971b) produced a trast or slowly moving stimuli in the parvoceUular relatively complete map of striate conex in Aorus laminae. (see Fig. 15). Myerson et al [1977] demonstrated Thick dark line represents Upper lip or F. parieto­ apex or F. calcarina F. calcanna occipitalis ,, , RIGHT. \

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Fig. IS. Representation of the visual field in striate posterior view and D is a ventromedial view of the cortex of owl monkey. Diagram A is a planar repre­ occipital lobe: in ventromedial view E. the lower sentation of the contralateral half of the visual field. bank of the calcarine fissure has been removed to which may be thought of as a quarter of a sphere. expose the upper bank. The gray area indicates the Diagram B is a planar representation of unfolded brain cut made to remove the lower bank of the striate cortex which is approximately one-half of an calcarine fissure. In F. the lower bank of the calca­ ellipsoid. The organization and location of striate rine fissure, which has been removed from the brain, cortex is shown in four views of the occipital lobe in is viewed dorsally. Reproduced from Allman and stages of dissection below (C-F). Diagram C is a Kaas. [197Ib], with permission. 294 Allman and McGuinness

for V-U in Saimiri. Anatomical evidence indicated a topographically organized projection from striate cortex to the second visual area in Macaca [Kuy­

20 pers et ai, 1965; Cragg and Ainswortb, 1969; Zeki, 19691 and in So.imiri [SpalZ et ai, 1970]. The visuotopic organization of V-U was mapped in

15 detail with microelectrodes in Aotus (see Fig. 17) [Allman and Kaas, 1971h, 1974aJ and in Macaca z [Gattass et ai, 1984]. V-II is an elongated strip of Q ~lO cortex that nearly surrounds V-I. The most distinc­ Z tive feature of the visuotopic organization of V-U < in primates is that a few degrees out from the "~ center of gaze the representation of the horizontal meridian splits to form most of the anterior border of the area. Allman and Kaas [l974a] termed this type of map a ~ second order transformation of the Ij 2S 3$45 5.5 visual hemifield" to conttast it with the topologi­ ECCENTRICITY [DEGREESl call y simpler "first order transformation" found Fig. 16. Magnification in seriate conex and the in V-I. reunal ganglion cell layer as a funcHon of eccenlnc­ iry. Values shown are for ponions of retina and smaee cortex corresponding to representations of FlJNCrIONAL ARCHITECTURE OF concenrric zones. each 10 degrees Wide. in the visual V-I At"'lD V-II field from 0 to 60 degrees and of the remainder of the visual field. the zone from 60 to 100 degrees. The distribution 01' the mitochondrial enzyme. Reproduced from Myerson. [1977]. with permission. cytochrome oxidase. has provided an important guide to the functional architecture of visual cor­ tex. Staining for cytochrome oxidase activity re­ in Aotus that the proportion of cells in striate cor­ veals dense concentrations in Brodmann'slayers tex devored to the representation of the central IVa. rvc. and VI in striate cortex, and a horizon­ visual field is much larger than the comparable tally repeating pattern most noticeable in layer ill proportion of retinal ganglion cells (see Fig. 16). (see Fig. 18). This pattern is most striking in These results. together with comparable observa­ tangential sections through layer III of flattened tions for Macaca [Malpeli and Baker. 1975~ Perry cortices. Figures 19 and 20 illustrate this pattern and Cowey. 19851. indicate that the relative repre­ for Saimiri and Aotus [Tootell et al. 1983. 19851· sentation of the central visual field expands in the The pattern in srriate cortex is a relatively regular asending pathway from the retina to the striate array of spots of high cytochrome oxidase activity cortex. The representation of the fovea in Macaca separated by a lattice of lower activity. The pattern has recently been mapped in considerable detail by in the adjacent area V-U is a series of thick stripes Dow et aI [1985] and for the entire visual field by and thin stripes of high cytochrome oxidase activ­ Van Essen et aI [1984]. ity separated by interstripes of lower activity that extend across the width of this beltlike area. The thin stripes are much more prominent in Saimiri TIlE REPRESENTATION OF THE VISUAL FIELD than in Aotus. In experiments conducted primarily IN THE SECOND VISUAL AREA in Macaca, this pattern has been linked to func­ Early electrophysiological recordings revealed tional architecture. [n metabolic studies using 14C_ the existence of a second visual area (V-U = V2) 2-deoxyglucose (2DG) as a functional marker, adjacent to the representation of the vertical merid­ Tootell et al [1982] found that stimulation with low ian representation in the primary area in cats [Tal­ spatial frequency gratings resulted in high 2DG bot. 1941] and rabbits [Thompson et al. 1950]. uptake in the spots while stimulation with high. Cowey [1964] found electrophysiological evidence spatial frequency gratings resulted in high uptake ------..... ­ DORSOLATERAL VIEW

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Fig. 17. Summary diagram illustrating the represen­ a dorsal view of me lower bank of me calcarine tations of me visual field in V-I. V-II. and MT in me sulcus which has been removed from me brain. The owl monkey. Diagram A is a dorsolateral view small circles indicate me representation of me verti­ of me posterior two-mirds of me left cerebral hemi­ cal meridian of me visual field; me black squares sphere. Diagram B is a ventromedial view of me indicate me representation of me horizontal meridian posterior two-mirds of me left cerebral hemisphere of me contralateral hemifield: me black triangles in which me brainstem and cerebellum have been indicate me representation of me temporal periphery removed to expose me ventral or tentorial surface of of me contralateral hemifield. The rows of VVVVV me occipital lobe. Diagram C is a similar ventrome­ indicate me anterior limits of visual cortex. Anterior dial view in which me lower bank of me calcarine is up in all of me diagrams. Reproduced from AU­ sulcus has been removed to expose visual cortex on man and Kaas. [1974aJ. wim permission. me upper bank of me calcarine sulcus. Diagram D is Fig. 18. Laminar pattern of cytochrome oxidase zyme activity spaced about 350 !Lm apart (arrows). activity compared with Nissl stain and cortical pro­ Columns are most obvious in layer ill. but are also jection from lateral geniculate nucleus labelled by visible in layers II and IVb in this section. Nissl (e) transneuronal radioautography. (a) Coronal section and cytochrome oxidase (d) stains compared with through striate cortex (area 17, primary visual cor­ geniculate projection to cortex labeled by eye injec­ tex. V I) from a normal macaque monkey stained tion with ['H]proline (e). Darkest cytochrome oxi­ with cresyl violet. Arrow marks a thin layer of cell dase staining is visible in layers VI. IVc. and IVa. bodies at interface between layers I and II. which all layers that receive a direct input from the lateral stains lightly for cytochrome oxidase activity (see geniculate. Note that sharp lower border of layer IVc corresponding in b). Scale =; I mm. (b) An adjacent in the cytochrome oxidase stain matches the lower section processed for cytochrome oxidase histo­ extent of proline label. Scale = 100 !Lm. Reproduced chemistry shows regular columns of enhanced en­ from Horton. [1984]. with permission.

- Visual Cortex in Primates 297

5 mm

Fig. 19. Section through layer !II of a flat-mounted ity in Saimiri sciureus. Reproduced from Tomei! e{ occipital lobe stained for cytochrome oxidase activ- al [1983]. with permission.

