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.
We have examined the origin and topography of cortical projections to area PO, an extrastriate visual area located in the parieto-occipital sulcus of the macaque. Distinguishable retrograde fluorescent tracers were injected into area PO at separate retinotopic loci identified by single-neuron recording. The results indicate that area PO receives retinotopically organized inputs from visual areas V1, V2, V3, V4, and MT. In each of these areas the projection to PO arises from the representation of the periphery of the visual field. This finding is consistent with neurophysiological data indicating that the representation of the periphery is emphasized in PO. Additional projections arise from area MST, the frontal eye fields, and several divisions of parietal cortex, including four zones within the intraparietal sulcus and a region on the medial dorsal surface of the hemisphere (MDP). On the basis of the laminar distribution of labeled cells we conclude that area PO receives an ascending input from V1, V2, and V3 and receives descending or lateral inputs from all other areas. Thus, area PO is at approximately the same level in the hierarchy of visual areas as areas V4 and MT. Area PO is connected both directly and indirectly, via MT and MST, to parietal cortex. Within parietal cortex, area PO is linked to particular regions of the intraparietal sulcus including VIP and LIP and two newly recognized zones termed here MIP and PIP. The wealth of connections with parietal cortex suggests that area PO provides a relatively direct route over which information concerning the visual field periphery can be transmitted from striate and prestriate cortex to parietal cortex. In contrast, area PO has few links with areas projecting to inferior temporal cortex. The pattern of connections revealed in this study is consistent with the view that area PO is primarily involved in visuospatial functioning.
The representation of the visual field in the area adjacent to striate cortex was mapped with multiunit electrodes in the macaque. The animals were immobilized and anesthetized and in each animal 30 to 40 electrode penetrations were typically made over several recording sessions. This area, V2, contains a topographically organized representation of the contralateral visual field up to an eccentricity of at least 80 degrees. The representation of the vertical meridian is adjacent to that in striate cortex (V1) and forms the posterior border of V2. The representation of the horizontal meridian in V2 forms the anterior border of V2 and is split so that the representation of the lower visual field is located dorsally and that of the upper field ventrally. As in V1, the representation of the central visual field is magnified relative to that of the periphery. The area of V2 is slightly smaller than that of V1. At a given eccentricity, receptive field size in V2 is larger than in V1. The myeloarchitecture of V2 is distinguishable from that of the surrounding cortex. The location of V2 corresponds, at least approximately, to that of cytoarchitectonic Area OB. V2 is bordered anteriorly by several other areas containing representations of the visual field.
To determine the locus, full extent, and topographic organization of cortical connections of area V4 (visual area 4), we injected anterograde and retrograde tracers under electrophysiological guidance into 21 sites in 9 macaques. Injection sites included representations ranging from central to far peripheral eccentricities in the upper and lower fields. Our results indicated that all parts of V4 are connected with occipital areas V2 (visual area 2), V3 (visual area 3), and V3A (visual complex V3, part A), superior temporal areas V4t (V4 transition zone), MT (medial temporal area), and FST (fundus of the superior temporal sulcus [STS] area), inferior temporal areas TEO (cytoarchitectonic area TEO in posterior inferior temporal cortex) and TE (cytoarchitectonic area TE in anterior temporal cortex), and the frontal eye field (FEF). By contrast, mainly peripheral field representations of V4 are connected with occipitoparietal areas DP (dorsal prelunate area), VIP (ventral intraparietal area), LIP (lateral intraparietal area), PIP (posterior intraparietal area), parieto-occipital area, and MST (medial STS area), and parahippocampal area TF (cytoarchitectonic area TF on the parahippocampal gyrus). Based on the distribution of labeled cells and terminals, projections from V4 to V2 and V3 are feedback, those to V3A, V4t, MT, DP, VIP, PIP, and FEF are the intermediate type, and those to FST, MST, LIP, TEO, TE, and TF are feedforward. Peripheral field projections from V4 to parietal areas could provide a direct route for rapid activation of circuits serving spatial vision and spatial attention. By contrast, the predominance of central field projections from V4 to inferior temporal areas is consistent with the need for detailed form analysis for object vision.
