In recent years, many new cortical areas have been identified in the macaque monkey. The number of identified connections between areas has increased even more dramatically. We report here on (1) a summary of the layout of cortical areas associated with vision and with other modalities, (2) a computerized database for storing and representing large amounts of information on connectivity patterns, and (3) the application of these data to the analysis of hierarchical organization of the cerebral cortex. Our analysis concentrates on the visual system, which includes 25 neocortical areas that are predominantly or exclusively visual in function, plus an additional 7 areas that we regard as visual-association areas on the basis of their extensive visual inputs. A total of 305 connections among these 32 visual and visual-association areas have been reported. This represents 31 % of the possible number of pathways if each area were connected with all others. The actual degree of connectivity is likely to be closer to 40%. The great majority of pathways involve reciprocal connections between areas. There are also extensive connections with cortical areas outside the visual system proper, including the somatosensory cortex, as well as neocortical, transitional, and archicortical regions in the temporal and frontal lobes. In the somatosensory/motor system, there are 62 identified pathways linking 13 cortical areas, suggesting an overall connectivity of about 40%. Based on the laminar patterns of connections between areas, we propose a hierarchy of visual areas and of somatosensory/motor areas that is more comprehensive than those suggested in other recent studies. The current version of the visual hierarchy includes 10 levels of cortical processing. Altogether, it contains 14 levels if one includes the retina and lateral geniculate nucleus at the bottom as well as the entorhinal cortex and hippocampus at the top. Within this hierarchy, there are multiple, intertwined processing streams, which, at a low level, are related to the compartmental organization of areas VI and V2 and, at a high level, are related to the distinction between processing centers in the temporal and parietal lobes. However, there are some pathways and relationships (about 10% of the total) whose descriptions do not fit cleanly into this hierarchical scheme for one reason or another. In most instances, though, it is unclear whether these represent genuine exceptions to a strict hierarchy rather than inaccuracies or uncertainties in the reported assignment.During the past decade, there has been an explosion of information about the organization and connectivity of sensory and motor areas in the mammalian cerebral cortex. Many laboratories have concentrated their efforts on the visual cortex of macaque monkeys, whose superb visual capacities in many ways rival those of humans. In this article, we survey recent progress in charting the layout of different cortical areas in the macaque and in analyzing the hierarchical relationships among these areas, part...
The primate visual system contains dozens of distinct areas in the cerebral cortex and several major subcortical structures. These subdivisions are extensively interconnected in a distributed hierarchical network that contains several intertwined processing streams. A number of strategies are used for efficient information processing within this hierarchy. These include linear and nonlinear filtering, passage through information bottlenecks, and coordinated use of multiple types of information. In addition, dynamic regulation of information flow within and between visual areas may provide the computational flexibility needed for the visual system to perform a broad spectrum of tasks accurately and at high resolution.
The somatotopic organization of the postcentral parietal cortex of the Old World monkey, Macaca fascicularis, was determined with multi-unit microelectrode recordings. The results lead to the following conclusions: 1) There are at least two complete and systematic representations of the contralateral body surface in the cortex of the postcentral gyrus. One representation is contained within Area 3b, the other within Area 1. 2) While there are important differences in the organization of the two representations, they are basically mirror-images of each other. 3) Each representation maintains body-surface adjacency by cortical adjacency in some mediolateral regions. In other regions, two types of discontinuities can be described: first, in which adjacent body surfaces are represented in separate cortical loci; second, in which adjacent cortical regions represent disparate body-surface regions. The internal organization of each representation is better described as a composite of somatotopic regions (Merzenich et al., '78) than as a serial array of dermatomal bands, or as a "homunculus." 4) While architectonic Area 2 responds to stimulation of deep body tissue, at least parts of Area 2 also respond to cutaneous stimulation. The organiation of the cutaneous representation of the hand in Area 2 is basically a mirror-image of the hand representation in Area 1. 5) Area 3a is activated by deep body tissue stimulation, suggesting the possibility of a fourth body representation within the traditional "S-I" region of somatosensory cortex in macaques. In accord with a previous study in a New World monkey (Merzenich et al., '78), we suggest that the cutaneous representation in Area 3b be considered as SI proper, and that the cutaneous representation in Area 1 be termed the posterior cutaneous field. Furthermore, based on the orientation of the representations of the body surface, as well as other factors, we suggest that the representation in Area 3b is homologous to "SmI" (or "SI") in non-primates.
