There are many levels of disorder in amblyopic vision, from basic acuity and contrast sensitivity loss to abnormal binocular vision and global perception of motion and form. Amblyopia treatment via patching to restore acuity often leaves other aspects of vision deficient. The source for these additional deficits is unclear. Neural correlates of poor binocular function and acuity loss are found in V1 and V2. However, they are generally not sufficient to account for behaviorally measured vision loss. This review summarizes the known cortical correlates of visual deficits found in association with amblyopia, particularly those relevant to binocular vision and higher-order visual processing, in striate and extrastriate cortex. Recommendations for future research address open questions on the role of suppression and oculomotor abnormalities in amblyopic vision, and underexplored mechanisms such as top-down influences on information transmission in the amblyopic brain.

Anatomical and electrophysiological studies have provided us with detailed information regarding the extent and topography of the primary (V1) and secondary (V2) visual areas in primates. The consensus about the V1 and V2 maps, however, is in sharp contrast with controversies regarding the organization of the cortical areas lying immediately rostral to V2. In this review, we address the contentious issue of the extent of the third visual area (V3). Specifically, we will argue for the existence of both ventral (V3v) and dorsal (V3d) segments of V3, which are located, respectively, adjacent to the anterior border of ventral and dorsal V2. V3v and V3d would together constitute a single functional area with a complete representation of both upper and lower visual hemifields. Another contentious issue is the organization of the parietal-occipital (PO) area, which also borders the rostral edge of the medial portion of dorsal V2. Different from V1, V2, and V3, which exhibit a topography based on the defined lines of isoeccentricity and isopolar representation, area PO only has a systematic representation of polar angles, with an emphasis on the peripheral visual field (isoeccentricity lines are not well defined). Based on the connectivity patterns of area PO with distinct cytochrome oxidase modules in V2, we propose a subdivision of the dorsal stream of visual information processing into lateral and medial domains. In this model, area PO constitutes the first processing instance of the dorsal-medial stream, coding for the full-field flow of visual cues during navigation. Finally, we compare our findings with those in other species of Old and New World monkeys and argue that larger animals, such as macaque and capuchin monkeys, have similar organizations of the areas rostral to V2, which is different from that in smaller New World monkeys.

The number, location, extent, and functional properties of the cortical areas that occupy the medial parieto-occipital cortex (mPOC) have been, and still is, a matter of scientific debate. The mPOC is a convoluted region of the brain that presents a high level of individual variability, and the fact that many areas of mPOC are located within very deep sulci further limits the possibility to investigate their anatomo-functional properties. In the present review, we summarize the location and extent of mPOC areas in the macaque brain as obtained by architectural, connectional, and functional data. The different approaches lead to a subdivision of mPOC that includes areas V2, V3, V6, V6Av, and V6Ad. Extrastriate areas V2 and V3 occupy the posterior wall of the parieto-occipital sulcus (POs). The fundus of POs and the ventralmost part of the anterior wall of the sulcus are occupied by a retinotopically organized visual area, called V6, which represents the contralateral part of the visual field and emphasizes its periphery. The remaining part of the anterior wall of POs is occupied by two areas, V6Av and V6Ad, which contain visual as well as arm reaching neurons. Our analyses suggest that areas V6 and V6Av, together, occupy the cortical territory previously described as area PO. Functionally, area V6 is a motion area particularly sensitive to the real motion of objects in the animal's field of view, while V6Av and V6Ad are visuomotor areas likely involved in the visual guidance of arm movement and object prehension.

This paper presents a general computational treatment of how mammals are able to deal with visual objects and environments. The model tries to cover the entire range from behavior and phenomenological experience to detailed neural encodings in crude but computationally plausible reductive steps. The problems addressed include perceptual constancies, eye movements and the stable visual world, object descriptions, perceptual generalizations, and the representation of extrapersonal space.

The entire development is based on an action-oriented notion of perception. The observer is assumed to be continuously sampling the ambient light for information of current value. The central problem of vision is taken to be categorizing and locating objects in the environment. The critical step in this process is the linking of visual information to symbolic object descriptions; this is called indexing, from the analogy of identifying a book from index terms. The system must also identify situations and use this knowledge to guide movement and other actions in the environment. The treatment focuses on the different representations of information used in the visual system.

The four representational frames capture information in the following forms: retinotopic, head-based, symbolic, and allocentric. The functional roles of the four frames, the communication among them, and their suggested neurophysiological realization constitute the core of the paper. The model is perforce crude, but appears to be consistent with all relevant findings.