The representation of the visual field in the striate projection zone in the posterior portion of the superior temporal sulcus of the macaque (MT) was mapped with multiunit electrodes. The animals were immobilized and anesthetized and in each animal 25-35 electrode penetrations were typically made over several recording sessions. 2. MT contains a representation of virtually the entire contralateral visual field. The representation of the vertical meridian forms its ventrolateral border and lies near the bottom of the lower bank of the superior temporal sulcus (STS). The representation of the horizontal meridian runs across the floor of STS. The upper field is located ventral and anterior and the lower field dorsal and posterior. The medial border lies at the junction of the floor of STS and its upper bank. 3. MT is similar to striate cortex in being a first-order transformation of the visual field. In both areas, receptive-field size and cortical magnification increase with eccentricity. MT is much smaller than striate cortex and has much larger receptive fields at a given eccentricity and a cruder topography. 4. The results further support the suggestion that MT in the macaque is homologous to visual area MT in New World primates. METHODS Animal preparation and maintenance Six Macaca fascicularis weighing between 3.0 and 4.8 kg were used. Five were recorded from on eight occasions and one twice. All recordings from an individual animal were made within a 4-0022-3077/8
In addition to the major anatomical pathways from V1 into the temporal lobe, there are other smaller, "bypass" routes that are poorly understood. To investigate the direct projection from V1 to V4 (bypassing V2) and from V2 to TEO (bypassing V4), we injected the foveal and parafoveal representations of V4 and TEO with different retrograde tracers in five hemispheres of four macaques and analyzed the distributions of labeled neurons in V1 and V2 using flattened preparations of the cortex. In V1, labeled neurons were seen after injections in V4 but not TEO. The V4-projecting neurons were located in the foveal representation of V1, in both cytochrome oxidase (CO)-rich blobs and CO-poor interblob regions. In V2, TEO-projecting neurons were intermingled with V4-projecting neurons, although the former were far sparser than the latter. Across the cases, 6-19% of the TEO-projecting neurons were double labeled, that is, also projected to area V4. Both V4- and TEO-projecting neurons formed bands that ran orthogonal to the V1/V2 border, and both were located in CO-rich thin stripes and CO-poor interstripe regions. In some cases, a continuous band of V4-projecting neurons was also found along the V1/V2 border in the foveal representation of V2. The results indicate that the pathways from V1 to V4 and from V2 to TEO involve anatomical subcompartments thought to be concerned with both color and form. These "bypass" routes may allow coarse information about color and form to arrive rapidly in the temporal lobe. The bypass route from V2 to TEO might explain the partial sparing of color and form vision that is seen after lesions of V4. By analogy, given the bypass route from the foveal representation of V1 to V4, lesions of V2 affecting the foveal visual field would also be insufficient to block color and form vision.
The layout of areas in the cerebral cortex of different primates is quite similar, despite significant variations in brain size. However, it is clear that larger brains are not simply scaled up versions of smaller brains: some regions of the cortex are disproportionately large in larger species. It is currently debated whether these expanded areas arise through natural selection pressures for increased cognitive capacity or as a result of the application of a common developmental sequence on different scales. Here, we used computational methods to map and quantify the expansion of the cortex in simian primates of different sizes to investigate whether there is any common pattern of cortical expansion. Surface models of the marmoset, capuchin, and macaque monkey cortex were registered using the software package CARET and the spherical landmark vector difference algorithm. The registration was constrained by the location of identified homologous cortical areas. When comparing marmosets with both capuchins and macaques, we found a high degree of expansion in the temporal parietal junction, the ventrolateral prefrontal cortex, and the dorsal anterior cingulate cortex, all of which are high-level association areas typically involved in complex cognitive and behavioral functions. These expanded maps correlated well with previously published macaque to human registrations, suggesting that there is a general pattern of primate cortical scaling.
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