Fig. 20. Section through layer !II of flat-mounted chrome oxidase activity. Reproduced from Tootell. cerebral cortex of Aotus rrivirgarus stained for cyto- et al [19851, with permission. 298 Allman and McGuinness in the surrounding lattice in striate cortex. Living­ THE MIDDLE TEMPORAL VISUAL AREA: stone and Hubel [1984] found that the neurons in AN AREA SPECIALIZED FOR THE ANALYSIS the cytochrome oxidase-rich spots in striate cortex, OFDOlliCTIONOFMOTION which they term "blobs," lack orientation selectiv­ ity (see Fig. 21), are rich in opponent-color mech­ The middle temporal visuai area (MT) is a highly anisms, and project to the thin stripes of distinctive, densely myelinated region that was first cytochrome oxidase activity in area V-II. By con­ identified and mapped in AolUS (see Figs. 22,31, trast, they found that the neurons in the "inter­ 33) [Allman and Kaas, 1971a]. In the cytochrome blob" lattice in striate cortex are orientation oxidase-stained section of flattened owl monkey selective and project to imerstripes of low cyto­ cortex illustrated in Figure 20. area MT appears chrome oxidase activity in area V-II. The thin as a densely stained oval that corresponds to the stripes and interstripes in turn project to area V4 myeloarchitecturally defined MT [Tootell et ai, [DeYoe and Van Essen, 1985; Shipp and Zeb, 1985). Area MT has also been mapped with both 1985]. The thick stripes of high cytochrome oxi­ anatomical and physiological methods in Galago dase activity in area V-II project to MT [DeYoe (see Fig. 23) [Allman et ai, 1973; Tigges et ai, and Van Essen, 1985; Shipp and Zeb, 1985]. 1973; Symonds and Kaas, 1978], Callithrix [Spatz, The spot-lattice pattern of cytochrome oxidase 1977], and Macaca [Ungerleider and Mishkin, activity has also been found in the striate cortex of 1979; Gattass and Gross, 1981; Van Essen et ai, Galago, Papio. and Homo [Horton. 1984; Horton 1981: Weller and Kaas, 1983]. Area MT contains Jnd Hedley-Whyte. 1984: Cusick et al. 1984]. It a representation of the comraiateral hemifield, ai­ appears to be absent in Tarsius. Hapalemur. and though the represemation of the far peripheral vi­ Cheirogaleus [McGuinness et ai. 1986]. It has thus suai field extends beyond the zone of dense far nm been identified in any nonprimate rested. myelination [Allman et ai. 1973; Gattass and including Rattus. Mus. Citellus. Felis. Tupaia. Or­ Gross. 1981; Desimone and Ungerieider. 1986]. vctolagus. and Mustela [Horton. 1984}. The stripe The striate input to area MT arises from Brod­ pattern in area V -IT has thus far been idennfied in mann's layer IVb and large cells located deep in Saimin, Aotus, Macaca, and Homo [Tootell et al. layer V in Callithrix [Spatz, 1975. 1977], Saimin 1982, 1985; Livingstone and Hubel, 1984: DeYoe [Tigges et ai. 1981], Aorus [Diamond et ai. 1985], and Van Essen, 1985; Shipp and Zeb. 1985: Too­ and Macaca [Lund et ai. 19751. Brodmann's layer tell and Hockfield, personal communicationJ. Liv­ lVb corresponds to the densely myelinated stria of ingstone and Hubel [1984] and Tootell [19851 have Gennari. which contains many horizontally ori­ found evidence that the spots of high cytochrome ented fibers, some of which travel for a consider­ oxidase activity in striate cortex are involved in able distance [Polyak, 1957: Fisken et ai, 1975; the analysis of color in Macaca, but the presence Fitzpatrick et ai. 19851. Layer [Vb receives its of well-defined spot-lattice systems in the noctur­ input from the rnagnocellular recipiem layer IVc­ nal genera, Aotus and Galago, suggests that the aipha [Fitzpatrick et ai, 1985]. The neurons in spots must be linked to functions other than color layer !Vb in monkeys are highly sensitive to the vision. As of yet there have been no studies of the direction of stimulus motion [Dow, 1974; Poggio, functional correlates of the cytOChrome oxidase­ 1984; Livingstone and Hubel. 1984; Movshon and defined structures in nocrurnal primates. How­ Newsome, 1984], as are the neurons in area MT ever, the findings in Macaca that the spots are [Zeb. 1974; Baker et ai, 1981; Maunsell and Van sensitive to low spatial frequency and low-contrast Essen, 1983a; Albright, 1984]. In Galago, Brod­ stimuli [Tootell et ai. 1982; Tootell, 1985], to­ mann's layer !Vb is not distinguishable, but neu­ gether with their lack of orientation selectivity rons in the deeper part of layer III and in layer V [Livingstone and HubeL 1984], suggest that they project to MT [Diamond et ai, 1985]. It would be may be linked to analysis of luminosity or possibly interesting to determine the functionai properties brightness constancy. of this system in Galago, which lacks the well­ Visual Cortex in Primates 299

Fig. 21. Two parallel penetrations in layers 2 and 3 of 18 of the unitS encountered in these two penetra­ of macaque parafoveal striate cortel(. The section tions. The penetrations go from bottom to top. Re­ was stained for cytochrome ol(idase. The lesions produced from Livingstone and Hubel [1984], with have been emphasized with dots. Polar histograms permission. t I i , ~

300 Allman and McGuinness

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Fig. 22. Photomicrographs of two adjacent coronal sections through the middle tem­ poral visual area (MT) in Aotus. The upper photomicrograph was taken of a section stained with hematoxylin for myelin. The lower photomicrograph was taken of the adjacent coronal section stained with thiomn. Scale bar I mm.

developed horizontal fiber system in the stria of As the microelectrode advances through MT there Gennari. is a systematic shift in the directional preference Neurons in MT have very transient responses of successively recorded neurons in Macaca [Zeki. with average latencies of 33 milliseconds in AOlUS 1974; Albright et al, 1984] and AOIUS [Baker et al. [Miezin et al, 19861 and 39 milliseconds in 1981]. The system of directional preferences is Macaca [Maunsell, 1986]. The relatively short la­ linked to an orientation-selective system, since in tencies and transient responses reflect the magno­ most MT neurons the directional preference tends cellular input relayed through V-I and V-II to MT. to be orthogonal to the orientation preference

Fig. 23. The topological transformation of the con­ maximum depth of 1,350 ILm. The average recording tralateral half of the visual field in MT in the bush­ site was approximately 360 ILm beneath the pial sur­ baby. The lower diagram is a drawing of a face. The receptive fields for recording sites 1-44 in dorsolateral view of the caudal two-thirds of the left MT are illustrated in the large perimeter chan of the hemisphere. The small circles indicate the represen­ contralateral half of the visual field. The receptive tarion of the vertical meridian, the black triangles fields for recording sites A through F in V II and the indicate the extreme temporal periphery, and the interstitial zone between V II and MT are shown in black squares indicate the horizontal meridian. The the small perimeter chan for the central 10° of the surface locations or recording sites 1-44 are shown contralateral hal f of the visual field. The extent of V in the enlarged view of MT. which is outlined by II exposed on the dorsolateral surface of the brain small circles and black triangles and lies below the and the receptive fields mapped from recording sites drawing of the brain. Receptive fields were mapping in V II are shaded. Scale = 1 mm. Reproduced from at various depths from near the pial surface to a Allman et al [1973], with permission. Visual Cortex in Pr:ima1es 301