We studied quantitatively the receptive-field properties of 74 units recorded from the representation of the central visual fields in the cat's lateral suprasylvian (LS) visual cortex. In agreement with previous workers, we found that LS receptive fields tended to be large and to lack discernible spatial structure. They resembled the complex receptive fields of areas 17 and 18 in their general organization. We examined the responses of these neurons to moving optimally oriented sinusoidal gratings that varied in spatial and temporal frequency of drift. Most LS neurons were selective for the spatial frequency of sinusoidal gratings; 7% responded to all spatial frequencies below a cutoff value. In agreement with previous reports, the optimal spatial frequencies for LS neurons covered a wider range than is seen in either area 17 or 18 alone (0.05–1 cycle/deg), but are certainly included in the range covered by both these afferent areas. Individual neurons in LS responded to a range of spatial frequencies broader than is typical for neurons in areas 17 and 18. The effect of varying the drift rate of otherwise optimal gratings was similar in LS to that reported for areas 17 and 18. Most neurons were optimally responsive to drift rates between 0.5 and 4 Hz, and resolved frequencies as high as 10–30 Hz. A few neurons had optima higher than 6 Hz and resolved frequencies in excess of 30 Hz. We conclude that the receptive fields of LS neurons reflect rather closely the properties of their afferents from areas 17 and 18. Apart from the increased incidence of directional selectivity in LS and the increase in receptive-field size seen there, we find no evidence for a significant reorganization of visual signals.

The purpose of the present study was to assess changes in the levels of cytochrome oxidase (CO) activity in the dorsal lateral geniculate nucleus (dLGN) of the adult cat following removal of primary visual cortical areas 17 and 18 on the day of birth (P1), P28, or in adulthood (≫6 months). Cytochrome oxidase activity was measured in histological sections 9 or more months after the cortical ablation. Control measures obtained from intact cats show that CO activity is normally highest in the A-laminae of dLGN, and slightly lower in the C-complex. Following visual cortex ablations incurred at any age, CO activity levels are reduced in the A-laminae. This reduction is most profound following ablations incurred on P28 or in adulthood. In contrast, CO activity in the C-complex of dLGN is at nearly normal levels following ablations on P1 or P28, but not in adulthood. These findings contribute to our understanding of the role played by the dLGN in the transfer of visual signals along retino-geniculo-extrastriate pathways that expand following early removal of areas 17 and 18. Moreover, they have implications for our understanding of spared behavioral functions attributed to the extrastriate cortex in cats which incurred early damage of areas 17 and 18.

Cytochrome-oxidase (CO) histochemistry has revealed important functional subdivisions, modules, and processing streams in the macaque visual cortex. The present study is aimed at analyzing the development and characteristics of CO patterns in the human visual cortex by means of histochemistry and immunohistochemistry. At 26 weeks of gestation, both the ventricular and subventricular zones had low levels of CO, while the cortical plate had moderate levels of CO. At birth, supragranular CO-rich zones (puffs) were not clearly organized, indicating that the development of puffs in the neonatal striate cortex lags behind that of the macaque monkey, whose puffs appear weeks before birth. Puffs were more clearly discernible in human cortex at postnatal day 24, and became well organized by the fourth postnatal month. Layer IVcα in the neonate exhibited a higher level of activity and amount of CO than the central portion of IVcβ, which contained a dense aggregate of small neurons. The base of IVcβ, however, was often as CO reactive as IVcα. In contrast, the majority of specimens available to us from the fourth postnatal month and from adults with no known neurological diseases had significantly greater CO reactivity in layer IVcβ than in IVcaβ. Layer VI was moderately reactive for CO throughout development. In V2, stripes with globular zones of high CO activity were sporadically present at birth, suggesting that their development may parallel or precede that of puffs in VI. These stripes with CO-rich globular zones became more prominent in the adult and radiated orthogonally from the V1/V2 border. They were not, however, clearly organized into alternating thick and thin stripes as they are in the squirrel monkey. Visual cortical areas beyond V2 exhibited high CO activity mainly in layers III and IV and moderate levels in VI, suggesting that sites associated with cortico-cortical pathways may be metabolically most active.

The effects of V4, MT, and combined V4+MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.

