Orientation discrimination in the cat: its cortical locus II. Extrastriate cortical areas.

Luminance-defined edges or bars are among the basic units of visual analysis: a "primitive" component of perception. We have utilized this stimulus in a psychophysical study of bar orientation discrimination in the cat before and after selective lesions in visual cortical areas. The cortices have been divided on the basis of their connectivity into three tiers. Tier I refers to areas 17 and 18, tier II includes areas that receive directly from tier I, and tier III includes those areas that receive directly from tier II. Previous studies (Vandenbussche et al. [1991] J. Comp. Neurol. 305:632-658) have shown that the discrimination of bar orientation depends heavily upon the integrity of areas 17 and 18 (tier I). The present study indicates that several extrastriate areas in tiers II and III contribute to this discrimination task. Our data suggest that the anterior medial lateral suprasylvian, the posterior lateral lateral suprasylvian (tier II), and the anterior lateral lateral suprasylvian (tier III) areas are most likely to contribute to bar orientation discrimination.

Two stages in visual texture segregation: a lesion study in the cat.

We have used five cats to investigate the effects of two distinct visual cortex lesions on the segregation of two different texture stimuli. The ablation of areas 17 and 18 (tier I) severely impaired the segregation between textures made of line elements differing in orientation, but spared the segregation between annulus and dot textures. In contrast, the ablation of those areas receiving direct afferents from areas 17 and 18 (tier II) destroyed the segregation for both texture stimuli. Strong deficits remained up to 1 year after the lesion, although limited recovery was observed after tier II lesions. We suggest that tier I areas are involved in the local filtering of the texture elements, and that tier II areas compute texture differences on the basis of the filtered image provided by tier I areas. The crucial contribution to texture segregation of visual areas belonging to a second level in the cortical hierarchy challenges the notion that texture segregation is entirely an early process in vision.

Effects of visual cortex lesions on orientation discrimination of illusory contours in the cat.

We have trained five cats in orientation discrimination using different contours, and compared the deficits caused by lesions of cortical areas 17 and 18 (tier I) to the deficits induced by removal of those areas receiving afferents originating in areas 17 and 18 (tier II). As contour stimuli we used two types of illusory contours and a luminance bar. The two illusory contours were defined by opposed line-ends. One of them coincided with a luminance gradient whereas the other did not. Tier I lesions destroyed the capacity to discriminate the orientation of both illusory contours, and also caused an important, though less severe, deficit in bar orientation discrimination. The deficits induced by tier I lesions were permanent. Tier II lesions also caused significant deficits in orientation discrimination of illusory contours, but only a negligible deficit in bar orientation discrimination, and this result was not a mere consequence of a difference in difficulty between the tasks involving bars and illusory contours. In addition, tier II lesions differentiated between illusory contour types, the deficit being more pronounced for the illusory contour without luminance gradient than for the one with luminance gradient. In contrast to tier I lesions, tier II lesions allowed significant recovery, leading to small final deficits for all contour types tested.

Longterm impairment of cat optokinetic nystagmus following visual cortical lesions.

Binocular and monocular gain of optokinetic nystagmus (OKN), OKN dynamics, vestibulo-ocular reflex (VOR) and VOR adaptation were measured in 5 normal cats and in 5 cats which underwent bilateral visual cortical lesions involving the 17-18 complex at least 4 months before testing. We observed longterm deficits after bilateral lesions involving area 17 and variable parts of area 18 but failed to observe deficits after 18-19 lesions. These deficits were limited to the OKN gain and the build-up time constant of OKN; the VOR and the optokinetic after-nystagmus (OKAN) time constant were within normal limits. Our results suggest that areas 17-18 operate in parallel to control the encoding of retinal slip velocity at the level of the nucleus of the optic tract (NOT) and the accessory optic system (AOS), which are known to represent the initial stage of the optokinetic pathways.

Orientation discrimination in the cat: its cortical locus. I. Areas 17 and 18.

An elementary unit of visual pattern and form perception is thought to be the orientation of edges; this element has been studied extensively by neurophysiologists using oriented line segments or bars. These same stimuli have been used in the present study to measure threshold discriminations in cats before and after cortical lesions of areas 17 and/or 18. Control experiments showed that the discriminations were made by using a single cue, orientation, and that other stimulus parameters, width, length and contrast of the bar, were optimized. The extent of the lesions was evaluated anatomically from cell and fiber stained sections through cortex and thalamus, matched to retinotopic maps of Tusa et al. (Cortical Sensory Organization, Vol. 2, Humana Press, pp. 1-31, '81) and Sanderson (Journal of Comparative Neurology 143:101-118, '71), and physiologically from visual field position of receptive fields of cells recorded in areas neighboring the lesions. Lesions involving area 17 and large parts of area 18 produced a marked deficit in orientation discrimination which included a loss in retention, and after retraining a substantial increase in thresholds for up to 3 years when tested with long bars. There was no recovery of discrimination when the animals were tested with short bars. Lesions which involved area 17 plus small parts of 18, or lesions of areas 18 and 19, produced no retention deficit and resulted in an increase in thresholds only at low contrast and narrow width. These experiments revealed an excellent correlation between lesion locus and size and behavioral deficit. They indicate that the cortical representation of bar orientation used for discrimination is distributed within and across areas 17 and 18. The spread of the distribution depends on other stimulus parameters such as bar width and length. Furthermore the experiments show that neither the most narrowly tuned cells nor the X-cell system is required for fine orientation discrimination of a long bar.