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[Baker et ai, 1981; Albright et ai, 1984J. In some penetrations there are abrupt 180 0 shifts in pre­ ferred direction as the electrode passes through populations of neurons sharing the same orienta­ tion preference (see Fig. 24). Orientation selectiv­ ity is the basis of the columnar system in striate cortex [Rubel and Wiesel, 1968] and is an ubiqui­ tous property of neurons in many extrastriate areas [Baker et ai, 1981J. In the evolution of the func­ tional organization of MT, the columnar system for directional selectivity may have developed out of a preexisting system for orientation selectivity. Albright et ai [1984] have found a systematic co­ lumnar representation of the axis of movement in area MT (see Fig. 25), which would be orthogonal to the orientation preferences of the majority of MT neurons. In this system, adjacent columns sharing the same axis of motion have opposite Fig. 25. Three-dimensional depiction of a block of preferred directions. Twenty-five percent of MT cortical tissue containing one configuration of axis neurons respond to the apparent motion of com­ and direction of motion columns that is consistent plex grating patterns (pattern direction-selective), with our data. The vertical dimension represents whereas most MT neurons and ail striate layer !Vb COrtical depth. The long axis of the figure may be viewed as two complete revolutions of axis of motIOn neurons respond to the actual direction of motion columns. Moving in this dimension. one would en­ of the components of the grating sUmulus (com- counter gradual changes in preferred direction. Within each axis of morion column (along the short axis of the figure>. the two opposite directions of Fig. 24. Direction and orientation selectivity for a motion along that axis of motion are represented as series of neurons recorded in a single penetration adjacent columns. Moving in this dimension. one nearly perpendicular to the surface of MT. A pair of would encounter frequent 180 0 reversals in preferred graphs is illustrated for each unit (HEMT69A-L). direction. with no change in preferred axis of mo­ The depth beneath the surface at which each cell was tion. Reproduced from Albright, [1984], with recorded is given beneath each identifying number. permission. An electrolytic lesion was made at the bottom of the mlcroelectrode track. Histological reconstruction in­ dicated that the penetration was perpendicular to the ponent direction-selective), which can be quite dif­ surface ofMT and nearly parallel to the radial fibers. ferent from the apparent direction of motion of the Cells A-J were located in layers II and III; cells K whole pattern (see Figs. 26, 27) [Movshon et ai, and L were located in layer lV. Graphs on the left illustrate the average response of each cell to five 1985; Movshon and Newsome, 1984J. The pattern presentations of a 20 X I ° light bar at 12 different direction-selective neurons may correspond to the angles. HEMT69A-F preferred 270°; HEMT69G­ population of MT neurons described by Albright K preferred 90°. Graphs on the right illustrate the [1984] that have preferred orientations roughly average response of the cells to ten presentations of parallel to their preferred orientation. Pattern di­ a flashed bar at the orientations shown. All cells rection selectivity appears to emerge from the ori­ except the last preferred the horizontal orientation; entation-selective system within MT, aithough their the last was inhibited by horizontal bars. The direc­ exact relationship to the columnar system remains tion of movement was 90° to the bar orientation. to be determined. The pattern direction-selective thus the preferred directions of 270° (down) and 90° MT neurons match perception and constitute a (up) are consistent with the preferred horizontal ori­ entation. The receptive-field centers were located an significant elaboration of function beyond that average of 16.6° below the horizontal meridian with found in striate cortex. The role of MT in the a standard deviation of 0.9 0 and an average of 6.7 0 perception of direction of moving stimuli is also temporal to the vertical meridian with a standard suggested by the effects of small lesions in this 0 deviation of 3.3 • Reproduced from Baker et al area, which produce deficits in the monkey's abil­ [1981]. with permission. ity to make smooth pursuit eye movements that , t ~. ~

304 Allman and McGuinness A B visual area (ST) where the neurons also are direc­ tionally selective but have much larger classical receptive fields [Sereno et al, 1986; Weller et al, 1984]. Figure 30 illustrates a pattern of intrinsic e. connections extending over a large portion of area •• MT inAotus [Weller et al, 1984]. The efferent cortical connections of area MT have been studied in Callithrix [Spatz and Tigges, l / 1972], Galago [Wall et al, 1982], AOlliS [Weller et al, 1984], Saimiri [Tigges et al, 1981], and Ma­ " caca [Maunsell and Van Essen, 1983b; Ungedei­ / der and Desimone, 1986]. Area MT's main / / ascending projection is to the superior temporal area (ST), which is located immediately anterior Fig. 26. A single grating (A) and a 90° plaid (B), to MT in AolliS [Weller et al, 1984], and may and the representation of their motions in velocity correspond to the medial superior temporal area space. Both patterns move directly to the right. but have different orientations and I-D motions. The (MST) , which also receives a major input from . dashed lines indicate the families of possible motions MT in Macaca [Maunsell and Van Essen, 1983b]. for each component. Reproduced from Movshon. et The location of these and other extrastriate areas al [1985], with permission. are illustrated in Figure 31 for AOlliS and Figure 32 for Macaca . •-\rea MT projects back upon striate track moving objects [Newsome et ai. 1985]. in layers. from which it receives input. It also pro­ contrast. eye movemems to stationary targets pre­ jects to the adjoining cortiCal area. termed DL In sented in the same position in the visual field were Aotus. and the V4 complex in Macaca. unimpaired. While area MT contains a visuotopic map as THE DORSOLATERAL AREA determined by conventional receptive-field map­ AND THE V4 COMPLEX ping techniques. 90% of its neurons are also influ­ enced by the direction and velocity of stimuli In AOfUS. the dorsolateral area rDLl wraps presented simultaneously outside of the classical around MT in much the same way that area V-II receptive field (see Figs. 28, 29) [Allman et al. forms an elonga[ed belt nearly surrounding area 1985a.bl. In spite of the obvious orientation selec­ V-I (see Fig. 33). Like area V-II. DL contains a tivity present in most MT neurons. they also re­ representation of the horizontal meridian that splits spond very well to moving random-dot patterns. to form most of the outer border of the area and is When mapped with moving sheets of random dots thus a second-order transformation of the visual presented simultaneously within and outside the field. A larger portion of DL is devoted to the classical receptive field, the total receptive fields representation of the central visual field than in of MT neurons typically are 50 to 100 times the any other cortical area in AOfUS. DL receives its size of the classical receptive fields. Thus MT main input from area V-II [Kaas and Lin. 1977] neurons are capable of integrating information and projects to caudal inferior temporal cortex about movement within their classical receptive (ITd [Weller and Kaas, 1985]. DL neurons have fields with more global information about move­ much longer average latencies (63 vs 33 millisec­ ment occurring elsewhere. The analysis of differ­ onds) and have much more sustained responses ential movement performed by these neurons may than MT neurons [Miezin et al, 1986], which may contribute to figure-ground discrimination and reflect a predominantly parvocellular system input depth perception based on motion parallax. The via V-I and V-II to DL. DL neurons are highly anatomical basis of these global mechanisms may selective for the size and shape of visual stimuli, result from intrinsic connections within MT irrespective of their position with the classical re­ [Maunsell and Van Essen, 1983b], or they may ceptive field [Petersen et al. 1980]. Most DL neu­ result from feedback from the superior temporal rons have a definite preferred size. while most Visual Cortex· in Primates 305 A Grating<' gOO PJoicl_ 90 911" - - . • ~ -- j~ • I. 1811" ~, CF JBOO ~ 11"