During locomotion, observers respond to objects in the environment that may represent obstacles to avoid or landmarks for navigation. Although much is known about how visual cortical neurons respond to stimulus objects moving against a blank background, nothing is known about their responses when objects are embedded in optic flow fields (the patterns of motion seen during locomotion). We recorded from cells in the lateral suprasylvian visual area (LS) of the cat, an area probably analogous to area MT. In our first experiments, optic flow simulations mimicked the view of a cat trotting across a plain covered with small balls; a black bar lying on the balls served as a target object. In subsequent experiments, optic flow simulations were composed of natural elements, with target objects representing bushes, rocks, and variants of these. Cells did not respond to the target bar in the presence of optic flow backgrounds, although they did respond to it in the absence of a background. However, 273/423 cells responded to at least one of the taller, naturalistic objects embedded in optic flow simulations. These responses might represent a form of image segmentation, in that cells detected objects against a complex background. Surprisingly, the responsiveness of cells to objects in optic flow fields was not correlated with preferred direction as measured with a moving bar or whole-field texture. Because the direction of object motion was determined solely by receptive-field location, it often differed considerably from a cell's preferred direction. About a quarter of the cells responded well to objects in optic flow movies but more weakly or not at all to bars moving in the same direction as the object, suggesting that the optic flow background modified or suppressed direction selectivity.

It has been proposed that one area of extrastriate cortex in the cat, the lateral suprasylvian area (LS), plays an important role in visual analysis during locomotion (Rauschecker et al., 1987). Cells in LS reportedly tend to prefer directions along a trajectory originating at the center of gaze, and passing outward through the receptive-field center. Such directions coincide with the directions of image motion in an optic flow field, the pattern seen by locomoting observers when they fixate the point towards which they are heading (Gibson, 1950). We re-examined this issue for cells in LS with receptive fields in the lower visual field. Cells recorded posterior to Horsley-Clarke A2 showed a clear correlation between preferred direction and receptive-field location, but not that predicted: preferred directions were generally orthogonal to “optic flow” directions. Since these cells were all located posterior to those in studies showing a bias for “optic flow” directions, we hypothesized that there are two cell populations within LS, an anterior population that tends to prefer radial-outward directions, and a posterior population that tends to prefer directions orthogonal to radial. Data from earlier mapping experiments (Sherk & Mulligan, 1993) supported this idea.

Extrastriate areas TEO and V4 have been associated with form and color vision. Area V4 has also been suggested to participate in processes concerned with attention, stimulus salience, and perceptual learning. In a continuing effort to elucidate the connectional interactions and microcircuitry of these areas, we describe in this report the pattern of feedback connections from TEO and V4. Connections were demonstrated by injections of the high-resolution anterograde tracers PHA-L or biocytin and further analyzed by reconstruction of 25 individual axons through serial sections. This analysis yielded several new results: (1) Both areas TEO and V4 have widespread feedback connections (defined by their preferential termination in layer 1 and avoidance of layer 4). From TEO, there are dense projections to area V4 and moderate ones to V2 and V1. From V4, there are dense projections to V2 and moderate ones to V3 and V1. (2) Terminal fields span large territories in area V1, up to 6.0 mm in the case of axons originating from TEO; up to 5.0 mm in the case of axons originating from V4. In V2, fields tend to be smaller, between 3.0–5.0 mm. (3) Many axons from TEO and some from V4 have terminations in both areas V1 and V2. (4) Because individual terminal clusters and segments are often larger than cytochrome oxidase compartments, especially in V1, we suggest they may not be correlated with this compartmental organization. These results are consistent with the hypothesis that feedback connections may contribute to processes other than perceptual discrimination.

Previous research suggests binocular rivalry disrupts extrastriate, but not striate processes, although the locus along the visual pathway at which such disruption first occurs is uncertain. It has been argued that subjective contours arise via a two-stage process in which end-stopped cells feed into orientation-sensitive neurones in V2, and that orientation aftereffects induced with subjective contours are the product of mechanisms similar to those giving rise to real contour aftereffects. If binocular rivalry disrupts the acquisition of subjective contour aftereffects, then it follows from this model that rivalry disrupts processing in V2. Experiments reported here confirm this and provide evidence which suggests binocular rivalry arises through interactions between binocular neurones, rather than via some type of specialized binocular rivalry mechanism.

Visually guided saccadic eye movements to singly presented stationary targets form a bimodal distribution. After superior colliculus lesions, the so called “express saccades” that form the first mode of the distribution are no longer obtained. The aim of this study was to determine what role several other neural systems play in the generation of express and regular saccades, with the latter being those that form the second mode in the bimodal distribution. Lesions were made in the parvocellular and magnocellular portions of the lateral geniculate nucleus to disrupt either the midget system or the parasol system that originates in the retina and areas V4 and MT. The effects of the lesions were examined on the accuracy and latency of saccadic eye movements made to stationary and to moving visual targets. Following magnocellular and MT lesions deficits were observed in smooth pursuit and in the amplitude of saccades made to moving targets. However, none of the lesions produced significant changes in the bimodal distribution of saccadic latencies to stationary targets. The results suggest that express saccades and regular saccades are not selectively mediated by either the midget or the parasol systems or by areas V4 and MT. Neither are the frontal eye fields involved as had previously been shown. We suggest that the superior colliculus plays a central role in producing both express and regular saccades by virtue of highly convergent input from numerous cortical structures.

