Neuroplasticity in the cat’s visual system Origin, termination, expansion, and increased coupling of the retino-geniculo-middle suprasylvian visual pathway following early ablations of areas 17 and 18

We used anterograde and retrograde transsynaptic pathway tracing techniques to reveal the retinal origin and the cortical termination of the expanded retino-geniculo-middle suprasylvian (MS) cortex pathway in adult cats which sustained lesions of areas 17 and 18 on the day of birth (P1) or at 1 month of age (P28). Following anterograde transsynaptic transport of tritiated amino acids from the eye, four major results were obtained: (1) a strong and specific pathway from retina through dorsal lateral geniculate nucleus (dLGN) to the posterior half of MS cortex was identified; this pathway is a substantial expansion of an insignificant pathway present in intact cats; (2) the terminus of the pathway was lower layer III and layer IV; (3) contralateral projections were stronger than ipsilateral projections; (4) projections in P28 cats were stronger than those in P1 cats. Following retrograde transsynaptic transport of WGA-HRP from posterior MS cortex, four additional results were obtained: (1) the pathway was enlarged and visuotopically organized; (2) the pathway arose primarily from α- and γ-retinal ganglion cells; (3) a small number of β-cells in P1 cats and a modest number in P28 cats also contribute to the pathway; (4) the combined numbers of γ- and β-cells relative to α-cells was greater in temporal retina than in nasal retina. The combined demonstration of both origin and terminus of the pathway with transsynaptic tracers argued strongly for high levels of coupling between primary and secondary pathway limbs in both P1 and P28 cats. This level of coupling, as well as other features of the pathway, have much in common with the retino-geniculo-17/18 pathway of intact cats. However, the retino-geniculo-MS system in P1 cats transmits primarily Y and W signals, in P28 cats X, Y, and W signals; whereas the retino-geniculo-17/18 pathway transmits primarily X and Y signals. These results have implications for understanding the repercussions of early visual cortex lesions in monkeys and humans. Received: 17 November 1997 / Accepted: 10 February 1998     

Differential effects of prefrontal lesions and combined prefrontal and limbic lesions on subsequent learning performance in the cat

On the basis of a previous experiment (Irle & Markowitsch, 1983) in which triple limbic lesions as opposed to double limbic lesions in the cat failed to impair the learning behavior of these animals, the effects of a lesion in a fourth brain structure, in addition to the original ones, were examined. Two groups of cats were given lesions in either the prefrontal cortex alone or in the prefrontal cortex, the anterior thalamus, the mamillary bodies, and the subiculum and subsequently tested in the acquisition of a visual reversal, a delayed alternation, and an active two-way avoidance task. Compared with control cats, cats with prefrontal lesions were strongly impaired in the acquisition of the visual reversal task and the delayed alternation task but only slightly impaired in the acquisition of the active two-way avoidance task. In contrast, animals with combined prefrontal cortical, anterior thalamic, mamillary, and subicular lesions were unimpaired in the acquisition of the visual reversal task, slightly facilitated in the acquisition of the active two-way avoidance task, but impaired in the acquisition of the delayed alternation task similarly to the animals with prefrontal lesions. The superior performance rates of the animals with fourfold lesions are considered to be due to a lesion-induced functional shift acting on intact brain structures which, prior to massive limbic lesions, remain inhibited or otherwise suppressed. The failure of the animals with fourfold lesions in the delayed alternation task indicates that the functions underlying this type of behavior cannot be compensated for or, alternatively, that a prefrontal lesion is not sufficient to disinhibit other structures involved in the same behavior.     

Spatial Recognition in Cats: Effects of Parahippocampal Lesions

The role of the posterior parahippocampal area of the brain in spatial types of memory in conditions of one-trial visual perception of the positions of objects was studied by training eight cats to remember the spatial positions of either two different objects covering two of three feeders placed on a test tray (tests for the “object–place” association) or the positions of two of three feeders (tests for place). Each trial used new objects and new positions for the two of three feeders. After training, four cats were subjected to electrolytic lesioning of the posterior parahippocampal area, primarily the parahippocampal cortex, parasubiculum, and presubiculum; the remaining four cats underwent all the surgical procedures except electrocoagulation of nervous tissue; this was the sham-operated control group. Cats of this group showed no impairment to the performance of tests of both types, while the experimental group showed similar levels of impairment to the performance of both tests. Thus, memory for one-trial perception of “object–place” associations and, more simply, two different object places in cats were critically dependent on the posterior parahippocampal area. Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 58, No. 3, pp. 331–338, May–June, 2008.     

