Representation of central and peripheral vision in the primate cerebral cortex: Insights from studies of the marmoset brain.

How the visual field is represented by neurons in the cerebral cortex is one of the most basic questions in visual neuroscience. However, research to date has focused heavily on the small part of the visual field within, and immediately surrounding the fovea. Studies on the cortical representation of the full visual field in the primate brain are still scarce. We have been investigating this issue with electrophysiological and anatomical methods, taking advantage of the small and lissencephalic marmoset brain, which allows easy access to the representation of the full visual field in many cortical areas. This review summarizes our main findings to date, and relates the results to a broader question: is the peripheral visual field processed in a similar manner to the central visual field, but with lower spatial acuity? Given the organization of the visual cortex, the issue can be addressed by asking: (1) Is visual information processed in the same way within a single cortical area? and (2) Are different cortical areas specialized for different parts of the visual field? The electrophysiological data from the primary visual cortex indicate that many aspects of spatiotemporal computation are remarkably similar across the visual field, although subtle variations are detectable. Our anatomical and electrophysiological studies of the extrastriate cortex, on the other hand, suggest that visual processing in the far peripheral visual field is likely to involve a distinct network of specialized cortical areas, located in the depths of the calcarine sulcus and interhemispheric fissure.

A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision.

We defined cortical areas involved in the analysis of motion in the far peripheral visual field, a poorly understood aspect of visual processing in primates. This was accomplished by small tracer injections within and around the representations of the monocular field of vision ('temporal crescents') in the middle temporal area (MT) of marmoset monkeys. Quantitative analyses demonstrate that the representation of the far periphery receives specific connections from the retrosplenial cortex (areas 23v and prostriata), as well as comparatively stronger inputs from the primary visual area (V1) and from areas surrounding MT (in particular, the medial superior temporal area, MST). In contrast, the far peripheral representation receives little or no input from most other extrastriate areas, including the second visual area (V2), the densely myelinated areas of the dorsomedial cortex, and ventral stream areas; these areas are shown to have robust projections to other parts of MT. Our results demonstrate that the responses of cells in different parts of a same visual area can be determined by different combinations of synaptic inputs, in terms of areas of origin. They also suggest that the interconnections responsible for motion processing in the far periphery of the visual field convey information that is crucial for rapid-response aspects of visual function such as orienting, postural and defensive reactions.

Visual thalamocortical projections in the flying fox: parallel pathways to striate and extrastriate areas.

We studied thalamic projections to the visual cortex in flying foxes, animals that share neural features believed to resemble those present in the brains of early primates. Neurones labeled by injections of fluorescent tracers in striate and extrastriate cortices were charted relative to the architectural boundaries of thalamic nuclei. Three main findings are reported: First, there are parallel lateral geniculate nucleus (LGN) projections to striate and extrastriate cortices. Second, the pulvinar complex is expansive, and contains multiple subdivisions. Third, across the visual thalamus, the location of cells labeled after visual cortex injections changes systematically, with caudal visual areas receiving their strongest projections from the most lateral thalamic nuclei, and rostral areas receiving strong projections from medial nuclei. We identified three architectural layers in the LGN, and three subdivisions of the pulvinar complex. The outer LGN layer contained the largest cells, and had strong projections to the areas V1, V2 and V3. Neurones in the intermediate LGN layer were intermediate in size, and projected to V1 and, less densely, to V2. The layer nearest to the origin of the optic radiation contained the smallest cells, and projected not only to V1, V2 and V3, but also, weakly, to the occipitotemporal area (OT, which is similar to primate middle temporal area) and the occipitoparietal area (OP, a "third tier" area located near the dorsal midline). V1, V2 and V3 received strong projections from the lateral and intermediate subdivisions of the pulvinar complex, while OP and OT received their main thalamic input from the intermediate and medial subdivisions of the pulvinar complex. These results suggest parallels with the carnivore visual system, and indicate that the restriction of the projections of the large- and intermediate-sized LGN layers to V1, observed in present-day primates, evolved from a more generalized mammalian condition.

Single-unit responses to kinetic stimuli in New World monkey area V2: physiological characteristics of cue-invariant neurones.

