Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens

Summary Previous studies have shown that functional compensation is present in the cat's posteromedial lateral suprasylvian (PMLS) area of cortex after damage to areas 17, 18, and 19 (visual cortex) early in life but not after damage in adults. These studies all have investigated animals with a unilateral visual cortex lesion, whereas all behavioral studies of compensation for early visual cortex damage have investigated animals with a bilateral lesion. In the present experiment, we investigated whether functional compensation also is present in PMLS cortex after a bilateral visual cortex lesion early in life. We recorded from single neurons in the PMLS cortex of adult cats that had received a bilateral lesion of areas 17, 18, and 19 on the day of birth or at 8 weeks of age. We found that PMLS cells in both groups of cats had functional compensation (normal direction selectivity and ocular dominance) similar to that seen after a unilateral lesion at the same ages. These results are consistent with the hypothesis that PMLS cortex is involved in the behavioral compensation seen after early visual cortex damage. In addition, the results indicate that inputs from contralateral visual cortex are not necessary for the development of functional compensation seen in PMLS cortex.     

Effects of visual cortex lesions following recovery from monocular deprivation in the cat

Six monocularly deprived (MD) and four normal cats were trained monocularly on two-choice form and pattern discriminations. MD cats trained through the initially deprived eye were able to learn the discriminations; however, they required many more trials than normals. Retention tests showed that MD cats have nearly perfect retention of the discriminations over periods of up to 4 months. With retention intervals of 6 months or longer, there is a tendency for the MD cats to show an initial drop in performance, particularly on more difficult discriminations. However, criterion performance typically was attained with considerable savings, indicating good retention even over these extended intervals. Following the preoperative training and retention testing, the cats received one of the three types of visual cortex lesions. Two MD cats received total visual cortex removal (areas 17, 18, and 19). This produced a complete postoperative loss of the discriminations with continued chance performance over 800--1000 trials. Two MD cats and two normal cats received removal of the monocular segment of area 17, with the central visual field projection region of area 17 and all of areas 18 and 19 remaining intact. This produced no loss of the discriminations in either normal or MD cats beyond what is expected on the basis of normal forgetting. Two MD cats and two normal cats received removal of areas 18, 19, and the central 5--10 deg. of the visual field projection in area 17. Postoperative retention was somewhat variable for both normal and MD cats. However, subsequent acquisition of the discriminations by both normal and MD cats was in sharp contrast to the prolonged deficits produced by total visual cortex lesions. These results indicate that one or more of visual cortical areas 17, 18, and 19 are involved in the recovery of visual discrimination capacities in MD cats. However, the monocular segment of striate cortex does not appear to be specially involved in this ability, as has been suggested by previous investigations. Possible mechanisms for the recovered visual capacities in MD cats are considered.     

How complete is physiological compensation in extrastriate cortex after visual cortex damage in kittens?

Summary Previous studies indicate that neurons in the cat's posteromedial lateral suprasylvian (PMLS) visual area of cortex show physiological compensation after neonatal but not adult damage to areas 17, 18, and 19 of the visual cortex (collectively, VC). Thus, VC damage in adults produces a loss of direction selectivity and a decrease in response to the ipsilateral eye among PMLS cells, but these changes are not seen in adult cats that received VC damage as kittens. This represents compensation for early VC damage in the sense that PMLS neurons develop properties they would have had if there had been no brain damage. However, this is only a partial compensation for the effects of VC damage. A full compensation would involve development of properties of the VC cells that were removed in the damage. The present study investigated whether this type of compensation occurs for detailed spatial- and temporal-frequency processing. Single-cell recordings were made in PMLS cortex of adult cats that had received a VC lesion on the day of birth or at 8 weeks of age. Responses to sine-wave gratings that varied in spatial frequency, contrast, and temporal frequency were assessed quantitatively. We found that the spatial- and temporal-frequency processing of PMLS cells in adult cats that had neonatal VC damage were not significantly different from PMLS cells in normal cats. Therefore, there was no evidence that PMLS cells can compensate for VC damage by developing properties that are better than normal and like those of the striate cortex cells that were damaged.We also assessed the effects of long-term VC damage in adult cats to determine whether the normal properties seen in cats with neonatal VC damage represent a compensation for abnormalities in PMLS cortex present after adult damage. In a previous study, we found that acute VC damage in adult cats has small but reliable effects on maximal response amplitude, maximal contrast sensitivity, and spatial resolution (Guido et al. 1990b). In the present study, we found that long-term VC damage in adult cats does not increase these abnormalities as a result of secondary degenerative changes. In fact, the minor abnormalities that were present after an acute VC lesion were virtually absent following a long-term adult lesion, perhaps because they were due to transient traumatic effects. Therefore, there was little evidence for abnormalities in spatial- or temporal-frequency processing following long-term adult VC damage for which PMLS cells might show compensation following long-term neonatal damage.Our results thus indicate that there is little or no difference in the spatial- or temporal-frequency processing of PMLS cells in normal cats and cats with long-term VC damage received early in life or as adults. These findings are discussed in relation to the inputs to PMLS cortex and to the behavioral abilities of cats with VC damage at different ages. The implications for under-standing the role of lateral suprasylvian visual cortex in behavioral recovery from VC damage is considered.     