Increased oxidative metabolism in middle suprasylvian cortex following removal of areas 17 and 18 from newborn cats

We measured changes in metabolic activity in middle suprasylvian (MS) cortex of cats subjected to early or late removal of areas 17 and 18 to localize shifts in activity possibly indicative of regions within MS cortex that may receive expanded inputs and be involved in the sparing of some visual behaviors following early primary visual cortex damage. Cytochrome oxidase (CO) activity was measured in MS cortex of mature, intact cats and of others with areas 17 and 18 removed in adulthood (P180), or on postnatal day 28 (P28) or postnatal day 1 (P1). Not less than 9 months after the ablation, brain sections were prepared and reacted for the presence of CO. The density of CO reactivity in each of the six cortical layers in MS cortex was measured and standardized against densities from ventral periaqueductal gray or hypothalamus on the same section. Following lesions on P1, significant increases in CO activity occurred in deep layer III and in layer IV of the medial bank of the MS sulcus, including all of area PMLS and the posterior portion of AMLS. In contrast, there were no significant differences in the level of CO activity among P28, P180, or intact cats for any of the cortical layers, and all had lower levels than the P1 cats. This metabolic change provides an anatomical marker for localizing adjustments in MS cortex and can be linked to amplified projections into MS cortex from the thalamus (LPm and A and C laminae of the dorsal lateral geniculate nucleus) and ventral posterior suprasylvian cortex following P1 ablations. Furthermore, this neurochemical analysis implicates a distinct region of MS cortex as the cortical locus of some spared visual functions following early primary visual cortex damage.     

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)     

Neuroplasticity in the cat’s visual system: test of the role of the expanded retino-geniculo-parietal pathway in behavioral sparing following early lesions of visual cortex

Sparing of the ability to redirect head and eyes to new stimuli and expansion of the retino-geniculo-parietal pathway are both robust aspects of the repercussions of early lesions of occipital visual areas in cats. The purpose of the present work was to test the proposition that the pathway expansions and spared behaviors are causally linked. The proposition was tested by deactivating either the dorsal lateral geniculate nucleus (dLGN) and thereby uncoupling the primary and secondary limbs of the retino-geniculo-parietal pathway, or silencing the terminus of the pathway, and then testing the ability of cats to detect and orient head and eyes to visual targets. Six cats sustained experimental unilateral lesions of occipital areas 17 and 18 and variable amounts of area 19 on postnatal days 1-2 or 26-30 to induce rewiring and expansion of visual pathways from retina through the dLGN onto a critical region of visuoparietal (VP) cortex. Unilateral lesions ensured that we could use the orienting performance of the intact hemisphere as a fiduciary marker of performance against which performance of the experimental hemisphere could be gauged. When the cats were adult, a secondary test lesion was made on the damaged side by injecting, under electrophysiological guidance, ibotenic acid into either dLGN of four cats or into VP cortex of two cats. Prior to injection of ibotenic acid, all cats oriented head and eyes with high proficiency throughout the contralesional field, and performance was indistinguishable from orienting to stimuli presented in the ipsilesional field; sparing of the orienting behavior was complete. Ibotenic acid lesions of both dLGN and VP cortex induced a profound neglect of stimuli introduced into the contralesional hemifield. Orienting into the ipsilesional field remained high throughout. Subsequently, there was restoration of orienting behavior over the next 4-6 (dLGN deactivation) and 9-12 (VP deactivation) days. The test results demonstrate the essential contribution made by the retino-geniculo-parietal pathway to the ability to detect and redirect head and eyes to look at visual stimuli following early lesions of occipital visual cortices. The subsequent post-test lesion restoration of high orienting proficiency shows that in the absence of dLGN, or the critical region of VP cortex, other regions of cerebral cortex, or other structures such as the superior colliculus, can emerge and make important contributions to orienting behavior. These results reveal a maintained residual, beneficial adaptive plasticity of mature neural circuits even in brains compromised by early lesions of occipital visual areas.     

Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory

Despite the connections of the retrosplenial cortex strongly suggesting a role in spatial memory, the lesion data to date have been equivocal. Whether subjects are impaired after retrosplenial lesions seems to depend on whether the lesions were aspirative or excitotoxic, with the latter failing to produce an impairment. A shortcoming of previous excitotoxic lesion studies is that they spared the most caudal part of the retrosplenial cortex. The present study thus used rats with extensive neurotoxic lesions of the retrosplenial cortex that encompassed the entire rostrocaudal extent of this region. These rats were consistently impaired on several tests that tax allocentric memory. In contrast, they were unimpaired on an egocentric discrimination task. Although the lesions did not appear to affect object recognition, clear deficits were found for an object-in-place discrimination. The present study not only demonstrates a role for the retrosplenial cortex in allocentric spatial memory, but also explains why previous excitotoxic lesions have failed to detect any deficits.     

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.     

Spatial and temporal summation in impaired regions of the visual field

1. Spatial and temporal summation have been measured in perimetrically impaired regions of the visual field. Two classes of impairment have been studied: that resulting from lesions in the pre-geniculate visual pathways, and that resulting from post-geniculate lesions (optic radiation and/or striate cortex).2. Control measurements were made in the perimetrically normal visual fields of subjects without visual pathway damage.3. Spatial summation was found altered in all impaired visual fields: the greater the threshold elevation produced by the lesion, the more nearly complete was spatial summation.4. The above relation between threshold and spatial summation has also been given numerical form. This has been shown to be very nearly identical to the threshold-spatial summation relation which is seen as stimuli are increasingly peripherally presented in normal visual fields.5. It has been shown that the alterations of spatial summation brought about by a lesion are found only in those parts of the visual field which are perimetrically impaired: spatial summation is always normal in perimetrically normal regions of a visual field, even if other parts of the same field show impairment.6. Temporal summation has been found altered in visual fields impaired by post-geniculate lesions: the greater the threshold elevation produced by the lesion, the more nearly complete was temporal summation. These changes in temporal summation were found only in perimetrically impaired regions of the field.7. Temporal summation was normal in visual fields impaired by pregeniculate lesions.     

Viewing the body modulates tactile receptive fields

Tactile discrimination performance depends on the receptive field (RF) size of somatosensory cortical (SI) neurons. Psychophysical masking effects can reveal the RF of an idealized “virtual” somatosensory neuron. Previous studies show that top–down factors strongly affect tactile discrimination performance. Here, we show that non-informative vision of the touched body part influences tactile discrimination by modulating tactile RFs. Ten subjects performed spatial discrimination between touch locations on the forearm. Performance was improved when subjects saw their forearm compared to viewing a neutral object in the same location. The extent of visual information was relevant, since restricted view of the forearm did not have this enhancing effect. Vibrotactile maskers were placed symmetrically on either side of the tactile target locations, at two different distances. Overall, masking significantly impaired discrimination performance, but the spatial gradient of masking depended on what subjects viewed. Viewing the body reduced the effect of distant maskers, but enhanced the effect of close maskers, as compared to viewing a neutral object. We propose that viewing the body improves functional touch by sharpening tactile RFs in an early somatosensory map. Top–down modulation of lateral inhibition could underlie these effects.     

Selective visual neglect in right brain damaged patients with splenial interhemispheric disconnection

Left unilateral neglect is frequently reported after right hemispheric lesions of the middle cerebral artery (MCA) damaging the parietal–frontal cortical–subcortical network subserving space representation and awareness. However, accumulating evidence shows that neglect can also follow lesions of the posterior cerebral artery (PCA) that do not directly affect this parietal–frontal network. Surgical studies in the monkeys have demonstrated that complete callosal resection combined with lesion of the right optic tract entirely deprives the right hemisphere of visual inputs from the left hemispace provoking severe left unilateral neglect. Here, through the detailed study of two patients we show, for the first time, that PCA lesions selectively affecting the splenium of the corpus callosum and the adjacent right primary visual cortex provoke severe neglect selectively restricted to the visual domain. No trace of personal, motor or representational-imagery neglect was found. Also at variance with previous case studies in which neglect followed lesion of the trunk or the genu of the corpus callosum, no restriction of neglect to tasks performed with the right hand, no left hemispatial limb akinesia, no tactile extinction for the left hand and no tactile anomia for stimuli explored with the left hand were observed. These findings demonstrate that brain lesions depriving intact parietal and frontal attentional areas from specific sensory inputs can yield spatial neglect limited to specific sensory modalities or sectors of space.     