In order to investigate the neural processes underlying figure-ground segregation on the basis of motion, we studied the responses of neurones in the second visual area (V2) of marmoset monkeys to stimuli that moved against dynamic textured backgrounds. The stimuli were either "solid" bars, which were uniformly darker or lighter than the background's average, or kinetic ("camouflaged") bars, formed by textural elements that matched the spatial and temporal modulation of the background. Camouflaged bars were rendered visible only by the coherent motion of their textural elements. Using solid bars, we subdivided the population of marmoset V2 neurones into motion-selective (uni- and bi-directional units, 73.3% of the sample) and weakly-biased (26.7%) subpopulations. The motion selective subpopulation was further subdivided into cue-invariant neurones (units which demonstrated a similar selectivity for the direction of motion of the solid and camouflaged bars) and non-cue-invariant neurones (units which showed selectivity to the direction of motion of solid bars, but had weak or pandirectional responses to camouflaged bars). Cells with cue-invariant responses to these stimuli were as common in V2 as in the primary visual area (V1; approximately 40% of the population). In V2, neurones with cue-invariant and non-cue-invariant motion selectivity formed distinct populations in terms of classical response properties: cue-invariant neurones were characterized by a sharp axis of motion selectivity and extensive length summation, while the majority of non-cue-invariant neurones had broader motion selectivity and were end-stopped. In the light of previous studies, these different constellations of classical response properties suggest a correlation with more traditionally recognized categories of V2 units and modular compartments. The responses of V2 cells to kinetic stimuli were slightly delayed relative to their responses to luminance-defined stimuli.

First- and second-order stimulus length selectivity in New World monkey striate cortex.

Motion is a powerful cue for figure-ground segregation, allowing the recognition of shapes even if the luminance and texture characteristics of the stimulus and background are matched. In order to investigate the neural processes underlying early stages of the cue-invariant processing of form, we compared the responses of neurons in the striate cortex (V1) of anaesthetized marmosets to two types of moving stimuli: bars defined by differences in luminance, and bars defined solely by the coherent motion of random patterns that matched the texture and temporal modulation of the background. A population of form-cue-invariant (FCI) neurons was identified, which demonstrated similar tuning to the length of contours defined by first- and second-order cues. FCI neurons were relatively common in the supragranular layers (where they corresponded to 28% of the recorded units), but were absent from layer 4. Most had complex receptive fields, which were significantly larger than those of other V1 neurons. The majority of FCI neurons demonstrated end-inhibition in response to long first- and second-order bars, and were strongly direction selective. Thus, even at the level of V1 there are cells whose variations in response level appear to be determined by the shape and motion of the entire second-order object, rather than by its parts (i.e. the individual textural components). These results are compatible with the existence of an output channel from V1 to the ventral stream of extrastriate areas, which already encodes the basic building blocks of the image in an invariant manner.

Visual maps in the adult primate cerebral cortex: some implications for brain development and evolution

In this paper, the topology of cortical visuotopic maps in adult primates is reviewed, with emphasis on recent studies. The observed visuotopic organisation can be summarised with reference to two basic rules. First, adjacent radial columns in the cortex represent partially overlapping regions of the visual field, irrespective of whether these columns are part of the same or different cortical areas. This primary rule is seldom, if ever, violated. Second, adjacent regions of the visual field tend to be represented in adjacent radial columns of a same area. This rule is not as rigid as the first, as many cortical areas form discontinuous, second-order representations of the visual field. A developmental model based on these physiological observations, and on comparative studies of cortical organisation, is then proposed, in order to explain how a combination of molecular specification steps and activity-driven processes can generate the variety of visuotopic organisations observed in adult cortex

Visual maps in the adult primate cerebral cortex: some implications for brain development and evolution.

In this paper, the topology of cortical visuotopic maps in adult primates is reviewed, with emphasis on recent studies. The observed visuotopic organisation can be summarised with reference to two basic rules. First, adjacent radial columns in the cortex represent partially overlapping regions of the visual field, irrespective of whether these columns are part of the same or different cortical areas. This primary rule is seldom, if ever, violated. Second, adjacent regions of the visual field tend to be represented in adjacent radial columns of a same area. This rule is not as rigid as the first, as many cortical areas form discontinuous, second-order representations of the visual field. A developmental model based on these physiological observations, and on comparative studies of cortical organisation, is then proposed, in order to explain how a combination of molecular specification steps and activity-driven processes can generate the variety of visuotopic organisations observed in adult cortex.

Cortical streams of visual information processing in primates

1. The topographic organization of the cortical visual areas in the Cebus monkey and their anatomical connections support the subdivision of the visuaol pathways into ventral and dorsal streams of visual information provessing. 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 across different visual areas

Pattherns of cytochrome oxidase activity in the visual cortex of a South American opossum

The normal pattern of cytochrome oxidase (CO) activity in the posterior cortical areas of the South American opossum (Didelphis marsupialis aurita) was assessed both in horizontal section of flattened cortices and in transversal cortical sextions. the tangential distribution of CO activity was uniformly high in the strate cortex. In the peristriate region alternating bands of dense and weak staining occupied all the cortical layers with the exception of layer I. This observation suggests the existence of a functional segregation of visual processing in the peristriate cortex of the opossum similar to that present in phylogenetically more recent groups