The role of the superior colliculus in facilitating visual attention and form perception.

When interhemispheric transfer in cats is studied from an intact hemisphere to a hemisphere with a suprasylvian cortical lesion, excellent transfer of grating discriminations, but no transfer of forms, is present. Stimuli with global, repetitive features covering a large visual field (gratings), which can be discriminated by preattentive vision, are transferred; perception of stimuli with local features (forms), which require serial exploration using focal vision, is defective in the hemisphere with cortical lesion and transfer is lacking. Influence of the midbrain in facilitating focal vision is shown by the restoration of form discriminations after section of the superior collicular commissure. It is hypothesized that the perceptual defect after lesion in the suprasylvian cortex is due to poor spatial attention and its restoration after midbrain lesion is due to improved function of those collicular cells that mediate orienting of attention.

Ibotenic acid lesions of the lateral substantia nigra restore visual orientation behavior in the hemianopic cat.

Transection of non-tectotectal fibers in the caudal one-half of the commissure of the superior colliculus restores visual orienting to a cat previously rendered hemianopic by a large unilateral visual cortical lesion. Other observations related to this recovery phenomenon (i.e., the Sprague effect) have suggested that the caudal commissural fibers whose destruction produces the recovery 1) are contralateral afferents to the superior colliculus on the side of the cortical lesion, and 2) profoundly influence visuo-motor processing in this superior colliculus. We performed anatomical and behavioral experiments to determine which of the more than 40 contralateral collicular afferents are directly involved in the Sprague effect. To guide subsequent behavioral studies, we performed a pilot anatomical experiment in which we injected WGA-HRP unilaterally into one superior colliculus at identical retinotopic loci in each of a pair of cats. One cat was normal (control), and the other (experimental) had previously received a caudal transection of the collicular commissure. Quantitative comparison of the retrograde labeling in collicular afferents revealed that a number of mesencephalic regions contain neurons that project to the colliculus via the caudal collicular commissure. Additional collicular injections of WGA-HRP demonstrated the exact location and distribution of collicular afferent neurons within these nuclei. In the behavioral experiments, we attempted to replicate the Sprague effect by destroying the neurons giving rise to the axons in the caudal collicular commissure. Ibotenic acid lesions of these neurons were performed in cats that were hemianopic following the removal of the contralateral visual cortex. Small lesions of a "critical zone" in the rostro-lateral substantia nigra pars reticulata and possibly the overlying ventral zona incerta consistently produced a visual recovery whereas lesions of the other collicular afferents did not. Paradoxically, large nigral lesions that also included the critical zone did not result in a recovery. A conceptual framework for these findings involving striato-nigro-tecto-preoculomotor interactions is presented.

Orientation discrimination in the cat: a distributed function.

Cats were trained to make fine orientation discriminations with stimuli similar to those used in physiological experiments--narrow, light bars 12 degrees long--before and after various combinations of lesions of areas 17 and 18. Discrimination thresholds were measured at different contrast levels and different bar widths, both pre- and postoperatively, for up to 1.5 years after the lesion. For high contrast stimuli, lesions restricted to area 17 or area 18 had little effect, but those lesions involving area 17 and a substantial part of area 18 raised thresholds. In the latter case there was a relationship between the amount of area 18 spared and the bar width at which discrimination was impaired. At low contrast deficits were seen only for narrow widths. These results lead to the following conclusions. (i) Orientation discrimination is a function distributed within and across areas 17 and 18. (ii) How this function is distributed in this cortex depends on stimulus width. (iii) The X system does not carry the signal necessary for orientation discrimination. (iv) Cells most narrowly tuned for orientation, which reside in the part of area 17 subserving central vision, do not determine the orientation discrimination threshold.

Recovery from cortical blindness mediated by destruction of nontectotectal fibers in the commissure of the superior colliculus in the cat.