This study examined the consequences of visual system lesions on visual aftereffects produced by achromatic stimuli of various luminance contrasts and chromatic stimuli of various wavelength compositions. The effects of repeated exposure to such adapting stimuli were assessed using probes whose luminance contrast and wavelength composition were systematically varied using both detection and discrimination paradigms. Interocular tests revealed that both peripheral and central mechanisms contribute to the visual aftereffects produced by the adapting stimulus arrays used in this study. Contrary to the hypothesis according to which the midget system of the retina is the conveyor of visual afterimages, we found that blocking this system with lesions of parvocellular lateral geniculate nucleus, through which the midget cells make their way to the striate cortex in primates, did not eliminate the visual aftereffects. It appears therefore that the parasol system of the retina, which courses through the magnocellular layers of the lateral geniculate nucleus to cortex, can convey the necessary signals for the generation of visual aftereffects. Lesions of areas V4 and MT did not have significant effects on the visual aftereffects studied suggesting that the central factors that contribute to the visual aftereffects occur either already in area VI or are conveyed to higher centers through regions other than areas V4 and MT.

We have examined the effects of rearing kittens with a unilateral convergent strabismus, induced surgically at 3 weeks of age, on the binocularity (ocular dominance) and receptive-field position of neurons in the motion-sensitive lateral suprasylvian (LS) area of cat extrastriate cortex. Data were compared to those obtained from area 17 in the same animals, and from the two areas of cortex in normal adult cats. Interocular alignment of the operated cats was assessed in alert adults using corneal reflex photography and during recording from the positions of retinal landmarks under paralysis. The strabismus magnitude in each operated cat was calculated by comparison with equivalent data from the normal animals.

Strabismus always caused a major loss of binocularity in area 17. The remaining binocular neurons had receptive-field (RF) pairs arising from positions of normal correspondence in the two retinae and would thus have been responsive to different regions of visual space through the misaligned eyes in the alert animal. In area LS, the effects were dependent on the strabismus magnitude. In the group of four cats with pronounced strabismus (18–30 deg crossed), a loss of binocularity occurred in area LS equivalent in severity to that in area 17. The majority of the remaining binocular LS neurons possessed RF pairs in normal retinal correspondence and would thus, in the alert animal, have received spatially disparate visual input through the two eyes. This also occurred in three other cats with more moderate strabismus (11–15 deg crossed), although only a small breakdown in the binocularity of area LS was apparent. The group of cats with mild strabismus (≤10 deg crossed) had normal proportions of binocular neurons in area LS. In three of these cats, the maintenance of binocularity was accompanied by shifts in RF position, with visual inputs arising from anomalous retinal locations. These shifts compensated, in part, for the strabismus angle present in each cat, so that most of the binocular LS neurons would have received inputs from regions of visual correspondence through the misaligned eyes when the animal was alert.

Similar mechanisms could afford a basis for the binocular visual compensations that occur in humans with small-angle strabismus of early onset. If so, anomalous retinal correspondence in such individuals would have as a locus areas of extrastriate cortex with a role in motion perception, and would involve alterations to the neural substrate underlying normal binocular vision.

The monoclonal antibody Cat-301 was used to stain neurons and neuropil in the visual thalamus and cortex of tree shrews —small, highly visual mammals that are closely related to primates. Previously, this antibody has been found to label neurons associated with the Y-cell stream of processing in cats and the magnocellular or M-cell stream in macaque monkeys. In tree shrews, the antibody selectively labeled layers 1, 2, 4, and 5 of the dorsal lateral geniculate nucleus, layers that are likely to contain neurons previously classified as Y-cells. Of the two layers that contain W-cells, layer 3 was unlabeled and layer 6 was lightly labeled. In area 17, layer 3c was densely stained, as in cats and macaque monkeys. The external half of layer 5 was also densely stained, in contrast to cats where the internal half of layer 5 is stained and macaques where layer 5 is sparsely stained. Area 18 was characterized by dense, uniform staining of inner layer 3 and outer layer 5, but no pattern of alternating light and dense bands crossed the width of area 18 as in macaques. Dense labeling of these same sublayers occurred in cortical areas TA and TD just lateral to area 18. Area TD may be the homologue of area MT of primates, which also stains densely with Cat-301 in macaques. These results indicate that Cat-301 differentially labels layers and areas in the visual system of tree shrews, and raise intriguing issues of comparison among tree shrews, primates, and cats.