Deficits in visual learning by cats with lesions of the visual cortex

Cats were trained for food reward in a divided straight maze or in a V-maze on a light-dark discrimination and on a series of horizontal-vertical stripe discriminations. Errors were scored by both door-push and alley-entrance criteria. After lesions of the visual cortex, cats could relearn or initially learn the light-dark discrimination but were not successfully trained to shift from brightness to pattern cues when learning the series of horizontal-vertical stripe discriminations, using a modified method of limits procedure. Both unoperated cats and cats with lesions of the visual cortex committed alley-entrance errors when learning the light-dark discrimination.     

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

Summary 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.     

Bilateral projections from the visual cortex to the striatum in the cat

Summary Direct projections from visual areas 17, 18, 19, and lateral suprasylvian visual area (LS) to the striatum were searched for in 12 adult cats using the autoradiographic technique to detect neuronal pathways. Striatal labels were found only after injections in areas 19 and LS. Projections homolateral to the injection sites were observed from both areas to the head and body of the caudate nucleus and to the putamen. Contralateral projections were found from both areas 19 and LS: however, area 19 did not project to the contralateral putamen. The extent of contralateral projections was smaller and they were confined within the same regions as the homolateral ones. Silver grains were often arranged in cluster-like patches, which were more evident ipsilaterally, in the head of the caudate nucleus and after injections in area LS.The present data support the view of a not strictly topographical segregation of striatal projections from the cat visual cortex.Supported by a grant from the CNR, Rome, Italy     

Critical periods for functional and anatomical compensation in lateral suprasylvian visual area following removal of visual cortex in cats

Previous experiments have found that neurons in the cat's lateral suprasylvian (LS) visual area of cortex show functional compensation following removal of visual cortical areas 17, 18, and 19 on the day of birth. Correspondingly, an enhanced retino-thalamic pathway to LS cortex develops in these cats. The present experiments investigated the critical periods for these changes. Unilateral lesions of areas 17, 18, and 19 were made in cats ranging in age from 1 day postnatal to 26 wk. When the cats were adult, single-cell recordings were made from LS cortex ipsilateral to the lesion. In addition, transneuronal autoradiographic methods were used to trace the retino-thalamic projections to LS cortex in many of the same animals. Following lesions in 18- and 26-wk-old cats, there is a marked reduction in direction-selective LS cortex cells and an increase in cells that respond best to stationary flashing stimuli. These results are similar to those following visual cortex lesions in adult cats. In contrast, the percentages of cells with these properties are normal following lesions made from 1 day to 12 wk of age. Thus the critical period for development of direction selectivity and greater responses to moving than to stationary flashing stimuli in LS cortex following a visual cortex lesion ends between 12 and 18 wk of age. Following lesions in 26-wk-old cats, there is a decrease in the percentage of cells that respond to the ipsilateral eye, which is similar to results following visual cortex lesions in adult cats. However, ocular dominance is normal following lesions made from 1 day to 18 wk of age. Thus the critical period for development of responses to the ipsilateral eye following a lesion ends between 18 and 26 wk of age. Following visual cortex lesions in 2-, 4-, or 8-wk-old cats, about 30% of the LS cortex cells display orientation selectivity to elongated slits of light. In contrast, few or no cells display this property in normal adult cats, cats with lesions made on the day of birth, or cats with lesions made at 12 wk of age or later. Thus an anomalous property develops for many LS cells, and the critical period for this property begins later (between 1 day and 2 wk) and ends earlier (between 8 and 12 wk) than those for other properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

Cross-modal plasticity after monocular enucleation of the adult rabbit

The mature brain undergoes compensatory reorganization of the primary visual cortex (V1) in response to retinal lesions. This study demonstrates that V1 also supports cross-modal reorganization by observing an increase in tactile responses in V1 after monocular enucleation of the adult rabbit. The proportion of tactile-responsive V1 neurons increased from 0% to 31%, in an area of cortex equivalent to 40 degrees of visual space. Retrograde fiber-tracing analysis suggests that intracortical connections from association areas may underlie these novel responses. Cortical plasticity of this kind may be involved in recovery from sensory system damage and could provide an enhanced sense of touch to the blind.     