Transection of the commissure of the superior colliculus restores visual orientation behavior to a cat previously rendered hemianopic by a unilateral visual cortical lesion (the Sprague effect). Using two methods, we asked whether this recovery resulted from the severing of the tectotectal component of the commissure or whether the destruction of some other connection was responsible. First, we transected either the rostral or the caudal one-half of the tectal commissure in hemianopic cats. If destruction of tectotectal fibers is responsible for the Sprague effect, then only rostral transections should produce the recovery since nearly all tectotectal connections lie in the rostral one-half of the commissure. However, rostral cuts failed to produce a recovery, whereas caudal commisurotomies did. Second, ibotenic acid was used to destroy the cells in the superior colliculus contralateral to the cortical lesion. This lesion eliminated the contralateral tectotectal pathway from the contralateral colliculus but left other fibers (originating elsewhere but coursing through the commissure) largely intact. These ibotenic acid lesions failed to produce the recovery; but when the caudal portion of the tectal commissure was subsequently transected in the same animals, the recovery was observed. The results of both experiments support the conclusion that the transection of a nontectotectal component of the commissure of the superior colliculus is responsible for the recovery of visual orientation behavior in a cortically blind cat.

Stimulus contrast and visual cortical lesions.

Intact animals can make fine orientation discriminations over a wide range of contrasts. After ablation of area 17 deficits in orientation discrimination are observed only at low contrast. The relevance of this finding for the design of sensitive ablation experiments is discussed.

Cortical mechanisms for local and global analysis of visual space in the cat.

The effects of lesions in the striate or extra-striate visual cortex of cats were evaluated using visual discrimination problems which required either local or global pattern processing. The results indicate that damage to areas 17 and 18 preferentially impairs local processes, while in addition they suggest that damage to the extra-striate cortex preferentially affects global processing. These findings may be related to the observations that cats with large lesions in the extra-striate cortex demonstrate deficits in form perception without reductions in visual acuity and those with lesions in areas 17-18 show elevations of acuity thresholds while maintaining excellent pattern and form vision.

Immediate postoperative retention of visual discriminations following selective cortical lesions in the cat.

Cats were trained preoperatively for brightness discrimination, and 7 pattern and form discriminations, and then retested for preoperative retention on each discrimination. Cortical lesions were then placed in areas 17 and 18 in one group (4 cats), in areas 17, 18 and 19 in another group (3 cats), and in suprasylvian cortex (areas 7, 21, and parts of 19, 5 and the lateral suprasylvian cortex) in a third group (4 cats). Results are also reported for a fourth group with extensive suprasylvian lesions, to which was added an unintended undercutting of areas 17 and 18 (4 cats). While during original preoperative learning the training continued until a fixed, stringent criterion of performance was attained, both preoperative and postoperative retention was tested in short sessions, involving a limited number of trials and a less stringent statistical criterion (significant run). After extensive removal of areas 17 and 18, all cats behaved as though following the cortical lesion they could immediately recognize the discriminative stimuli as efficiently as before, with no need for retraining. On the contrary, the group with areas 17, 18 and 19 lesions showed a substantial postoperative loss of all discriminations, and especially for the more difficult form discriminations, the reattainment of a significant level of performance was hard or impossible within the allotted number of trials. Also in the group with limited suprasylvian lesions, postoperative retention was generally impaired, but the reacquisition of efficient performance was superior to that of the previous group. Finally, large suprasylvian lesions encroaching on the white matter under areas 17, 18 and 19 proved disruptive for all discriminative capacities, both in retention and in relearning. The excellent retention of all discriminations following areas 17 and 18 lesions once again shows that these areas are by no means essential for complex vision in the cat. In addition, the results strongly indicate that the high-level visual capacities of destriate cats are not due to reorganization of readaptation processes occurring in extrastriate areas after a 17/18 removal. The clear-cut retention deficits which were present in cats with cortical lesions more extensive than areas 17 and 18 or outside of the latter areas prove the essential participation of extrastriate cortical areas in visual discrimination including form. However, the distribution of functions among the various visual cortical areas in visual discrimination remains poorly understood.(ABSTRACT TRUNCATED AT 400 WORDS)

Visual discrimination learning and interhemispheric transfer in the cat, as affected by 6-hydroxydopamine.

Learning and interhemispheric transfer of visual flux, pattern and form discriminations were studied in the cat after selected exposure of one suprasylvian cortex to 6-hydroxydopamine (6-OHDA). Biochemical assay using High Performance Liquid Chromatography (HPLC) two weeks after 6-OHDA revealed no discernible norepinephrine or dopamine in the treated cortex, but elevated concentrations of these transmitters in the cortex of the opposite hemisphere. Visual discriminations learned before treatment with 6-OHDA were retained at a high level using either the eye on the side of chemical lesion or the eye on the untreated side. An asymmetric deficit in learning new form discriminations was present, however, when the eye on the untreated side was used, in contrast to normal learning using the eye on the side of the hemisphere with depleted adrenergic nerve supply. Once learning was achieved using the lesioned hemisphere transfer of the engram was found to the untreated hemisphere. Thus, the unlesioned hemisphere was unable to learn normally using direct retinal input from the ipsilateral eye, but showed good capacity for learning using indirect visual input from the contralateral eye. This suggests a powerful influence of the callosum on the learning abilities of the two hemispheres, an influence proved by sectioning the callosum. Callosotomy resulted in a reversal of the discriminative capacities seen after 6-OHDA, i.e. the lesioned hemisphere was defective relative to the unlesioned hemisphere.