Tritiated proline and leucine were injected into areas 17 and 18 of intact cats and into the medial bank of the lateral suprasylvian (LS) cortex of intact cats and cats from which areas 17 and 18 had been removed on postnatal day 1 (P1), P28, or in adulthood (A). The density of label transported to the superior colliculus was quantified using image-analysis equipment. The results from the intact cats confirmed previous reports that areas 17 and 18 project most heavily to stratum zonale (SZ) and stratum griseum superficiale (SGS) and LS cortex projects most heavily to stratum opticum (SO) of the superior colliculus. However, in cats with lesions of areas 17 and 18, the projections from LS cortex showed an age-dependent reorganization. LS projections to SGS and SZ were enhanced following ablation of areas 17 and 18 on P1, and projections to SGS were enhanced following an ablation on P28. The pattern of LS-collicular projection following ablations incurred in adulthood was indistinguishable from the pattern presented by intact cats. This study demonstrates that the LS corticocollicular projection expands in SGS and possibly substitutes for inputs eliminated by the removal of areas 17 and 18 from the immature brain. This enhanced pathway may contribute to compensatory neuronal changes and to spared behaviors that accompany damage of immature cortex.

Lateral suprasylvian visual cortex in the cat has been studied extensively, but its retinotopic organization remains controversial. Although some investigators have divided this region into many distinct areas, others have argued for a simpler organization. A clear understanding of the region’s retinotopic organization is important in order to define distinct areas that are likely to subserve unique visual functions. We therefore reexamined the map of the lower visual field in the striate-recipient region of lateral suprasylvian cortex, a region we refer to as the lateral suprasylvian area, LS.

A dual mapping approach was used. First, receptive fields were plotted at numerous locations along closely spaced electrode penetrations; second, different anterograde tracers were injected at retinotopically identified sites in area 17, yielding patches of label in LS. To visualize the resulting data, suprasylvian cortex was flattened with the aid of a computer.

Global features of the map reported in many earlier studies were confirmed. Central visual field was represented posteriorly, and elevations generally shifted downward as one moved anteriorly. Often (though not always) there was a progression from peripheral locations towards the vertical meridian as the electrode moved down the medial suprasylvian bank.

The map had some remarkable characteristics not previously reported in any map in the cat. The vertical meridian’s representation was split into two pieces, separated by a gap, and both pieces were partially internalized within the map. Horizontal meridian occupied the gap. The area centralis usually had a dual representation along the posterior boundary of the lower field representation, and other fragments of visual field were duplicated as well. Finally, magnification appeared to change abruptly and unexpectedly, so that compressed regions of representation adjoined expanded regions. Despite its complexity, we found the map to be more orderly than previously thought. There was no clearcut retinotopic basis on which to subdivide LS’s lower field representation into distinct areas.

To examine the subcorctical connections of the medial superior temporal and fundus of the superior temporal visual areas (MST and FST, respectively), we injected anterograde and retrograde tracers into 16 physiologically identified sites within the two areas in seven macaque monkeys. The subcortical connections of MST and FST were found to be very similar. Both areas were found to be reciprocally connected with the pulvinar, mainly with its medial subdivision, and with the claustrum. Nonreciprocal projections from both MST and FST were consistently found in the striatum (caudate and putamen), reticular nucleus of the thalamus, and the pontine nuclei. The labeled terminals in the pons were in the dorsolateral, lateral, dorsal, and peduncular nuclei. Additional nonreciprocal projections were found in one MST and one FST case to the nucleus of the optic tract, and, in one FST case, to the lateral terminal nucleus. Finally, three cases showed a nonreciprocal projection to FST from the basal forebrain. The subcortical structures containing label following MST and FST injections were largely the same as those labeled after injections of the middle temporal visual area (MT), but the label within each structure after MST and FST injections was more widespread than that from MT, overlapping the distribution of label that has been reported after injections of parietal visual areas. This finding is consistent with the known contributions of MST and FST to the functions of parietal cortex, such as eye-movement control.

We have examined the distribution of preferred directions of motion for neurons in the middle temporal visual area (MT) of the macaque. We found a marked anisotropy favoring directions that are oriented away from the center of gaze. This anisotropy is present only among neurons with peripherally located receptive fields. This peripheral centrifugal directionality bias corresponds well to the biased distribution of motions characteristic of optic flow fields, which are generated by displacement of the visual world during forward locomotion. The bias may facilitate the processing of this common form of visual stimulation and could underlie previously observed perceptual anisotropies favoring centrifugal motion. We suggest that the bias could arise from exposure of modifiable cortical circuitry to a naturally occurring form of selective visual experience.