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neurons in other areas (MT. DM. and M) tend to In Callithrix, MT projects to separate dorsal and increase their responses with increasing stimulus ventral foci, which correspond in location to the length, width, or diameter up to the maximwn dorsal and ventral wings of DL in owl monkeys dimension tested, which corresponds to the size of [Spatz and Tigges, 1972]. In Saimiri, MT and V­ the classical receptive field (see Fig, 34). The II project to the presumptive location of DL dimensional selectivity of DL neurons suggests [Tigges et al, 1974, 1981; Wong-Riley, 1979], that DL contributes to size and shape perception, which in tum projects to the posterior part of which is consistent with the area's expanded rep­ inferior temporal cortex [Weller, 1982]. resentation of the central visual field and its starus Area V4 in Macaca was originally identified by as the principal source of input to inferior temporal Zeki [197lJ as a major recipient of input from the cortex. DL also is present in Galago. where it has second visual area. The extent of this region in a relatively expanded representation of the central Macaca has yet to be determined and it may con­ visual field [Allman and McGuinness. 1983J and tain several visual areas: for these reasons it has projects to inferior temporal cortex [Weller, 19821. been termed the V4 complex. Possible subdivisions 306 Allman and McGuinness

CENTER DOTS MOVE IN OPTIMUM DIRECTION BACKGROUND DIRECTION TYPE I VARIES HCMT328 50% z CENTER DOTS 2 MOVE ...... \. /.\ It ,: r~~-l .• < BACKGROUND ... DOTS .... :t:~!: .:! STATIONARY u ... " ~... ." ,,'" .. ; [§J ~.. 100% .,./.-'-'\ o UJ \ I '"Z 0 . / a.. '"UJ ex: 50% -50% \ . 0 UJ N :::i ..: "', ~ ...... / a: • 0 2 / . 01.. -100% r ! -180' -,20' -60' O' 50' 120' . / . \ . OIREC~ION OF MOVEMENT -20%L· . ," OF BACKGROUND DOTS -r80' -12Cl' -60' (J 60' !20' DIRECTION OF MOVEMENT OF CENTER DOTS Fig. 28. Response properties of a Type 1 neuron moving in the cell's preferred direction. In the right (antagonistic direcuon-selective surround\. The left graph the crf was stimulated by the array moving in graph depicts the response of the cell. HCMT32B. the optimum direction during the 2 second sample to 12 directions of movement of an array of random periods preceding background movements; thus a dots coextensive with its claSSical receptive field response of 100% in the left graph IS equivalent to (crt). The response is normalized so that 0% is equal 0% in the right graph. A value of - 100% in the to the average level of spontaneous activity sampled right graph indicates that the movement in the sur­ for 2 second periods before each presentation. Neg­ round reduced the neuron's tiring rate to zero. The ative percentages in the left graph indicate inhibition stimulus conditions are depicted schematically above relative to the level of spontaneous activity, The each graph. In the experiment the dots were much response in the optimum direction is 100%. The denser and the background much larger relative to right graph depicts the response of the cell to differ­ the center than depicted schematically. Reproduced ent directions of movement in the surround while the from Allman. et al (1985aJ. with pennission. crf was simultaneously stimulated with an array of the V4 complex have been suggested on the sustained responses than MT neurons [MaunselL basis of connections, neural response properties, 1987]. which presumably reflects a predominately and visuotopic organization [Zeki, 1971, 1977, parvocellular system input from the thin stripes 1983a; Maguire and Balzer, 1984]. Like area DL and interstripes in the second visual area [DeYoe in Aotus, the V4 complex is the major source of and Van Essen, 1985: Shipp and Zeki. 1985]. The input to inferior temporal cortex [Desimone et al. formidable complexity of this region in Macaca 1980]. Similarly like DL, V4 neurons are very may be related to the similarities between ma­ selective for the size and shape of stimuli [Desi­ caques and humans in color perception and spatial mone and Schein, 1987]. Also like DL. V4 neu­ contrast sensitivity [DeValois et al. 1974a.b]. This rons have longer latencies and much more complexity parallels the expansion of the parvocel-

I Visual Cortex in Primates 307

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{/)"" z /-\ o a. {/) z III Q a: ... 050%... -50% !::! /1 \ :r: ..oJ . . z :l! a: ~ .'\/ I OL -!000/1ll 2° 4'11 8 9 '6.0 32° 64" !2SO 2· 4" go ·6'" 32· 64" !28C1 PER SECOND PER SECOND Fig. 29. The effect of bar and background velocity ing the bar movmg at the optimum velocity (16° on neuron HCMT33C. The left graph is a velocity sec - I). The stimulus conditions are depicted sche­ tuning curve for a bar moving in the op(Jmum direc­ maucally above the graphs. bur in the experiment the tion with the background stationary. The right graph dots were much denser and the surround larger. IS a velocity tuning curve for background movement Reproduced from Allman. et al [1985al, with in the same direction while simultaneously present­ permission.

lular geniculate laminae relative to the magnocel­ lective and color coded. The responses of the first lular laminae and the formation of anatomically type were highly dependent on the wavelength of and functionally differentiated leaflets within the light illuminating the classical receptive field while parvocellular laminae in Macaca and most other the color-coded cells exhibited color constancy diurnal higher primates. including humans [Kaas over a certain range of illumination conditions. et al, 1972. 1978; Schiller and Malpeii, 1978]. The response of the color-coded cells depended on Recent recordings from neurons in the V 4 com­ the color of objects located outside the classical plex in Macaca have revealed broad surround re­ receptive field, which indicated that they possess gions tuned for orientation, spatial frequency, and surround mechanisms with complex and as yet color [Desimone and Schein, 1987]. Moran et al undetermined properties [Zeki, 1983b]. The influ­ [1983] found that while the classical receptive fields ence of the surround on the color of an object was for V4 cells located near the vertical meridian limited to the ipsilateral hemifield in a corpus extended an average of only 0.60 into the ipsilat­ callosum-sectioned human subject [Land et al, eral hemifield, the inhibitory surrounds extended 1983], which restricts the locus of the "retinex" at least 16 0 into the ipsilateral hemifield. The effect to the cortex. but regions other than the V4 suppression resulting from stimulation in the ipsi­ complex. particularly area V-II and the ventral lateral hemifield was gready reduced by section of posterior area (VP) and inferior temporal cortex. the corpus callosum. Zeki [1983a. b J reported two may be involved in these color constancy effects types of neurons in macaque V4: wavelength se- as well [Allman et al. 1985aJ. 308 Allman and McGuinness