Abolition of visual cortical direction selectivity affects visual behavior in cats

Summary We reared cats in an environment illuminated stroboscopically at 8 Hz, and studied their ability to detect and discriminate the direction of motion of sinusoidal gratings. Normal cats, like humans, could discriminate the direction of a grating's motion at contrasts that are just barely visible. Strobe-reared cats could detect the grating at contrasts similar to those required by normal cats, but required contrasts that were about 10 times threshold to identify the direction of motion. We subsequently studied the activity of single units in the striate cortex in these cats, and found that directional motion selectivity — normally a prominant feature of striate cortical neurons — was almost absent; other cortical receptive field properties were roughly normal. These results suggest that directionally selective neurons are involved in visual discriminations based on the direction of motion.     

Lesions of extrastriate cortex and consequences for visual guidance during locomotion

One of the functions of the putative motion pathway in visual cortex may be visual guidance during locomotion. Using cats, we have investigated the role of the first area in this pathway, the lateral suprasylvian visual area (LS, often considered analogous to the primate area MT). Visual function during locomotion was tested by looking at the accuracy of foot placement as cats walked down a cluttered alley. Cats were tested before and after LS was lesioned bilaterally using ibotenic acid. In all four cats tested, partial lesions of LS caused a significant deterioration in the accuracy of foot placement, though cats showed no deficit in acuity or in pattern discrimination. To determine whether the observed deficit was specific to the motion pathway, in two additional cats lesions were made in the central field representation in area 19, which lies adjacent to LS but belongs to the putative object recognition pathway. Surprisingly, both cats showed significant improvements in their accuracy of foot placement during locomotion. The reason for this improvement was unclear.     

The primate visual system after bilateral removal of striate cortex

Summary This study examined the strategies used by monkeys lacking striate cortex to perform visual pattern discriminations. Complete bilateral removal of area 17 initially produced severe visual impairment with recovery of even rudimentary visual capacities (e.g., flux discrimination) dependent on gradually retraining the monkeys through a set of increasingly more complex pattern discriminations. After extended periods of postoperative testing, however, three of five monkeys lacking striate cortex were able to discriminate a number of complex visual patterns even when such local stimulus cues as amount of contour and number of elements were equal. Further testing demonstrated that these animals could distinguish a pattern's spatial organization. They were also able to transfer good performance to tasks with novel patterns.This work was supported by USPHS Grants NS 10576 and EY 02941, and by the Veteran's Administration Research Service to E. G. Keating     

Change in the pattern of behavioural specialization of neurons in the motor cortex of the rabbit following lesion of the visual cortex

In order to find out whether damage of the visual cortex (area 17) of the brain results in a functional reorganization of the motor cortex, experiments were carried out with freely moving rabbits performing a food acquisition task in an experimental cage. Two rabbits served as controls, while in three rabbits the visual cortex was bilaterally damaged. Analysis of the activity of 575 neurons in the control and operated rabbits after the recovery of the original instrumental food acquisition behaviour revealed a marked difference in the behavioural specialization of the neurons in the motor cortex of two operated rabbits compared with the control animals. Although the same types of units as in the control rabbits could be found in the operated rabbits (M neurons activated in relation to body and limb movements, S neurons activated in relation to food seizure and L neurons activated in relation to learned food acquisition task), the number of S units was about half of that in the controls and the number of L units about double. The relative number of activations of the neurons in the operated rabbits was significantly less frequent during the food seizure and more frequent during the learned behaviour. This difference indicates a change in the pattern of behavioural specialization of the neurons in the motor cortex due to the damage of the visual cortex. In this reorganization, the motor cortex became more like (but not identical to) visual and limbic cortices that normally contain noticeably more L neurons than the motor cortex. The number of neurons activated in relation to the behaviour in the operated rabbits, as compared with the control animals, was smaller in the upper and larger in the lower layers of the motor cortex. This may indicate recruitment of new neurons from the lower cortical layers.     

