Information processing in the primate visual system: an integrated systems perspective.

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.

Recovery of normal topography in the somatosensory cortex of monkeys after nerve crush and regeneration.

After median nerve fibers to glabrous skin on the hands of monkeys were crushed and allowed to regenerate, normal topographical organization was recovered in the representation of the hand in primary somatosensory cortex. Similar recovery of normal cortical organization may underlie the sensory restoration that usually follows nerve crush injury in humans.

Representations of the body surface in postcentral parietal cortex of Macaca fascicularis.

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.

Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex.

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.

Somatotopic organization of the lateral sulcus of owl monkeys: area 3b, S-II, and a ventral somatosensory area.

Multiunit microelectrode recordings and injections of horseradish peroxidase (HRP) were used to reveal neuron response properties, somatotopic organization, and interconnections of somatosensory cortex in the lateral sulcus (sylvian fissure) of New World owl monkeys. There were a number of main findings. 1) Representations of the face and head in areas 3b, 1, and S-II are found on the upper bank of the lateral sulcus. Most of the mouth and lip representations of area 3b were found in a rostral extension along the lip of the lateral sulcus. Adjacent cortex deeper in the lateral sulcus represented the nose, eye, ear, and scalp. 2) S-II was located on the upper bank of the lateral sulcus and extended past the fundus onto the deepest part of the lower bank. The face was represented most superficially in the sulcus, with the hand, foot, and trunk located in a rostrocaudal sequence deeper in the sulcus. The orientation of S-II is "erect," with the limbs pointing away from area 3b. 3) Neurons in S-II were activated by light tactile stimulation of the contralateral body surface. Receptive fields were several times larger than for area 3b neurons. 4) A 1-2-mm strip of cortex separating the face and hand representations in S-II was consistently responsive to the stimulation of deep receptors but was unresponsive to light cutaneous stimulation. 5) Injections of horseradish peroxidase in the electrophysiologically identified hand or foot representations of area 3b revealed somatotopically matched interconnections with mapped hand and foot representations in S-II. 6) A systematic representation of the body, termed the "ventral somatic" area, VS, was found extending laterally from S-II on the lower bank of the lateral sulcus. Within VS, the hand and foot were represented deep in the sulcus along the hand and foot regions of S-II, and the face was lateral near the ventral lip of the sulcus. 7) Neurons at most recording sites in the VS region were activated by contralateral cutaneous stimuli. However, a few sites had neurons with bilateral receptive fields. Receptive field sizes were comparable to those in S-II. In addition, neurons in islands of cortex in the VS region had properties that suggested that they were activated by pacinian receptors, while other regions were difficult to activate by light tactile stimuli but responded to stimuli that would activate deep receptors. 8) A few recording sites caudal to S-II on the upper bank of the lateral sulcus were responsive to somatic stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

Abnormal central visual pathways in the brain of an albino green monkey (Cercopithecus aethiops).

The visual pathways of an albino green monkey have been studied electrophysiologically and by autoradiographic methods. The monkey had a white coat and pink eyes; it had a strabismus and a nystagmus. When comparisons were made with normal macaque and green monkeys, several abnormalities could be defined. In the retina there was no foveal pit. A whole mount preparation showed a central area of high ganglion cell density in which the ganglion cells were significantly larger than the most central ganglion cells of a normal monkey. More peripheral retinal areas showed an apparently normal distribution of ganglion cell sizes and packing densities. Within the optic tract the number of uncrossed retinofugal fibers was less than normal, the part of the tract that represents central vision showing almost no uncrossed component. The uncrossed input to the lateral geniculate nucleus and to the superior colliculus was similarly reduced. Regions normally receiving ipsilateral afferents from the central retina were innervated exclusively by crossed afferents. The pathways to the magnocellular geniculate layers showed a more extensive abnormality than did the pathways to the parvicellular layers. Not only were the afferents to the geniculate layers abnormal, but the laminar pattern in the nucleus was also clear than normal in some parts of the nucleus, and there were a number of abnormal laminar fusions. Within the visual cortex it was possible to demonstrate a normal mapping of the contralateral visual field through the contralateral nasal retina and through the peripheral parts of the ipsilateral temporal retina. The central parts of the temporal retina mapped abnormally in the contralateral visual cortex, so that there was a monocular map of the central parts of the visual field forming as a mirror reversal of the normal map. The normal map of the contralateral hemifield formed columns that alternated with the abnormal map of the ipsilateral hemifield. The peripheral parts of the visual field were represented as ocular dominance columns, demonstrable electrophysiologically and also by the transneuronal transport of 3H-proline.

Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys.

In an earlier study (Neuroscience 8, 33-55, 1983), we found that the cortex representing the skin of the median nerve within parietal somatosensory fields 3b and 1 was completely occupied by 'new' inputs from the ulnar and radial nerves, 2-9 months after the median nerve was cut and tied in adult squirrel and owl monkeys. In this report, we describe the results of studies directed toward determining the time course and likely mechanisms underlying this remarkable plasticity. Highly detailed maps of the hand surface representation were derived in monkeys before, immediately after, and at subsequent short and intermediate time stages after median nerve section. In one monkey, maps were derived before nerve section, immediately after nerve section, and 11, 22 and 144 days later. Thus, direct comparisons in cortical map structure could be made over time in this individual monkey. In other experiments, single maps were derived at given post-section intervals. These studies revealed that: (1) large cortical sectors were 'silenced' by median nerve transection. (2) Significant inputs restricted to the dorsum of the radial hand and the dorsum of digits 1, 2 and 3 were immediately 'unmasked' by median nerve transection. (3) These immediately 'unmasked' regions were topographically crude, and represented only fragments of this dorsal skin. They were transformed, over time, into very large, highly topographic and complete representations of dorsal skin surfaces. (4) Representations of bordering glabrous skin surfaces progressively expanded to occupy larger and larger portions of the former median nerve cortical representational zone. (5) These 'expanded' representations of ulnar nerve-innervated skin surfaces sometimes moved, in entirety, into the former median nerve representational zone. (6) Almost all of the former median nerve zone was driven by new inputs in a map derived 22 days after nerve section. At shorter times (3, 6 and 11 days), 'reoccupation' was still incomplete. (7) Very significant changes in map dimensions within and outside of the former median skin cortical field were seen after the 'reoccupation' of the deprived cortex by 'new' inputs was initially completed. (8) Progressive changes were recorded within the original ulnar and radial nerve cortical representational zones, as skin surfaces originally overtly represented wholly within these regions expanded into the former median nerve zone. (9) Throughout the studied period, the cortical representational loci of many skin sites appeared to change continually and often markedly. (10) The locations of map discontinuities also shifted significantly over time. (11) Concomitant with changes in representational magnification over time, inverse changes in receptive field sizes were recorded.(ABSTRACT TRUNCATED AT 400 WORDS)

Radiation-induced micrencephaly in guinea pigs.

The effect of X rays on brain weight of guinea pig pups at birth was studied in 21-day-old embryos exposed in utero to doses of 75 and 100 mGy. When compared to controls and when corrected for body weight, gestation time, litter size, sex, and examiner differences, the brains of irradiated pups weighed approximately 46 mg less than those of controls (P < 0.001) for the 75-mGy group and about 55 mg less for the 100-mGy group. Brains of females weighed 51 mg less than those of males of the same body weight. Dam weight and caging conditions had no observed effect on brain weight.

The popout in some conjunction searches is due to perceptual grouping.

The target in a visual search task usually pops out if it can be distinguished from its background on the basis of only one visual feature but not if the target represents a conjunction of two or more features. However, several recent reports suggest that in certain cases, search targets defined by a conjunction of two features also pop out. We have reinvestigated three pairs of such features to determine whether the popout in these cases can be attributed to perceptual grouping. We find that that in all three cases, popout no longer occurs when perceptual grouping is degraded, suggesting that the popout is the result of perceptual grouping and not of novel mechanism/s of conjunction search.

Representations of the body surface in areas 3b and 1 of postcentral parietal cortex of Cebus monkeys.