Striate cortex and visual acuity functions in the cat.

Using a two-choice visual discrimination paradigm, thresholds for size (gratings), parallelness (parallel vs. non-parallel lines), contour alignment (vernier offset), and angularity (polygon figures) were behaviorally determined in cats before and after ablations of portions of the geniculo-cortical system. Animals with a total loss of cortical area 17, and with a loss, in some cases, of up to 90% of areas 18 (with and without infringement into area 19), showed about a 30% reduction in grating acuity, a three-fold increase in parallelness and angularity thresholds, and a total loss of contour alignment ability. Control animals with ablations sparing area 17 showed no significant threshold changes. All animals were able to learn classic form discriminations postoperatively, but those with area 17-18 lesions at a somewhat slower than normal rate. Control procedures indicated that all tested discrimination capabilities did not depend on luminance differences between targets, local flux cues within the targets, or on the animals' use of residual portions of area 17 representing the peripheral visual field. Since the cat has multiple thalamo-cortical visual pathways, the results of the present study are consistent with the hypothesis that pathways parallel to the geniculo-striate system are capable of processing spatial information of considerable detail. The results also suggest, however, that the geniculo-striate system is uniquely necessary for the processing of the finest attributes of spatial contours.

Behavioral and electrophysiological effects of unilateral optic tract section in ordinary and Siamese cats.

In ordinary cats, section of one optic tract produced a complete contralateral hemianopsia in both eyes. Single-unit recordings showed a normal representation of the contralateral nasal retina and ipsilateral temporal retina in the SC on the side of the intact optic tract. In addition, in the rostral portion of this SC there was a representation of a small portion of the contralateral temporal retina. This portion was apposed to the vertical meridian and its width was at most 6 degrees. In the anterior half of the SC on the side of the optic tract section, despite the interruption of any direct optic input, there was an extensive representation of the ipsilateral nasal retina and the contralateral temporal retina. This indirect visual input to the SC ipsilateral to the optic tract section was absent in a cat with a section of the forebrain commissures. In Boston Siamese cats, section of one optic tract led to a virtually complete blindness in the eye contralateral to the section, whereas the other eye retained a full visual field, although the responsiveness of the temporal retina beyond 20 degrees from the vertical meridian was reduced. Similarly, the nasal hemiretina and most of the temporal hemiretina on the side of the section were represented in the opposite SC, whereas stimulation of the eye contralateral to the section could not drive SC units. There was some evidence that the visual field of the eye on the side of the section could at least in part be represented in the SC on the same side. The findings indicate that the crossed projections from temporal hemiretina in the ordinary cat, and the uncrossed projections from temporal hemiretina in the Siamese cat are insufficient by themselves to sustain visual orientation and to drive SC neurons. Each half of the visual field in the ordinary cat, and the field of each eye in the Siamese cat, can be represented in the ipsilateral SC via across-the-midline, indirect connections.

Learning and interhemispheric transfer of visual pattern discriminations following unilateral suprasylvian lesions in split-chiasm cats.

A suprasylvian lesion removing cortical areas 7 and 21 and portions of area 19 and of the lateral suprasylvian area was placed in one hemisphere of split-chiasm cats. By comparison with the normal side and with cortically intact split-chiasm and split-brain cats, form discrimination learning with the eye on the injured side was severely retarded. This deficit could not be attributed to an unintentional undercutting of areas 17 and 18, since in three cases the laminae of the lateral geniculate nucleus showed little retrograde atrophy; marked degeneration was found in the medial interlaminar nucleus and the pulvinar complex. In addition, interocular transfer of form discriminations to the eye on the injured side was absent or poor, while transfer in the opposite direction was normal. A cat with a suprasylvian lesion undercutting areas 17 and 18 was unable to learn pattern discriminations with the eye on the injured side, in spite of prolonged training with that eye and normal learning with the other eye. Another cat with a suprasylvian lesion selectively removing the anteromedial and posteromedial portions of the lateral suprasylvian area showed no learning deficit on the injured side, but poor transfer to that side. A learning deficit on the side of the lesion emerged in this cat after forebrain commissurotomy. The results support the hypothesis of a major involvement of cortical areas outside of 17 and 18 in the processes of abstraction and generalization of visual information necessary for learning and interhemispheric transfer of form discrimination in the cat.