MT 74 - 72R which is strongly implicated in memory processes 3H - PROLINE [Mishkin, 1982]. The inferior temporal visual cor­ tex, as well as higher somatosensory and auditory cortices, projects to the amygdala [Whit­ lock and Nauta, 1956; Aggleton et al, 1980; Turner et ai, 1980]. The amygdala in tum is reciprocally connected with the neuroendocrine centers of the hypothalamus [Price and Amaral, 1981]. The amygdala projects to the visual cortex [Tigges et al, 1981, 1982; Mizuno et ai, 1981], particularly to the junction between layers r and II in V4 and other cortical visual areas [Amaral and Price, 1984]. These connections provide avenues for in­ fluences for other sensory modalities. as well as motivation and memory, to mediate responses within the visuotopically organized cortical areas. Fig. 30. Intrinsic connections in MT. An injection of 3H-proline in MT of owl monkey 74-72 resulted in a densely labeled injection site (black) wah a less INFERJOR TEMPORAL CORTEX densely labeled surround (shaded). Other concentra­ tions of label (dots) tended to form spaced columns Lesions of infenor temporal cortex greatly di­ from white matter to cortical surface in frontal brain mmish a monkey's ability to learn new visuaI dis­ sections 150= JLm sections numbered caudoros­ criminations [Gross. 1973]. In humans. damage to trallYI. In a surface view or MT (upper left). the the ventromedial aspect of the occipito-temporal columns joined to form bands. The boundaries of cortex produces a syndrome known as prosopag­ MT were architectonically determined from tlber­ nosia. or the inability to recognize the faces of stained sections. The fiber-stained sections vaned in familiar individuals [Meadows. 1974al. Such le­ quality and dashed lines indicate less certam esti­ sions may also affect the patient's ability to rec­ mates of the position of the boundaries. Reproduced ognize other familiar objects such as animals. It from Weller. et aI [1984]. with permission. has been suggested that the main deficit in proso­ pagnosia is an inability to sort out an individual from a large array of similar objects [Damasio et aJ. 1982]. Many neurons in the inferior temporal cortex in Recent investigations have also demonstrated Macaca respond selectively to complex stimuli. important attentional and nonvisual inputs to the particularly those with special biological rele­ V4 complex in Macaca. Moran and Desimone vance, such as the image of hands and faces in [1985] have found in trained monkeys that the different orientations (see Fig. 35) [Gross et aJ. spatial location of focal attention gates visual pro­ 1972; Desimone et al. 1984]. The preferred ori­ cessing by filtering out irrelevant visual informa­ entation for the image of the hand usually corre­ tion within the classical receptive fields of neurons sponded to the way in which the monkey would in V4 and IT. Haenny et al [1987] have trained see its own hand. The neurons selectively respon­ macaques to match the orientation of a visually sive to faces are particularly common in the depths presented grating with a tactually presented grating of the superior temporal sulcus [Bruce et ai, 1981; and recorded the responses of V4 neurons during Perrett et al. 1982]. This region also contains neu­ this task. Sixty percent of the V4 cells were influ­ rons responsive to facial expressions and particu­ enced by the orientation of the tactile gratings. larly to whether the eyes are gazing at the subject which were not visible to the monkey; some of or not, which is an important social signal in Ma­ these responses were very specific and are likely caca [Perrett et al, 1984]. This area also contains to have developed as a consequence of the animal's neurons selectively responsive to views of body training. It is not clear how these influences are movement, such as a person walking toward or relayed to the visuotopically mapped areas; how­ away from the monkey [Perrett et al. 1985aj. These ever one possible route involves the amygdala, highly selective visual neurons in the depths of the Visual Cortex in Primates 309

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Fig. 31. The cortical areas of the owl monkey based eral auditory area; PP. posterior parietal visual cor­ on microelectrode mapping and architectonic and tex; R, rostral auditory area; ST, superior temporal connectional studies. Above is a ventromedial view; visual cortex; TP, temporal parietal visual cortex; below is a dorsolateral view. On the left is a perim­ V-I. first visual area; V-II. second visual area; VA. eter chart of the visual field. The pluses indicate ventral anterior visual area; VP, ventral posterior upper quadrant representations: minuses indicate visual area; X. optic chiasm. The cortical visual lower quadrants. The row ofVs indicate the approx­ areas were mapped by Allman and Kaas [1971a.b; imate border of visually responsive cortex. AI. first 1974a,b; 1975; 1976] and Newsome and Allman auditory area; AL. anterolateral auditory area: CC. [1980]; the somatosensory areas by Merzenich et al corpus callosum; DI. dorsointermediate visual area; [1978]; the auditory areas by Imig et al [1977]. The OL. dorsolateral crescent; OM. dorsomedial visual subdivisions of superior temporal and inferotem­ area; ITc, inferotemporal-caudal; ITM. inferotem­ poral cortex are based on the connectional studies of poral-medial: ITR. inferotemporal-rostral: M, me­ Weller [1983]. Weller et al [1984]. and Weiler and dial visual area: MT. middle temporal visual area: Kaas [19851. Scale =5mm. ON. optic nerve; OT. optic tectum; PL. posterolat­ 310 Allman and McGuinness

Fig. 32. The cortical areas of the macaque monkey temporal visual cortex; MT. middle temporal visual based on microelectrode mapping and architectonic area; PIT, posterior inferotemporal cortex; PO, pa­ and connectional studies [see review by Van Essen. rietal occipital visual area; PS, prostriata; VIP, ven­ 1985J. In the upper left is a lateral view of the cortex tral intraparietal cortex; VI, first visual area; V2, of the right hemisphere in the macaque monkey. In second visual area: V3, third visual area; V3A. third the lower right this cortex is unfolded. The cortex visual area (accessory); V4. fourth visual area; VA. has been cut along the upper and lower borders ventral anterior area; VP. ventral posterior area. between the first and second visual areas. AIT, an­ Courtesy of David Van Essen. . terior inferotemporal cortex; MST, medial superior

superior temporal sulcus are mixed with neurons THE MEDIAL VISUAL AREA AND responsive to auditory and somesthetic stimulation PARIETOOCCIPITAL AREA [Bruce et al, 1981; Perrett et ai, 1982]. It would be interesting to determine whether the auditory The medial visual area (M) is unique among all cells in this area respond selectively to specific the cortical visual areas in AoIUS in that it has a macaque vocalizations or whether there is any proportionally large representation of the periph­ relationship between cells responsive to the image eral visual field (see Fig. 36) [Allman and Kaas, of the hand and somesthetic stimulation. as would 1976]. Only 4% of area M is devoted to the rep­ occur in visuo-tactile exploration. Inferior tem­ resentation of the central 10° of the visual field. In poral cortex projects to the amygdala, which also Macaca there is an area in the same location with contains neurons selectively responsive to faces a similar visuotopic organization and emphasis of and facial expression [Sanghera et al, 1979; Leon­ the peripheral visual field representation that has ard et al, 1986], as well as to entorhinal cortex and been termed the parieto-occipital area (PO) [Covey portions of the frontal lobe (Weller, 1982]. et al, 1983]. In Macaca this area receives a strong Visual Cortex in Primates 311

vvvYVVVVvv v Y : Y v vvV : pp vy v V? v yV y yv > y v V V Y Y Y v :...... v v ....~ ....•. v v ''''~ \ '. v TP , L J " ___ +~:f.\.~~.,•• ~ •••.: ~ :--t-rMT,-j­ 1_················ r y ~.V .. v ''':V. .: v ~ ..: .... v : iii...• .. v :...... v v v '1. _ v '. v .. '.. .. (1) v v '.0 0 0. VP+ 0 Qo • Vv oo IT '~ .. ~VA+ 00000.0"0000;0' v v v v v v v v y v vVVV VVv 'iVVVVVVVV