The somatotopic organization of postcentral parietal cortex was determined with microelectrode mapping methods in a New World monkey, Cebus albifrons. As in previous studies in macaque, squirrel and owl monkeys, two separate representations of the body surface were found in regions corresponding to the architectonic fields 3b and 1. The two representations were roughly mirror-images of each other, with receptive field locations matched for recording sites along the common border. As in other monkeys, the glabrous digit tips of the hand and foot pointed rostrally in the Area 3b representation and caudally in the Area 1 representation. Both representations proceeded in parallel from the tail on the medial wall of the cerebral hemisphere to the teeth and tongue in lateral cortex along the Sylvian fissure. Compared with the other monkeys, the tail of the cebus monkey, which is prehensile, was represented in a very large region of cortex in Areas 3b and 1. Like its close relative, the squirrel monkey, the representation of the trunk and parts of the limbs were reversed in orientation in both Area 3b and Area 1 in cebus monkeys as compared to owl and macaque monkeys. The reversals of organization for some but not all parts of the representations in cebus and squirrel monkeys suggest that one line of New World monkeys acquired a unique but functionally adequate pattern of somatotopic organization for the two adjoining fields.

Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex.

This report provides an overview of the functional organization of cortex immediately anterior to area V2 in extrastriate visual cortex of the macaque monkey. Contrary to previous suggestions that a single area, V3, lies anterior to V2, we have obtained evidence that this strip of cortex includes two separate areas, V3 and the ventral posterior area, VP. The evidence supporting this conclusion is based on dorso-ventral asymmetries in cortico-cortical connections, myeloarchitecture, and single-unit physiological properties relating to the processing of information about color and motion.

Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys.

Response properties of single neurons in the middle temporal visual area (MT) of anesthetized owl monkeys were determined and quantified for flashed and moving bars of light under computer control for position, orientation, direction of movement, and speed. Receptive-field sizes, ranging from 4 to 25 degrees in width, were considerably larger than receptive fields with corresponding eccentricities in the striate cortex. Neurons were highly binocular with most cells equally or nearly equally activated by either eye. Neurons varied in selectivity for axis and direction of moving bars. Some neurons demonstrated little or no selectivity, others were bidirectional on a single axis, while the largest group was highly selective for direction with little or no response to bar movement opposite to the preferred direction. Over 70% of neurons were classified as highly selective and 90% showed some preference for direction and/or axis of stimulus movement. Neurons typically responded to bar movement only over a restricted range of velocities. The majority of neurons responded best to a particular velocity within the 5-60 degrees/s range, with marked attenuation of the response for velocities greater or less than the preferred. Some neurons failed to show significant response attenuation even at the lowest tested velocity, while other neurons preferred velocities of 100 degrees/s or more and failed to attenuate to the highest velocities. Response magnitude varied with stimulus dimensions. Increasing the length of the moving bar typically increased the magnitude of the response slightly until the stimulus exceeded the receptive-field borders. Other neurons responded less to increases in bar length within the excitatory receptive field. Neurons preferred narrow bars less than 1 degree in width, and marked reductions in responses characteristically occurred with wider stimuli. Moving patterns of randomly placed small dots were often as effective as or more effective than single bars in activating neurons. Selectivity for direction of movement remained for the dot pattern. for the dot pattern. Poststimulus time (PST) histograms of responses to bars flashed at a series of 21 different positions across the receptive field, in the "response-plane" format, indicated a spatially and temporally homogeneous receptive-field structure for nearly all neurons. Cells characteristically showed transient excitation at both stimulus onset and offset for all effective stimulus locations. Some cells responded mainly at bright stimulus onset or offset.

Distributed hierarchical processing in the primate cerebral cortex.

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 V1 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 uncertainities in the reported assignment.

Modular organization of occipito-temporal pathways: cortical connections between visual area 4 and visual area 2 and posterior inferotemporal ventral area in macaque monkeys.