Recognition of lateralized halftone and outline images of everyday objects in conditions of masking

Recognition of the shapes of halftone and outline images of everyday objects in conditions of lateralized tachystoscopic presentation and different levels of noise masking (with “raindrops”) by humans was studied. Mean group data for 15 subjects demonstrated significantly better recognition of outline images of everyday objects by the left hemisphere of the brain than the right at all levels of masking. Increases in masking produced gradual and significant degradation of recognition as compared with controls (recognition of unmasked figures). Recognition of outline images at all levels of masking was significantly better than recognition of halftone images of the same objects. In men, there were no significant differences between hemispheres either at different levels of masking or for different types of stimuli. The neurophysiological mechanisms and functional significance of these effects are discussed. Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavliva, Vol. 58, No. 1, pp. 56–62, January–February, 2008.     

Participation of the anterior suprasylvian cortex of the cat in the preparation of the paw extension reaction

The electrical stimulation of the anterior suprasylvian cortex of cats (field 5b) induces the contralateral forepaw extension reaction. Neurons were recorded in the focus of effective stimulation which were tonically activated under the influence of motivationally significant visual and tactile stimuli which anticipate or elicit the reactions of paw extension and/or paw placement on a support. M. V. Lomonosov Moscow State University. Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 44, No. 1, pp. 40–47, January–February, 1994.     

Visual evoked potentials in humans during recognition of emotional facial expressions

Visual evoked potentials were recorded from the occipital, parietal, central, frontal, and posterior temporal areas of the cortex during recognition of emotionally positive, negative and neutral facial expressions and during passive observation in 22 right-handed healthy subjects. These studies showed that in the posterior temporal areas, the latencies of the N90, P150, and N180 waves of potentials evoked by faces with emotionally negative expressions were significantly shorter than those evoked by other types of facial stimuli. Differences were seen both on recognition and during passive observation. Correct recognition involved both hemispheres and was characterized by high levels of interhemisphere temporal correlation of the processes occurring during the development of the P150 wave in the posterior temporal and the N180 wave in the frontal parts of the cortex. The possible relationship of these data to primary subthreshold recognition of facial expressions in the posterior temporal fields of the cortex is discussed, as is the role of the frontal cortex in completing this process and in taking the correct decision about the nature of the image. Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 48, No. 5, pp. 797–806, September–October, 1998.     

Low frequency transcranial magnetic stimulation on the posterior parietal cortex induces visuotopically specific neglect-like syndrome

The visuo-parietal (VP) region of the cerebral cortex is critically involved in the generation of orienting responses towards visual stimuli. In this study we use repetitive transcranial magnetic stimulation (rTMS) to unilaterally and non-invasively deactivate the VP cortex during a simple spatial visual detection task tested in real space. Adult cats were intensively trained over 4 months on a task requiring them to detect and orient to a peripheral punctuate static LED presented at a peripheral location between 0° and 90°, to the right or left of a 0° fixation target. In 16 different interleaved sessions, real or sham low frequency (1 Hz) rTMS was unilaterally applied during 20 min (1,200 pulses) to the VP cortex. The percentage of mistakes detecting and orienting to contralateral visual targets increased significantly during the 15–20 min immediately following real but not sham rTMS. Behavioral deficits were most marked in peripheral eccentricities, whereas more central locations were largely unaffected. Performance returned to baseline (pre-TMS) levels when animals were tested 45 min later and remained in pre-TMS levels 24 h after the end of the stimulation. Our results confirm that the VP cortex of the cat is critical for successful detection and orienting to visual stimuli presented in the corresponding contralateral visual field. In addition, we show that rTMS disrupts a robust behavioral task known to depend on VP cortex and does so for the far periphery of the visual field, but not for more central targets.Prof. Payne passed away May 2004. This article is submitted in his memory.     

