Feedforward and feedback connections and their relation to the cytox modules of V2 in Cebus monkeys.

To study the circuitry related to the ventral stream of visual information processing and its relation to the cytochrome oxidase (CytOx) modules in visual area V2, we injected anterograde and retrograde cholera toxin subunit B (CTb) tracer into nine sites in area V4 in five Cebus apella monkeys. The injection site locations ranged from 2° to 10° eccentricity in the lower visual field representation of V4. Alternate cortical sections, cut tangentially to the pial surface or in the coronal plane, were stained for CTb immunocytochemistry or for CytOx histochemistry or for Nissl. Our results indicate that the V4-projecting cells and terminal-like labeling were located in interstripes and thin CytOx-rich stripes and avoided the CytOx-rich thick stripes in V2. The feedforward projecting cell bodies in V2 were primarily located in the supragranular layers and sparsely located in the infragranular layers, whereas the feedback projections (i.e., the terminal-like labels) were located in the supra- and infragranular layers. V4 injections of CTb resulted in labeling of the thin stripes and interstripes of V2 and provided an efficient method of distinguishing the V2 modules that were related to the ventral stream from the CytOx-rich thick stripes, related to the dorsal stream. In V2, there was a significant heterogeneity in the distribution of projections: feedforward projections were located in CytOx-rich thin stripes and in the CytOx-poor interstripes, whereas the feedback projections were more abundant in the thin stripes than in the interstripes.

Projection from visual areas V2 and prostriata to caudal auditory cortex in the monkey.

Studies in humans and monkeys report widespread multisensory interactions at or near primary visual and auditory areas of neocortex. The range and scale of these effects has prompted increased interest in interconnectivity between the putatively "unisensory" cortices at lower hierarchical levels. Recent anatomical tract-tracing studies have revealed direct projections from auditory cortex to primary visual area (V1) and secondary visual area (V2) that could serve as a substrate for auditory influences over low-level visual processing. To better understand the significance of these connections, we looked for reciprocal projections from visual cortex to caudal auditory cortical areas in macaque monkeys. We found direct projections from area prostriata and the peripheral visual representations of area V2. Projections were more abundant after injections of temporoparietal area and caudal parabelt than after injections of caudal medial belt and the contiguous areas near the fundus of the lateral sulcus. Only one injection was confined to primary auditory cortex (area A1) and did not demonstrate visual connections. The projections from visual areas originated mainly from infragranular layers, suggestive of a "feedback"-type projection. The selective localization of these connections to peripheral visual areas and caudal auditory cortex suggests that they are involved in spatial localization.

Distribution of neurofilament proteins in the lateral geniculate nucleus, primary visual cortex, and area MT of adult Cebus monkeys.

We investigated the distribution pattern of SMI-32-immunopositive cells in the lateral geniculate nucleus (LGN) and in the primary (V1) and middle temporal (MT) cortical visual areas of the adult New World monkey Cebus apella. In the LGN, the reaction for SMI-32 labeled cells in both the magnocellular (M) and parvocellular (P) layers. However, the cellular label was heavier in M layers, which also showed a more intense labeling in the neuropil. In V1, the reaction showed a lamination pattern, with the heaviest labeling occurring in layer 4B and upper layer 6 (layers that project to area MT). Area MT shows a dense band of labeled neuropil and large pyramidal neurons in layer 3, large darkly labeled but less densely packed neurons in layer 5, and a population of small, lightly labeled cells in layer 6. These results resemble those found in other New and Old World monkeys, which suggest that the preferential labeling of projection neurons associated with fast-conducting pathways to the extrastriate dorsal stream is a common characteristic of simian primates. In the superficial layers of V1 in Cebus monkeys, however, SMI-32-labeled neurons are found in both cytochrome oxidase blobs and interblob regions. In this aspect, our results in Cebus are similar to those found in the Old World monkey Macaca and different from those described for squirrel monkey, a smaller New World Monkey. In Cebus, as well as in Macaca, there is no correlation between SMI-32 distribution and the blob pattern.

Cortical visual areas in monkeys: location, topography, connections, columns, plasticity and cortical dynamics.

The visual system is constantly challenged to organize the retinal pattern of stimulation into coherent percepts. This task is achieved by the cortical visual system, which is composed by topographically organized analytic areas and by synthetic areas of the temporal lobe that have more holistic processing. Additional visual areas of the parietal lobe are related to motion perception and visuomotor control. V1 and V2 represent the entire visual field. MT represents only the binocular field, and V4 only the central 30 degrees-40 degrees. The parietal areas represent more of the periphery. For any eccentricity, the receptive field grows at each step of processing, more at anterior areas in the temporal lobe. Minimal point image size increases towards the temporal lobe, but remains fairly constant toward the parietal lobe. Patterns of projection show asymmetries. Central V2 and V4 project mainly to the temporal lobe, while peripherals V2 (more than 30 degrees) and V4 (more than 10 degrees) also project to the parietal lobe. Visual information that arrives at V1 projects to V2, MT and PO, which then project to other areas. Local lateral propagation and recursive loops corroborate to perceptual completion and filling in. Priority connections to temporal, parietal and parieto-temporal cortices help construct crude early representations of objects, trajectories and movements.

Three streams of visual information processing in V2 of Cebus monkey.

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).