Fig. JJ. A schematic unfolding of the visual cortex perimeter chart on the left shows the contralateral of the left hemisphere in the owl monkey. The visual (right) half of the visual field. The "prostriata" is conex corresponds to approximately the posterior histologically and physiologically distinct from V-II. third of the entire neocortex. The unfolded visual Symbols are the same as in Figure 31. [Sanides, cortex is approximately a hemispherical surface, 1970; Allman and Kaas, 1971bJ. Reproduced from which is viewed from above in this diagram. The Allman, [1982), with permission. input from area V-II, with lesser inputs from striate from V-I and V-ll in AolUS. Area M is unusual cortex, V3, V3A. VP, and parts of posterior pari­ among cortical areas tested in AoIUS in that most etal cortex [Colby et al, 1983; 1987]. In Saimiri of its neurons respond preferentially to rapidly there is a region in the same location on the medial moving stimuli (> 50° per second) [Baker et al, wall that receives input from the peripheral visual 1981). Finally, area M is unique in that all of its field representation of striate cortex in a pattern outgoing projections terminate in cortical layers I, corresponding to the visuotopic organization in V, and VI [Graham et al, 1979], which are usually area M [Martinez-Millan and Hollander. 1975; feedback connections (see Fig. 38, and below), Allman and Kaas, 1976]. Area M has been re­ Thus it appears that the main function of area M ported not to receive input from striate cortex or may be to modulate the activity of other areas, area V-II in AolUS, but it does receive input from such as DM and posterior parietal cortex (PP). We DM and posterior parietal cortex (Weller and Kaas. hypothesize that area M may detect suddent move­ 1981]. Area M may be homologous with the "dor­ ments in the periphery of the visual field and sal" area in Galago, which is located anterior to facilitate the corresponding parts of the visual field the lower field peripheral representation in V-II. representation in other cortical areas resulting in a and possesses a similar visuotopic organization shift of attention to the novel stimulus. Neurons in and emphasis on periphery [Allman et al, 1979]. posterior parietal cortex in Macaca are specifically Medial area neurons have very transient re­ facilitated when visual stimuli are presented in a sponses, which suggests that this area may be position in the visual field upon which the mon­ related to the magnocellular system [Miezin et al, key's attention has been directed [Robinson et al, 1986]. Medial area neurons have average latencies 1978]. Lesions in this locality in humans produce that are slightly longer than in area MT (42 vs 33 visual neglect and the inaccurate localization of milliseconds). which suggests that contrary to ex­ visual stimuli [Holmes and Horrax, 1919; Critch­ isting anatomical evidence there may be inputs ley, 1953]. I~

312 Allman and McGuinness

MT TIlE DORSOMEDlAL VISUAL AREA AND Dl M THIRD VISUAL AREA OM ~ The dorsomedial visual area (DM), like area Mf x=:n - MT. is a highly distinctive, densely myelinated A 50=16 50"'.39 zone in Aotus [Allman and Kaas, 19751.' OM re­ 20 M X-17 SO=J' ceives input from striate conex, area MT, and area OM j( =28 M and projects to posterior parietal cortex [Lin et ML SO=JJ 10 al, 1982; Wagor et al, 1975]. The responses of ~ t" .J L OM neurons are more sustained than neurons in ; ~ areas MT and M, but more transient than in OL 0' ....,..·.. ,....,....· 0 o .25 5 75>1S RESPONSE TO MAXIMUM (ENGTH Fag. JS. Responses of a unit that responded more 1 RESPONSE !O OPTIMUM LENGTH strongly to faces than to any other stimulus tested. A) Comparison of responses to faces, to faces with Mf X=JJ components removed, and to a hand. Stimuli were 50= 31 B X= 70 1SO= 45 photographic slides, presented for 2.5 sec, indicated ,0 M x: =4J by the bar under each histogram. All stimuli were J so= J3 centered on the fovea. Drawings under each histo­ DM ;( =.£0 gram were traced from stimuli. l. Monkey face in 5-0=20 101 IIIIII '0 narural color: 2. same monkey face with components rearranged (four pIeces); 3, second monkey face in color: 4, same monkey face with snout removed: 5. eyes removed: 6. color removed: 7. human face; 8. l5 l';>l'; hand. The bar graph at top left indicates summed - RESPONSE TO MAX IMUM WIDTH responses to each stimulus. Responses were com­ 1 RESPONSE ro OP'1 MUM wlQTH puted from the firing rate of the unit during the stimulus presentation minus the average firing rate i:::::: 63 before the stimulus presentation. 0 represents the c SO= 27 20 base line firing rate. Removing any component of the face reduced the response, while scrambling the componems eliminated the response. B) Responses

10 to a monkey face in differem degrees of rotation. Ali stimuli were colored slides; other conditions were the same as in A. Responses decreased as the face was rotated from frontal to profile view. As in A. removing the eyes from the frontal view reduced the RESPONSE TO MAX IMUM OIAMETER response. C) Responses to faces in different loca­ 1 RESPONSe 10 OPTIMUM OIAMETER tions within receptive field. The stimulus was the same as in B (frontal view of face). Ine stimulus Fag. 34. Distributions of stimulus dimension selec­ was centered on the horizontal meridian of the visual tivity indices for length (A), width (B), and spot field. I, Ipsilateral visual field; C. contralateral vi­ diameter (C). The distributions for DL cells are on sual field: FOV, fovea. The best response was to the the left, and the distributions for MT. M, and DM stimulus positioned over the fovea. D) Responses to cells are on the right. S£atistics comparing these sine-wave gratings and bars. Gratings ranged from distributions; df for length = 3.94; width = 3.66: 0.25 to 8 cycles/degree. and bars were 0.10 wide. spot diameter = 3.81. S-values for length. width. All stimuli had a venical orien£ation. Gratings were and spot diameter selectivity, respectively: DL vs drifted at I cycle/sec for 5 sec. and bars were moved MT 3.42,* 3.91. * 8.66*; DL vs M = 3.14, *1.53, at 10 !sec. Stimuli were generated on a 10 0 diameter 3.44*; DL vs DM = 2.76.*1.55.4.94*; MT vs M CRT display. LB, Light bar; DB. dark bar. There 0.05,0.21, 0.29; MT vs DM = 0.03, 0.07, 0.01: was no response to either bars or gratings of any M vs DM = 0.01.0.02.0.21. *, P < 0.05. Repro­ frequency. Reproduced from Desimone et al [1984]. duced from Petersen, et al [1980], with permission. with permission. SO .1 B1 .1 B " z: 1 5"0 0/:> SZ-O f ''':11 ,,* 'tFlf,pmh 4Pij;''''~i 'fII'/4Mi1fl fl""'''' 1fiMjflftf41 I1l"'rM 'ftffii;H o

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o 314 Allman and McGuinness

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Fig. 36. Microelectrode recording penetrations and is an expanded map of the visuotopic organization of receptive field data for the medial visual area in owl the medial area. The circles Indicate the representa­ monkey 72-455. The diagram on the lower left is a tion of the vertical meridian (midline) of the visual view of the posterior half of the medial wall of field: the squares indicate the horizontal meridian of cerebral cortex of the left hemisphere with the brain­ the contralateral half of the visual field: the triangles stem and cerebellum removed. Anterior is up and indicate the temporal periphery of the contralateral dorsal is to the left in this diagram. Microelectrode hemifield. V I is the first visual area: V n is the penetrations are numbered. and recording sites are second visual area: DM is the dorsomedial visual indicated by short bars denoted by letters. Scale I area. OD indicates the projection of the optic disk or mm. The corresponding receptive fields are shown blind spot. Reproduced from Allman and Kaas in the perimeter chart on the right. In the upper left (1976), with permission.

