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Gattass and collaborators (Gattass R, Rosa MGP, Souza APB, Piñon MCG, Neuenschwander S [1990a] Braz J Med Biol Res 23:375-393) proposed that the dorsal stream of visual processing, as defined by Ungerleider and Mishkin (Ungerleider LG, Mishkin M [1982] In: Ingle DJ, Goodale MA, Mansfield RJW, editors. Analysis of visual behavior. Cambridge: Massachusetts Institute of Technology. p 549-586), can be subdivided into dorsolateral and dorsomedial streams, and suggested that they may be involved in different aspects of the processing of motion and spatial perception, respectively. The goal of the present study was to provide additional evidence for this hypothesis by using cytochrome oxidase immunohistochemistry combined with retrograde tracing techniques. In Old World monkeys, the locations of visual area 4 (V4; ventral stream) and middle temporal area (MT; dorsal stream) projecting neurons in V2 supports the hypothesis that the cytochrome oxidase (CytOx)-rich thin stripes and the CytOx-poor interstripes are associated with the ventral stream, and that the CytOx-rich thick stripes belong to the dorsal stream. In this study we describe, in the New World monkey Cebus, the distribution of retrogradely labeled cells in V2 relative to the CytOx compartments after fluorescent tracers were placed in areas V4, MT, and the parietooccipital area (PO). We found PO-projecting neurons in CytOx-rich thick stripes and CytOx-poor interstripes in V2, whereas MT-projecting neurons appeared almost exclusively in thick stripes. In contrast, V4-projecting neurons were located mostly in CytOx-poor interstripes and CytOx-rich thin stripes. In addition, V4- and MT-projecting neurons were located mainly in supragranular layers, whereas PO-projecting neurons were located in supragranular and infragranular layers. These results support the hypothesis for the existence of three distinct streams of visual processing: ventral (including V4), dorsolateral (including MT), and dorsomedial (including PO)., (Copyright 2003 Wiley-Liss, Inc.)

The ventral extrastriate cortex adjacent to the second visual area was studied in the New World monkey Cebus apella, using anaesthetised preparations. The visuotopic organisation and myeloarchitecture of this region demonstrate the existence of a distinct strip of cortex, 3-4 mm wide, with an ordered representation of the contralateral upper visual quadrant, up to 60 degrees eccentricity. This upper-quadrant representation is probably homologous to the ventral subdivision of the third visual complex (V3v) of Old World monkeys, also known as the ventral posterior area. The representation of the horizontal meridian in V3v forms its posterior and medial border with V2, while the upper vertical meridian is represented anterior and laterally, forming a congruent border with the fourth visual area (V4). Central visual fields are represented in posterior and lateral portions of V3v, in the inferior occipital sulcus, while the periphery of the visual field is represented anteriorly, on the tentorial surface. Cortex anterior to V3v, at the ventral occipitotemporal transition, had neurones that had poor visual responses. No representation of the lower quadrant was found adjacent to V3v in ventral cortex. However, we observed cells with perifoveal receptive fields centred in the lower quadrant immediately dorsal to V3v, around the junction of the inferior occipital and lunate sulci. These observations argue against the idea that V3v is an area restricted to the ventral cortex in New World monkeys and support the conclusions of previous anatomical studies in Cebus that showed a continuity of myeloarchitecture and connectional patterns between ventral and lateral extrastriate cortices. Together, these data suggest that V3v may be part of a larger area that extends into dorsolateral extrastriate cortex, overlapping to some extent with the caudal subdivision of the dorsolateral area described in other New World monkeys.

We used electrophysiological mapping and myeloarchitectural criteria in order to define the location, extent and visual topography of the fourth visual area (V4) in anesthetized and paralyzed Cebus monkey. Based on these criteria, the borders of V4 with surrounding areas were defined both on the dorsal and ventral cortical surfaces. In addition, to better visualize the visuotopic organization and to evaluate its regularity, we constructed bidimensional maps and projected the recording sites onto them. Area V4 has an almost complete representation of the binocular visual field with the lower visual field represented dorsally (V4d) and the upper field ventrally (V4v). We found this representation to be more extensive than those previously described. The representation of the central portion of the visual field is largely expanded in comparison with that of the periphery. This emphasis in central vision could be related with the involvement of V4 in the ventral stream of visual information processing. Receptive field size increases with increasing eccentricity, while cortical magnification factor decreases. The cortical magnification factor measured along isopolar lines is, on average, 1.5-2.0 times greater than that measured along the isoeccentric lines, suggesting the existence of a small anisotropy in central and peripheral V4.