Neurons responding selectively to different colours have been found in various cortical areas in macaque monkeys; however, little is known about whether and how the representation of colour is spatially organized in any cortical area. Cortical area V2 contains modules that respond preferentially to chromatic modulation, which are located in thin cytochrome oxidase stripes. Here we show that within and beyond these modules, gratings of different colours produce activations that peak at different locations. Optical recording of intrinsic signals revealed that the peak regions of the responses to different colours were spatially organized in the same order as colour stimuli are arranged in the DIN (German standard colour chart) colour system. Nearby regions represented colours of a similar hue. We found that the set of colour-specific regions formed 0.07-0.32-mm-wide and approximately 1.3-mm long bands that varied in shape from linear to nearly circular. Our finding suggests that thin stripes in V2 contain functional maps where the colour of a stimulus is represented by the location of its response activation peak.
Receptive field properties of 147 neurons histologically verified to be located in area V3 were investigated during semichronic recording from paralyzed anesthetized macaque monkeys. Quantitative analyses were made of neuron selectivities for direction, orientation, speed, binocular disparity, and color. The majority of neurons in V3 (76%) were strongly orientation selective; 40% demonstrated strong direction selectivity. Most cells were tuned for stimulus speed and almost half showed optimum responses at 16 degrees/s. The distribution of optimum speeds ranged primarily from 4 to 32 degrees/s. Several cells in V3 displayed multi-peaked orientation- and/or direction-tuning curves. These cells had two or more narrowly tuned peaks that were not co-axial. In some ways, they resemble higher-order hypercomplex cells of cat area 19 and may subserve a higher level of form or motion analysis than is seen at antecedent visual areas. Roughly half (45%) of the cells were selective for binocular disparity. Approximately half of these were tuned excitatory in that they showed weak responses when tested through either eye alone, but showed strong binocular facilitation centered on the fixation plane. The other disparity-selective cells were tuned inhibitory or asymmetric in their responses in front and behind the fixation plane. Contrary to previous reports, approximately 20% of the neurons in V3 were color selective in terms of showing a severalfold greater response to the best monochromatic wavelength compared with the worst. Color-tuning curves of the subset of color selective cells had, on average, a full bandwidth at half maximum response of 80-100 nm. A comparison of the receptive field properties of neurons in V3 to those in other areas of visual cortex suggests that V3, like MT, is well suited for the analysis of several aspects of stimulus motion. V3 may also be involved in some aspects of form analysis, particularly at low contrast levels. Comparison with area VP, a thin strip of cortex anterior to ventral V2, which was previously considered part of V3, indicates that direction selectivity is much more prevalent in V3 than in VP. Conversely, color-selective cells are the majority in VP but a minority in V3. This suggests that visual information is processed differently in the upper and lower visual fields.
The cortical connections of visual area 3 (V3) and the ventral posterior area (VP) in the macaque monkey were studied by using combinations of retrograde and anterograde tracers. Tracer injections were made into V3 or VP following electrophysiological recording in and near the target area. The pattern of ipsilateral cortical connections was analyzed in relation to the pattern of interhemispheric connections identified after transection of the corpus callosum. Both V3 and VP have major connections with areas V2, V3A, posterior intraparietal area (PIP), V4, middle temporal area (MT), medial superior temporal area (dorsal) (MSTd), and ventral intraparietal area (VIP). Their connections differ in several respects. Specifically, V3 has connections with areas V1 and V4 transitional area (V4t) that are absent for VP; VP has connections with areas ventral occipitotemporal area (VOT), dorsal prelunate area (DP), and visually responsive portion of temporal visual area F (VTF) that are absent or occur only rarely for V3. The laminar pattern of labelled terminals and retrogradely labeled cell bodies allowed assessment of the hierarchical relationships between areas V3 and VP and their various targets. Areas V1 and V2 are at a lower level than V3 and VP; all of the remaining areas are at a higher level. V3 receives major inputs from layer 4B of V1, suggesting an association with the magnocellular-dominated processing stream and a role in routing magnocellular-dominated information along pathways leading to both parietal and temporal lobes. The convergence and divergence of pathways involving V3 and VP underscores the distributed nature of hierarchical processing in the visual system.
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