[Petersen et ai, 19861. The average latencies of respond to the dorso-intermediate visual area (Dl) DM neurons are the same (42 milliseconds) as in in Aotus. V3 was originally considered to extend area M [Miezin et aL 1986]. DM neurons are more along the entire anterior border of the second vi­ sharply tuned for stimulus orientation than sual area in Macaca on the basis of striate projec­ neurons in area MT, M, or DL. In Macaca, the (ions [Zeki. 1969], but this is no longer consistent third visual area (V3) is located in a similar posi­ with available data [Van Essen. 1985]. tion, is densely myelinated. and receives input from striate cortex [Felleman and Van Essen. THE VENTRAL AREAS 1986]. Area V3 differs from DM in that its visual field map is restricted to the lower visual field and Following corpus callosum section in Aotus there its shape is more stretched out along its common is a clear-cut band of degeneration extending across border with the second visual area (see Fig. 32). the ventral surface of the anterior occipital lobe Area V3's dense myelination and input from Brod­ that corresponds to the vertical meridian represen­ mann's layer 4B in striate cortex links this area tation separating the ventral posterior (VP) from with the magnoceilular system [Van Essen. 1985]. the ventral anterior (VA) visual areas (see Figs. Adjacent to V3 is another area termed V3A [Van 31. 33. 37) [Newsome and Allman. 1980). In the Essen and Zeki. 1978] that contains both an upper original studies of this region, all of the receptive and lower visual field representation and may cor­ fields were located in the upper field; however, in Visual Cortex in Primates 315 A. 78-3 VENTRAL VIEW

B. 72-3.43 VENTRAL VIEW

c. D.

~ ~§ ANT. Fig. 37. Comparison of anatomical results with and the unshaded receptive fields are in VP and VA. physiological data for the ventral surface of owl Note the progression of receptive fields from the monkey visual cortex. A. The pattern of degenera­ horizontal meridian (recording site 5) at the V2- VP tion on the ventral surface of owl monkey 78-3. border to the vertical meridian (recording site 8) at Heavy degeneration is solid black. moderate degen­ the VP·VA border. D. Receptive fields for recording eration is represented by the large dots. and light sites 12-14. Note the change in scale between C and degeneration by the small dots. B. Electrophysiolog­ D. Recording site 12. near the VP-VA boundary. ieal recording sites (1-14) on the ventral surface of yielded a receptive field very near the vertical merid­ owl monkey 72-343 (Allman and Kaas, unpublished ian. The physiological representations of the vertical observations). The location of the recording sites is mendian illustrated in B appear remarkably similar based on a histological reconstruction of the elec­ to the distinct bands of callosal degeneration in A trode tracks superimposed on a photograph of the (solid arrows). The data of C and D also illustrate ventral surface taken postmortem. Open circles de­ the progression from representation of the center-of­ note the vertical meridian representations and the gaze laterally to representation of the periphery me­ solid squares signify the horizontal meridian repre­ dially. 00. optic disk; VA. ventral anterior area; sentation. Dashed lines represent uncertain bounda­ VP. ventral posterior area: V 1. first visual area. or ries. Scale in A and B = 2 mm. C. Receptive fields striate cortex; V2. second visual area. Reproduced for recording sites I-II. The black receptive field is from Newsome and Allman [1980], with permission. in VI. the gray-shaded receptive fields are in V2. 316 Allman and McGuinness

Afferents Corttco- cortical Thalama-cortical

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m *:Jf''''''":J:f,'OU','' IU b#4:>f,"tWU<)... • .• ~"Q')'~:d~"bi ""41,.-.,,,,&;1",,­ I: ?1ilI :f'.};;P!. Wiliii?a]{t I ~ ~?S1~,*\~!.;;*.7 ¥.~~t!~~..~}.~i. VI r>:;t1is\1} ?';;·?)f.$1U~ Vi VI-VII.MT VII-VI M-VII.Ol. MT-VI LGN-VI PUL-VII* PUl-VI VI-DLDM. PP-OM MT.DM. PUL-Ext ..... MT.FE 01 striate DM-MtOL. M MT-OLPf'. M.FE PP-MT.Dl. M.DM. FE Efferents