Competition and convergence between auditory and cross-modal visual inputs to primary auditory cortical areas

Sensory neocortex is capable of considerable plasticity after sensory deprivation or damage to input pathways, especially early in development. Although plasticity can often be restorative, sometimes novel, ectopic inputs invade the affected cortical area. Invading inputs from other sensory modalities may compromise the original function or even take over, imposing a new function and preventing recovery. Using ferrets whose retinal axons were rerouted into auditory thalamus at birth, we were able to examine the effect of varying the degree of ectopic, cross-modal input on reorganization of developing auditory cortex. In particular, we assayed whether the invading visual inputs and the existing auditory inputs competed for or shared postsynaptic targets and whether the convergence of input modalities would induce multisensory processing. We demonstrate that although the cross-modal inputs create new visual neurons in auditory cortex, some auditory processing remains. The degree of damage to auditory input to the medial geniculate nucleus was directly related to the proportion of visual neurons in auditory cortex, suggesting that the visual and residual auditory inputs compete for cortical territory. Visual neurons were not segregated from auditory neurons but shared target space even on individual target cells, substantially increasing the proportion of multisensory neurons. Thus spatial convergence of visual and auditory input modalities may be sufficient to expand multisensory representations. Together these findings argue that early, patterned visual activity does not drive segregation of visual and auditory afferents and suggest that auditory function might be compromised by converging visual inputs. These results indicate possible ways in which multisensory cortical areas may form during development and evolution. They also suggest that rehabilitative strategies designed to promote recovery of function after sensory deprivation or damage need to take into account that sensory cortex may become substantially more multisensory after alteration of its input during development.     

Amphetamine-induced recovery of visual cliff performance after bilateral visual cortex ablation in cats: measurements of depth perception thresholds

After bilateral visual cortex ablation, cats exhibit a loss of depth perception as measured on a visual cliff, which recovers following administration of d-amphetamine. In this Study, 3 amphetamine-treated cats with visual cortex ablations showed a rapid and enduring recovery, with 2 of these animals obtaining levels of performance seen only with binocular vision, suggesting a restoration of binocular depth perception. Cats with asymmetrical lesions showed only a transient improvement during amphetamine treatment, and some animals not displaying autonomic signs of amphetamine intoxication did not improve. Saline-treated cats showed no signs of improvement, and the effect of amphetamine was blocked by the catecholaminergic antagonist haloperidol. These results indicate that amphetamine can induce an enduring recovery from a behavioral deficit after brain injury, which if left untreated would not spontaneously recover.     

Feedback training of 36 - 44 HZ EEG activity in the visual cortex and hippocampus of cats: evidence for sensory and motor involvement

Milk reinforcement was contingent on the occurrence of 36 -44 (40) Hz EEG activity in the left visual cortex (VC) of one group of cats and in the right hippocampus (H) of a second group. Both groups learned to increase 40 Hz activity, and acquisition of reinforcement was associated with immobility. A third group (behavioral controls - BC) was trained by the method of successive approximation to behave in a similar manner to VC and H cats. Training significantly increased 40 Hz activity in all of the following structures, except the hippocampi of VC cats and between the right and left visual cortex of H and BC cats: posterior primary visual cortex (bilateral), anterior primary visual cortex (left), primary motor cortex (bilateral), dorsal hippocampus (bilateral), and midbrain reticular formation (bilateral). Since the behavioral and EEG changes of H and BC animals were similar, immobility appears to be important for increased hippocampal 40 Hz activity produced by feedback training. Testing in darkness enhanced 40 Hz activity in the trained area of VC cats but had no effect on H or BC animals. These results, in conjunction with the observation that VC cats appeared to visually fixate, suggest that VC cats may have learned to increase 40 Hz activity in the visual cortex by altering visual processing.     

Alternation behavior of cats with medial visual cortex ablation

Previous work by Lubar et al. [15] showed that cats with medial visual cortex ablation were impaired in acquisition of two-way active avoidance while pattern discrimination and gross behavior remained normal. In the present study cats with comparable ablations served in 6 experiments involving visual and nonvisual spatial alternation in a two-choice Yerkes alley as well as home cage and neurological observations. Animals with ablations were significantly impaired in (1) a spatial alternation task; (2) spatial alternation after peripheral occlusion; (3) a reversal using pattern and spatial elements; (4) one-way active avoidance with shock punishment; (5) a form discrimination requiring spatial alternation. Experimental animals were equal to controls in alternation using only a single cue. The deficits observed mainly involved acquisition and were in all but two cases reduced by training. The exceptions were (2) peripheral occlusion and (3) reversal learning. Though grossly and neurologically normal, experimental animals had higher home cage activity and vocalization levels than controls. The results are evaluated in terms of visual and nonvisual functions of the visual cortex.     