Two visual areas of the anterior bank of the parietooccipital sulcus, areas PO and POd, were identified and their visual field representations were studied in six anesthetized and paralyzed Cebus monkeys. The definition of these areas was based on electrophysiological mapping and myeloarchitecture. PO is located in the ventral aspect of the anterior bank of the parietooccipital sulcus and ventral precuneate gyrus. It borders area V2 posteriorly and ventrally in the depth of the parietooccipital sulcus, area V3d laterally, and another undescribed visual area medially. POd was located dorsal to area PO and ventral to architectonic area PE. The representations of the visual field in areas PO and POd are complex. In each hemisphere, these areas have a virtually complete representation of the contralateral visual hemifield. Different from the previously described visual areas, in PO and POd there is a precise organization of isopolar lines and a complex organization of the isoeccentric ones. In PO, as well as in POd, the representation of the horizontal meridian runs dorsoventrally along the parietooccipital sulcus. The upper visual quadrant is represented medially and the lower visual quadrant laterally. A large and complex representation of the periphery, from 20 degrees to 60 degrees eccentricity is present at the lateral and medial portions of these areas. By contrast, the representation of the central 20 degrees is very small in both PO and POd. The central visual field is represented ventrally in PO and dorsally in area POd. Area POd shows a more stratified myeloarchitectonic pattern than PO and both areas can be distinguished from other surrounding areas by their heavier myelinated pattern.

Cortical afferents to area V1 were studied in seven Cebus monkeys by means of retrograde fluorescent tracers. Injections were placed in V1, under electrophysiological guidance, in the regions of representation of both the upper and lower visual quadrants, at eccentricities that ranged from 0.5 to 64 degrees. In all cases retrogradely filled neurons were found in retinotopically corresponding portions of areas V2 and MT, as defined electrophysiologically (Rosa et al: J. Comp. Neurol. 275:326, 1988; Fiorani et al: J Comp Neurol 287:98, 1989). The results also revealed two other visual zones located anterior to V2 here named third and fourth visual areas. A topographical organization of the connections was observed in these areas, with upper quadrant located ventrally and lower quadrant located dorsally. A clear central-peripheral gradient, from the lateral to the medial cortical surface, was also observed in these areas. Lower field injections revealed crude topographic organization in area DZ and a diffuse projecting zone in the annectent gyrus. Peripheral injections in V1 revealed a clear upper and lower field segregation in areas PO and prostriata as well as a complex topography in MST. In addition, another region of labeling revealed the presence of an area, the temporal ventral posterior region, with an organized topographic representation of the upper field, with a central to peripheral gradient, from the lateral to the medial cortical surface. Three groups of cortical areas were distinguished according to the laminar distribution of neurons labeled from V1. In the first group, which is characterized by dense infra- and supragranular labeling, only V2 was included. The second group consists of areas V3, MT, and PO. These areas show dense labeling in the infragranular layers and occasionally sparse labeling in the supragranular layers. Finally, V4 and the other projecting areas, which are characterized by exclusive labeling of the infragranular layers were included in the third group.

1. The topographic organization of the cortical visual areas in the Cebus monkey and their anatomical connections support the subdivision of the visual pathways into ventral and dorsal streams of visual information processing. 2. We propose that the dorsal stream, as defined by Ungerleider and Mishkin (In: Ingle DJ, Goodale MA and Mansfield RJW (Editors), Analysis of Visual Behavior. MIT Press, Boston, 1982), be subdivided into dorsolateral and dorsomedial streams, which are concerned with different aspects of the processing of motion and spatial perception. 3. The data support the hypothesis of concurrent, modular processing of visual attributes in cortical visual areas in the different streams, and highlight some features of the visual field representation in each area which may reflect functional specialization of these streams. 4. The visual topography is locally disrupted in some cortical areas by the existence of functionally different modules. However, a global visuotopic organization is preserved in most areas. 5. The visuotopic organization may provide the address of space coordinates to integrate information concerning the same retinotopic locus across different visual areas.