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.••• j •••••; •.,.;. :. :.;.;.:••':;:! i.:;: •.: .....;.;.;.;••:.:.; ':.:))(::~.: VI-LGN VI-SC.PUl Oth_ VIl-PUl Fig. 38. Laminar patterns of afferent tenmnations resent efferent cells of origin. Reproduced from and efferent neurons for visual areas of conex. Small Weller and Kaas [1981 J. with permission. dots indicate projections into conex: larger dOL~ rep- a more extensive mapping study in progress in our [Burkhalter and Van Essen, 1982]; conversely the laboratory, there is evidence for a considerable incidence of directionally selective cells is three region of lower field representation on the ventral times as high (40%) in V3 as in VP (13%) [FeUe­ surface [Sereno et ai, 1986]. Following corpus man and Van Essen, 19871. callosum section in Macaca there also is a clear­ The discovery of a high incidence of color­ cut line of degeneration extending across that lobe selective neurons in VP is particularly interesting with a similarly organized ventral posterior area in view of color-vision deficits resulting from ven­ [Newsome et ai, 1986]. It is not clear at present tral occipital lesions in humans. Damasio et aI whether area VA is a separate representation or a [19801 described a very carefully documented case ventral extension of the V4 complex. of hemiachromo.lopsia resulting from such a le­ Area VP. which has been considered to be a sion. Their patient "was unable to recognize or detached ventral part of V3 by some authors [Gat­ name any color in any portion of the left field of tass et ai, 1984; Ungerleider et ai, 1983J, differs either eye, including bright reds, blues, greens and from V3 in a number of significant respects [Van yellows. As soon as any portion of the colored Essen, 1985]. First, V3 recives an input from object crossed the vertical meridian, he was able striate cortex; VP does not [Burkhalter and Van to recognize and accurately name its color. When Essen, 1983; Burkhalter et ai, 1986]. Second, V3 an object such as a large red flashlight was held so is densely myelinated; VP is not [Van Essen. 1985; that it was bisected by the vertical meridian, he Felleman and Van Essen, 1986]. Third, corpus reported that the hue of the right half appeared callosum connections crisply defme the anterior normal while the left half was gray. Except for the border of vp. but not V3 [Van Essen. 1985]. achromatopsia, he noted no other disturbance in Fourth, in quantitative studies of response proper­ the appearance of objects (Le. objects did not ties, the incidence of color-selective neurons is change in size or shape. did not move abnonnally, three times as high (60%) in VP as in V3 (21 %) and appeared in correct perspective). Depth per­ Visual Cortex in Primates 317 ception in the colorless field was normal. The mann's layer IVb to actually be part of layer m visual acuity was 20/20 in each eye." The patient (Hasler, 1967; Spatz, 1975, 1977; Tigges et al, had a small left upper visual field scotoma, but 1977; Weller and K.a.as, 1981, and see Fig. 38; apart from this, had no other neurological abnor­ Diamond et al, 1985).] The visual cortex treats the mality. A CAT scan revealed a well-defined lesion amygdala as a higher cortical area; the projections due to a stroke in the ventral part of the right from the inferior temporal cortex arise largely occipital lobe, primarily in extrastriate cortex. A from layer ill and the amygdalar projections back similar case of hemiachromatopsia was reported onto visual cortex terminate at the border between by Verrey [1888} that resulted from a contralateral layers I and n [Amaral and Price, 1984]. ventral occipital lesion confirmed by autopsy. Da­ masio et al [1980} concluded: "judging from case EVOLurION OF CORTICAL VISUAL AREAS 1 and in Verrey's case, one single area in each hemisphere controls color processing of the entire It has been proposed that new cortical areas hernifield. This is so regardless of the fact that resulted from major genetic mutations that pro­ such an area is eccentrically located, in the lower duced replicas of preexisting areas, which was visual association cortex, classically related to up­ followed in subsequent generations by a series of per quadrant processing only. The remarkable minor mutations that produced the gradual diver­ finding further supports the view that visual pro­ gence of structure and function of the replicated cessing is organized in parallel, proceeding through areas [Allman and Kaas, 1971a; see Allman, 1987. specific and preassigned structures. The classic for review]. This general idea of genetic replica­ concept of a concentrically organized visual asso­ tions as a source of evolutionary novelty was first ciation cortex no longer appears tenable." Since a advanced by Bridges in 1918 as a result of gene ventral lesion is unlikely to have damaged the mapping experiments in the giant chromosomes of lower field representation in V -II. it is probable Drosophila. Bridges [1935] later remarked: "In that it affected an area containing both an upper my first report on duplications at the 1918 meeting and lower field representation anterior to V-II. of the A.A.A.S., I emphasized the point that the These results suggest that one or more of the main interest in duplications lay in their offering a ventral areas contains a complete map of the visual method for evolutionary increase in lengths of field and is involved in the perception of color in chromosomes with identical genes which could humans. subsequently mutate separated and diversify their effects." Lewis [1951] and 0000 [1970] extended this concept by pointing out that duplicated genes THE LAMINAR CONNECIlONS OF ASCENDING escape the pressure of natural selection operating AND DESCENDING SYSTEMS on the original gene and thereby can accumulate Many authors have noted that the apparent di­ mutations that enable the new gene to perform rection of information flow in visual cortex is previously nonexistent functions, while the old correlated with the lamina of origin of the neurons gene continues to perform its original and presum­ and the lamina of termination in the target area ably vital functions. It is now well documented [Tigges et al, 1977; Rockland and Pandya, 1979: that gene duplication is probably the most impor­ Weller and Kaas, 1981; Maunsell and Van Essen, tant mechanism for generating new genes and new 1983b}. In general, ascending projections originate biochemical processes [Britten and Kohne, 1968; in layers n and ill and terminate in layer IV of the Li, 1983]. It is likely that analogous processes target area; feedback projections tend to avoid have occurred in the evolution of the cortical vi­ layer IV and prefer layers I and VI; layer V pro­ sual areas. A number of cortical structures share jects subcortically; layer VI is the source of feed­ similar anatomical location. connections, and vi­ back to lower areas (see Fig. 38). [The connec­ suotopic organization in different primate species tions of area MT are a partial exception to these and therefore are very likely to be homologous; rules in that the projection arises from Brodmann's nevertheless they may be functionally quite differ­ layer IVb and the deeper part of layer V and ent. For example, in Macaca the cytochrome oxi­ feedback from MT returns to these layers. This dase "blobs" and area VP are rich in color­ may reflect the anatomical and functional discrete­ selective processes, yet both structures are present ness of this system. Some authors consider Brod- in the nocturnal Aot/lS, where the color mecha­ 318 Allman and McGuinness nisms are unlikely to be well developed. A careful to map homologous systems of connections among comparative examination of the response proper­ cortical visual areas in different primate species, ties of neurons in these structures could reveal including our own. which functions these structures have in common Finally, the ability to map stimulus-evoked and which have emerged since these structures changes in local cerebral blood flow with positron originally developed in their common ancestor. emission tomography (PET scanning) has opened many new possibilities in the study of human vi­ sual cortex. An important feature of this technique NEW METHODS FOR THE sruDY is that local cerebral blood flow changes resulting OF VISUAL CORTEX from different stimulus conditions, as well as un­ Recently several powerful new methods. mono­ stimulated control conditions recorded in the same clonal antibody technology and positron emission experimental session, can be compared quantita­ tomography, have been applied to the study of the tively. In an initial study of the retinotopic organi­ organization of visual cortex. These new methods zation of primary visual cortex, a resolution of promise to be particularly useful in studying the about 3 millimeters was achieved and the data visual cortex in our own species. revealed remarkable consistency in the cortical Hockfield and colleagues [1983] have developed . locations activated by retinotopic stimuli in all six a monoclonal antibody (Cat-3ot) that binds to neu­ subjects tested [Fox et al, 1986]. In this study rons at various levels in the magnocellular system macular stimulation also resulted in activation of a in macaque monkeys, including the magnocellular region on the lateral aspect of the occipital lobe, laminae in the lateral geniculate nucleus. layer IVb possibly corresponding to the conjunction of areas in striate cortex. the thick stripes in the second V 4 and MT. and an additional focus in posterior visual area. and area MT [De Yoe et al. 1986J. parietal cortex that may be related to visual fIXa­ Tootell and Hockfield [personal communication] tion [Fox et al, 1987]. A new scanner now being have used Cat-3ot binding in conjunction with tested at Washington University may provide a staining for cytochrome oxidase activity and fibers significant improvement in resolution, possibly to to map the organization and extent of the thick the range of 1 to 2 millimeters. Thus it appears to stripes in V-II in human visual cortex obtained be possible to map the retinotopic and functional from autopsies. organization of visual cortex in our own species. McDonald, Thai. and Allman [1986] have de­ veloped monoclonal antibodies that selectively bind ACKNOWLEDGMENTS to fiber pathways associated with area MT in the owl monkey. These monoclonal antibodies were This work was supported by NIH grants EY­ generated by using a differential immunosuppres­ 03851 and RR-07003. sive technique [Matthew and Patterson, 1983] in which mice were immunized with frontal cortex, followed by immunosuppression with cyclophos­ REFERENCES phamide. and then immunized with tissue from Aggleton, J.P.; Burton. M.J.; Passingham. R.E. Corti­ area MT. This approach suppressed common brain eaI and subcortical afferents to the amygdala of the antigens and allowed for the selection of antigens rhesus monkey (Macaca mulatta). BRAIN RE­ specific to area MT. One particularly interesting SEARCH 190:347-368. 1980. monoclonal antibody (2E 10) appears to be associ­ Albright. T.O. Direction and orientation selectivity of ated with the fiber pathway connecting MT with neurons in visual area MT of the macque. JOUR­ the ventral visual areas VP and VA. It is intriguing NAL OF NEUROPHYSIOLOGY 52:1106-1130, that thus far this differential immunosuppressive 1984. method has yielded only monoclonal antibodies Allman, J. Evolution of the visual system in the early that appear to bind mainly to fiber pathways rather primates. PROGRESS IN PSYCHOBIOLOGY AND PHYSIOLOGICAL PSYCHOLOGY 7:1-53, 1977. than cortical neurons. This may be due to technical Allman, J. Reconstructing the evolution of the brain in factors; however, it may also be that what is unique primates through the use of comparative neurophys­ about a particular cortical area is its set of connec­ iological and neuroanatomical data. pp. 13-28 in tions with other brain structures. 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