The modular organization of cortical pathways linking visual area 4 (V4) with occipital visual area 2 (V2) and inferotemporal posterior inferotemporal ventral area (PITv) was investigated through an analysis of the patterns of retrogradely labeled cell bodies after injections of tracers into V4 and PITv. Although cytochrome oxidase or other stains have failed to yield reliable independent anatomical markers for cortical modules beyond V1 and V2, V4 and PITv seem to have modular compartments with specific patterns of cortico-cortical connectivity. Tracer injections of V4 labeled cells in V2 (1) thin stripes exclusively, (2) interstripes exclusively, or (3) specific combinations of interstripe and thin stripe subcompartments. These labeling patterns suggest (1) that there is a complicated organization of inputs to V4, (2) that projections from V2 to V4 display a submodular selectivity, and (3) that projections from V2 to V4 display some degree of cross-stream convergence. Consistent with this framework, extensive regions of PITv provide feedback projections to interstripe-recipient portions of V4, whereas more restricted portions of PITv provide feedback to thin stripe-recipient portions of V4. Similarly, the feedforward projection from V4 to PITv often arose from multiple cell clusters across a wide expanse of V4. When distinguishable fluorescent tracers were injected into two PITv sites separated by 3-5 mm, a variety of projection patterns was observed in V4. In most cases, labeled cells were found in multiple, interdigitating, nonoverlapping clusters of 1-3 mm width, whereas in other cases the two labeled fields were highly intermixed. These results suggest that V4 and PITv contain functional modules that can be characterized by the specific patterns of segregated and convergent projections they receive from lower cortical areas. These specific patterns of intercortical input, in conjunction with intrinsic cortical circuitry, may endow extrastriate cortical neurons with new and more complex receptive field properties.

Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex.

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.

Segregation and convergence of functionally defined V2 thin stripe and interstripe compartment projections to area V4 of macaques.

The organization of projections from V2 thin stripes and interstripes to V4 was investigated using a combination of physiological and anatomical techniques. The compartments of V2 were first characterized, in vivo, using optical recording of intrinsic signals. Multiple anterograde tracers were then injected into different V2 compartments. The distribution of labeled axons was analyzed in tangential or horizontal sections including V4. A small iontophoretic injection, either in a thin stripe or an interstripe, labeled a large primary and several secondary foci in V4. The primary foci from the thin stripe and interstripe were spatially segregated by a gap of approximately 1 mm. Furthermore, less dense regions within the primary foci were often 'filled-in' by secondary foci from the opposite V2 compartment. When two injections were made both at interstripes, their projections to V4 were almost entirely overlapping. These anatomical patterns indicate that segregation and convergence of intercortical pathways are both important features of V4 organization. Furthermore, the size of cortical modules increases considerably from the blobs of V1, through the stripes of V2, to the afferent domains of V4.

Multiple processing streams in occipitotemporal visual cortex.

The earliest stages of cortical visual processing in areas V1 and V2 of the macaque monkey contain internal subdivisions ('blobs' and 'interblobs' in layer 4B in V1; thin, thick and interstripes in V2) that are selectively interconnected and contain neurons with distinctive visual response properties. Here we use anatomical pathway tracing to demonstrate that higher visual areas, V4 and the ventral posterior inferotemporal cortex, each contain anatomical subdivisions that have distinct input and output projections. These findings, in conjunction with others, suggest that modularity and multistream processing within individual cortical areas are widespread features of neocortical organization.

The representation of the body surface in S-I of cats.

In both cats and monkeys, the traditional region of the first somatosensory area of cortex, S-I, has been described as containing four strip-like architectonic fields, areas 3a, 3b, 1, and 2. In monkeys, a number of recent studies have provided evidence that each of these architectonic fields constitutes a separate representation of the body. Because of the observations in monkeys, we decided to re-examine the S-I region of cats to determine whether the evidence supported the traditional concept of a single representation, or the existence of several representations related to the described architectonic fields. Microelectrode multiunit mapping techniques were used to determine the somatotopic organization of the S-I region of 10 cats. The results indicate that a single representation of the body surface occupies most or all of the traditional S-I region including cortex defined as area "3b," area "1," and much of area "2," but excluding area "3a." Neurons throughout this single representation were activated by cutaneous stimuli, indicating that all parts of S-I receive input from cutaneous receptors. Neurons in area 3a were activated by inputs from deep receptors, as reported by others. Neurons caudal to S-I were activated by cutaneous stimuli and appeared to constitute the additional body surface representations of S-II and possibly S-III. Thus, the significance of the architectonic fields "3b," "1," and "2" is quite different in cats than in monkeys. We propose that most or all of these three fields, as described in cats, constitute the homologue of area 3b in monkeys.