Sequential auditory and visual discriminations after temporal lobe ablation in monkeys

Studies in the monkey have shown that cortex outside of the primary projection areas in the superior temporal gyrus and in the inferotemporal region in important for the execution of some auditory and visual descriminations. In this study, six monkeys were trained to perform four auditory and two visual discriminations. Retention tests were given prior to bilateral removal of the anterior part of the lateral surface of the superior temporal gyrus, the inferotemporal region, or both areas together. Superior temporal ablations elicited severe deficits on some auditory discriminations. Inferotemporal ablations caused little or no impairment on visual discriminations. This negative finding is attributed to the sequential rather than spatial mode of presentation of visual stimuli, and to overtraining. A single monkey trained on a spatial visual pattern problem without overtraining was impaired. Another monkey tranied to perform an auditory reverse intensity discrimination exhibited a deficit in ability to perform the problem after removal of auditory cortex within the lateral fissure.     

A comparison of magnification functions in area 19 and the lateral suprasylvian visual area in the cat

A retinotopic map can be described by a magnification function that relates magnification factor to visual field eccentricity. Magnification factor for primary visual cortex (VI) in both the cat and the macaque monkey is directly proportional to retinal ganglion cell density. However, among those extrastriate areas for which a magnification function has been described, this is often not the case. Deviations from the pattern established in V1 are of considerable interest because they may provide insight into an extrastriate area's role in visual processing. The present study explored the magnification function for the lateral suprasylvian area (LS) in the cat. Because of its complex retinotopic organization, magnification was calculated indirectly using the known magnification function for area 19. Small tracer injections were made in area 17, and the extent of anterograde label in LS and in area 19 was measured. Using the ratio of cortical area labeled in LS to that in area 19, and the known magnification factor for area 19 at the corresponding retinotopic location, we were able to calculate magnification factor for LS. We found that the magnification function for LS differed substantially from that for area 19: central visual field was expanded, and peripheral field compressed in LS compared with area 19. Additionally, we found that the lower vertical meridian's representation was compressed relative to that of the horizontal meridian. We also examined receptive field size in areas 17, 19, and LS and found that, for all three areas, receptive field size was inversely proportional to magnification factor.     

Effects of lesions of areas 17, 18 and 19 on interocular transfer of pattern discriminations in split-chiasm cats

Summary Split-chiasm cats with unilateral or bilateral lesions largely removing the commissurally connected portions of visual cortical areas 17, 18 and 19 showed good interocular transfer of monocularly learned pattern discriminations. The capacity for interocular transfer in these cats was in fact little or not different from that of split-chiasm cats with an intact cortex. Split-chiasm cats with an additional section of the forebrain commissures, as well as two split-chiasm cats with 17–18 lesions also submitted to forebrain commissurotomy after having shown good interocular transfer, were generally incapable of transferring pattern discriminations between the eyes. It is concluded that interocular transfer of pattern discriminations, in split-chiasm cats does not require areas 17, 18 and 19 and must therefore depend on other cortical areas.     

Callosal agenesis and absence of primary visual cortex induced by prenatal X rays impair navigation's strategy and learning in tasks involving visuo-spatial working but not reference memory in mice

This study was designed for the identification of possible and distinct abilities for behavioral recovery after prenatal cerebral damage. We adopted an interesting tool for promotion of cell's death. Due to the fact that neuroblastic cells and early postmitotic neurons on the beginning of differentiation are particularly sensible for the promotion of apoptosis, we used a low whole-body dose of X radiation on pregnant female mice on E16 (sixteenth gestational day) to promote damage on specific cerebral areas of the progeny, given that the pattern of cerebral neurogenesis is not homogeneous. The morphological results were previously described by our team. Here we noticed that the recovery of behavioral functions after prenatal damage seems to be related to specific factors of local cortical circuitry organization. The deficits found on visual navigation and working memory contrast with the recovery of primary visual functions and also with reference memory, where the mice have a delay on acquisition of learning but get it. As a conclusion we reasoning that changes on laminar organization on frontal cortex as well as the inter hemispheric cortical integration through the corpus callosum could promote relatively fixed cognitive dysfunctions, as those observed on performances that require strategies for navigation (decision making) and working memory, with consequences also observed on the subsequent learning.