The representation of the visual field in the dorsal portion of the superior temporal sulcus (ST) was studied by multiunit recordings in eight Cebus apella, anesthetized with N2O and immobilized with pancuronium bromide, in repeated recording sessions. On the basis of visuotopic organization, myeloarchitecture, and receptive field size, area MT was distinguished from its neighboring areas. MT is an oval area of about 70 mm2 located mainly in the posterior bank of the superior temporal sulcus. It contains a visuotopically organized representation of at least the binocular visual field. The representation of the vertical meridian forms the dorsolateral, lateral, and ventrolateral borders of MT and that of the horizontal meridian runs across the posterior bank of ST. The fovea is represented at the lateralmost portion of MT, while the retinal periphery is represented medially. The representation of the central visual field is magnified relative to that of the periphery in MT. The cortical magnification factor in MT decreases with increasing eccentricity following a negative power function. Receptive field size increases with increasing eccentricity. A method to evaluate the scatter of receptive field position in multiunit recordings based on the inverse of the magnification factor is described. In MT, multiunit receptive field scatter increases with increasing eccentricity. As shown by the Heidenhain-Woelcke method, MT is coextensive with two myeloarchitectonically distinct zones: one heavily myelinated, located in the posterior bank of ST, and another, less myelinated, located at the junction of the posterior bank with the anterior bank of ST. At least three additional visual zones surround MT: DZ, MST, and FST. The areas of the dorsal portion of the superior temporal sulcus in the diurnal New World monkey Cebus are comparable to those described for the diurnal Old World monkey, Macaca. This observation suggests that these areas are ancestral characters of the simian lineage and that the differences observed in the owl monkey may be secondary adaptations to a nocturnal ecological niche.

The representation of the visual field in the striate cortex (V1) was mapped with multiunit electrodes in the Cebus monkey. Nine Cebus apella, anesthetized with N2O and immobilized with pancuromium bromide were studied in repeated recording sessions. In each hemisphere, V1 contains a continuous representation of the contralateral visual hemifield. The representation of the vertical meridian (VM) forms the external border of V1 except at the anteriormost portion of the calcarine fissure. The representation of the horizontal meridian (HM) divides the area so that the representation of the lower visual field is located dorsally, and that of the upper field ventrally. The convoluted surface of V1 can be only partially unfolded, and no precise "flattened" map can be obtained without introducing surface discontinuities. The visual topography of V1 is presented in a series of coronal sections and in "flattened" maps. The representation of the central visual field is magnified relative to that of the periphery in V1. The evaluation of the cortical magnification factors measured along isoeccentric and isopolar dimensions in the partially unfolded model of V1 revealed anisotropies in the representation of the visual field with larger magnification along isopolar lines than along isoeccentric lines. Receptive field size increases with increasing eccentricity, whereas point image size decreases with increasing eccentricity.

The representation of the visual field in areas V3 and V4 of the macaque was mapped with multiunit electrodes. Twelve Macaca fascicularis were studied in repeated recording sessions while immobilized and anesthetized. V3 is a narrow strip (4-5 mm wide) of myeloarchitectonically distinct cortex located immediately anterior to V2. It contains a systematic representation of the central 35-40 degrees of the contralateral visual field; the representation of the upper quadrant is located ventrally in the hemisphere and that of the lower quadrant, dorsally. There is a small gap between the dorsal (V3d) and ventral (V3v) portions of V3. The representation of the horizontal meridian is adjacent to that in V2 and forms the posterior border of both V3d and V3v. Most or all of the anterior border of V3d consists of the representation of the lower vertical meridian. The entire anterior border of V3v consists of the representation of the upper vertical meridian. V4 is a strip of myeloarchitectonically distinct cortex 5-8 mm wide, immediately anterior to V3. It contains a coarse, but systematic, representation of approximately the central 35-40 degrees of the contralateral visual field. The representation of the upper visual field is located ventrally in the hemisphere. Most of the representation of the lower visual field is located dorsally. The posterior border of V4 corresponds to the representation of the vertical meridian, and the representation of the horizontal meridian is located at or near its anterior border. In both V3 and V4, the representation of the central visual field is magnified relative to that of the periphery. In both areas, the size of receptive fields increases with increasing eccentricity; however, at a given eccentricity, the receptive fields of V4 are larger than those of V3.

The projection of the visual field in the pulvinar nucleus was studied in 17 Cebus monkeys using electrophysiological techniques. Visual space is represented in two regions of the pulvinar; (1) the ventrolateral group, Pvlg, comprising nuclei P delta, P delta, P gamma, P eta and P mu 1; and (2) P mu. In the first group, which corresponds to the pulvinar inferior and ventral part of the pulvinar lateralis, we observed a greater respresentation of the central part of the visual field. Approximately 58% of the volume of the ventrolateral group is concerned with the visual space within 10 degrees of the fovea. This portion of the visual field is represented at its lateral aspects, mainly close to the level of the caudal pole of the lateral geniculate nucleus (LGN). Projection of the vertical meridian runs along its lateral border while that of the horizontal one is found running from the dorsal third of the LGN's hilus to the medial border of the ventro-lateral group. The lower quadrant is represented at its dorsal portion while the upper quadrant is represented at the ventral one. In Pmu the representation is rotated 90 degrees clockwise around the rostrocaudal axis: the vertical meridian is found at the ventromedial border of this nucleus. Thus, the lower quadrant is represented at the later portion of Pmu and the upper at its medial portion. Both projections are restricted to the contralateral hemifield.