The effects of the experience of forming visual images on the spatial organization of the EEG

The spatial organization of biopotentials in the cerebral cortex of 23 subjects who were students at the Faculty of Graphic Arts (“professionals”) as well as 39 subjects lacking systematic experience of visual images (“non-professionals”) was compared with the aim of identifying EEG correlates of the experience of visual images (image formation) in humans. Changes in measures of the spatial organization of biopotentials (spatial synchronization, spatial disordering, coherence, and spectral power) were analyzed as subjects mentally composed visual images consisting of two simple graphic elements — right angles and oblique lines. The total number of image elements increased in each of four sequential tasks, from a number which could be analyzed at the conscious level (4–7 elements) to a number exceeding analysis at the conscious level (8–16). Intergroup differences, particularly increases in the spatial disordering of biopotentials (non-linear processes), were detected when large numbers of elements were used (tasks 3 and 4). This measure increased more markedly in professionals than in non-professionals. Changes were significant in the anterior areas of the right hemisphere. Spatial synchronization of biopotentials (linear processes) increased in non-professionals in the posterior areas of the right hemisphere. Coherence and spectral power increased in professionals in a larger number of narrow-band EEG frequency subranges than in non-professionals. These data show that experience of visual imagery results in a more complex neurodynamic process during the activity, with non-linear dynamics and a multitude of EEG resonance systems at different frequencies. __________ Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 55, No. 6, pp. 812–821, November–December, 2005.     

Tuning of striate neurons to cross-shaped figures in conditions of local blockade of intracortical inhibition

The recently observed selective sensitivity to cross-shaped and angular figures was studied in 85 primary visual cortex (field 17) neurons in cats before and after local blockade of GABA_A ergic inhibition by microiontophoretic application of the GABA antagonist bicuculline. Two opposite effects were seen: half of the neurons studied showed decreases or complete loss of sensitivity to crosses, and a third of the cells showed increases or the appearance of sensitivity to crosses. These data provide evidence for significant roles for intracortical inhibition in providing sensitivity to crosses and intersecting lines in two types of visual cortex neurons, the effects on these two types of neuron being opposite. Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti, Vol. 49, No. 2, pp. 271–278, March–April, 1999.     

Visual–spatial and anatomical constraints interact in a bimanual coordination task with transformed visual feedback

There is a debate in the literature about the influence of spatial and anatomical constraints on bimanual coordination dynamics. In the present experiment, participants swung hand-held pendulums about the wrist while attending to visual feedback about relative phase (superimposed phase plots of each pendulum) that was displayed on a screen. Participants were instructed to maintain in-phase or anti-phase coordination in the visual display. Visual–spatial and anatomical constraints were dissociated by introducing a phase shift in the visual display so that visual feedback differed from the movements being performed by the participants in 15° increments from −180° to +180°. Analysis of mean relative phase and its variability suggested that visual–spatial and anatomical constraints interact in bimanual coordination dynamics.     

Neurochemical cellular mechanisms of the assessment of the results of behavioral activity

Neurons of the visual area of the cerebral cortex of cats were investigated at various stages of alimentary instrumental behavioral activity. The impulse activity of the neurons was recorded both during standard food-procuring behavior and during the performance of an instrumental reaction without reinforcement. Biologically active substances were applied microiontophoretically to the neurons in the experiment. Varying chemical sensitivity of individual neurons to neuromediators was established in both experimental situations, as was the significance of the mechanisms of protein synthesis for these processes. Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 43, No. 2, pp. 326–332, March–April, 1993.     

Neuronal activity of somatosensory cortex in a cross-modal (visuo-haptic) memory task

Studies have shown that in the monkey′s associative cerebral cortex, cells undergo sustained activation of discharge while the animal retains information for a subsequent action. Recent work has revealed the presence of such ″memory cells″ in the anterior parietal cortex (Brodmann′s areas 3a, 3b, 1, and 2) – the early stage of the cortical somatosensory system. Here we inferred that, in a cross-modal visuo-haptic short-term memory task, somatosensory cells would react to visual stimuli associated with tactile features. Single-unit discharge was recorded from the anterior parietal cortex – including areas of hand representation – of monkeys performing a visuo-haptic delayed matching-to-sample task. Units changed firing frequency during the presentation of a visual cue that the animal had to remember for making a correct tactile choice between two objects at the end of a delay (retention period). Some units showed sustained activation during the delay. In some of them that activation differed depending on the cue. These findings suggest that units in somatosensory cortex react to visual stimuli behaviorally associated with tactile information. Further, the results suggest that some of these neurons are involved in short-term active memory and may, therefore, be part of cross-modal memory networks. Received: 24 March 1997 / Accepted: 8 May 1997