Role of the lateral suprasylvian visual area in behavioral recovery from effects of visual cortex damage in cats

The purpose of the present experiment was to determine the specific cortical areas involved in the behavioral recovery observed after visual cortex damage. Eight cats were trained preoperatively on brightness, form and pattern discriminations. They then underwent bilateral removal of visual cortical areas 17, 18, and 19. Postoperatively, the cats showed a loss of the learned discriminations. In agreement with previous studies, they were able to recover their visual discrimination ability, and all 8 cats reattained criterion performance on all three discriminations. Retention tests of the postoperatively learned tasks were then conducted after a period of 40 days or more. They showed that cats with visual cortex lesions have good retention of easier discriminations, but show some forgetting of more difficult tasks.Following the visual cortex lesion and recovery, 4 cats received a second lesion of the crown of the middle and posterior suprasylvian gyri (CROWN group). This produced no loss of the discriminations beyond what is expected on the basis of forgetting, as determined by the retention tests. The remaining cats received a second lesion which included the lateral suprasylvian visual area in the middle and posterior suprasylvian sulci (LS group). In two of these animals, the lesion also damaged some of the crown of the suprasylvian gyrus (LS + CROWN group). These lesions produced a second loss of the form and pattern discriminations, and relearning was more prolonged than that following damage to visual cortex alone. There was no difference between the LS and the LS + CROWN groups.These results indicate that the lateral suprasylvian visual area plays an important role in the behavioral recovery of form and pattern discrimination ability following visual cortex damage in cats.     

Rats with lesions in anteromedial extrastriate cortex fail to learn a visuosomatic conditional response

The involvement of rat anteromedial extrastriate cortex (area AM, in the anterior portion of area 18b) in the integration of visual and somatic cues was assessed behaviorally. Following restricted bilateral lesions of selected cortical regions, rats were tested on their ability to retain or relearn a conditional visuosomatic discrimination task learned prior to surgery. Two compound, visuosomatic stimuli were used: white or black associated with either one of two degrees of roughness. The use of a guided-response procedure was essential for rats to learn this difficult conditional bimodal task. None of the 6 rats with lesions aimed at area AM retained the habit postoperatively. Four of these rats were incapable of relearning the task after 3 postoperative training series, and they had either extensive lesions of area AM or relatively small, symmetric damage of anterior portions of AM. The remaining two rats with lesions in area AM were able to relearn the task in the second postoperative training series, and their lesions either were restricted to posteromedial aspects of area AM or they involved asymmetric loci in anterior area AM. In contrast to rats with lesions of area AM, rats with lesions in visual cortex in areas 17 and 18a, or in auditory cortex in area 41, were able either to retain the task or to relearn in the first postoperative training series. These results indicate that the integrity of area AM appears necessary for rats to discriminate between pairs of compound stimuli that differ in brightness and roughness. The behavioural data point to the notion that this area might be involved in the integration of these types of visual and somatic stimuli. In addition, our finding that performance was largely unimpaired following extensive lesions of lateral extrastriate area supports previous reports indicating that medial and lateral extrastriate visual areas differ in function.     

A neurochemical signature of visual recovery after extrastriate cortical damage in the adult cat

In adult cats, damage to the extrastriate visual cortex on the banks of the lateral suprasylvian (LS) sulcus causes severe deficits in motion perception that can recover as a result of intensive direction discrimination training. The fact that recovery is restricted to trained visual field locations suggests that the neural circuitry of early visual cortical areas, with their tighter retinotopy, may play an important role in attaining perceptual improvements after damage to higher level visual cortex. The present study tests this hypothesis by comparing the manner in which excitatory and inhibitory components of the supragranular circuitry in an early visual cortical area (area 18) are affected by LS lesions and postlesion training. First, the proportion of LS-projecting pyramidal cells as well as calbindin- and parvalbumin-positive interneurons expressing each of the four AMPA receptor subunits was estimated in layers II and III of area 18 in intact animals. The degree to which LS lesions and visual retraining altered these expression patterns was then assessed. Both LS-projecting pyramidal cells and inhibitory interneurons exhibited long-term, differential reductions in the expression of glutamate receptor (GluR)1, -2, -2/3, and -4 following LS lesions. Intensive visual training post lesion restored normal AMPAR subunit expression in all three cell-types examined. Furthermore, for LS-projecting and calbindin-positive neurons, this restoration occurred only in portions of the ipsi-lesional area 18 representing trained visual field locations. This supports our hypothesis that stimulation of early visual cortical areas-in this case, area 18-by training is an important factor in restoring visual perception after permanent damage to LS cortex.     

Acquiring long-term representations of visual classes following extensive extrastriate damage

Different areas of human visual cortex are thought to play different roles in the learning of visual information: whereas in low/intermediate cortical areas, plasticity may be manifested by enhanced selectivity to learned visual features, in higher-level areas, plasticity may result in generalization and development of tolerance to degraded versions of the learned stimuli. The most effective tolerance to degraded information is presumably achieved in the case of cooperation between the different forms of plasticity. Whether this tolerance to degraded information also applies when the visual input is degraded as a result of a lesion to lower levels of the visual system remains an open question. To address this, we studied visual classification learning in a patient with an extensive bilateral lesion affecting intermediate/low-level visual areas but sparing higher-level areas. Despite difficulty in perceiving the stimuli, the patient learned to classify them, albeit not as quickly as control participants. Moreover, the patient's learning was maintained over the long term and was accompanied by improved discrimination of individual stimuli. These findings demonstrate that degraded output from lesioned, lower areas can be exploited in the service of a new visual task and the results likely implicate a combination of bottom-up and top-down processing during visual learning.     

Recovery of pattern discrimination ability in rats receiving serial or one-stage visual cortex lesions.

Two groups of 10 hooded rats were trained on a pattern discrimination between horizontal and vertical striped stimuli which were equated for contour-length and total luminous flux, and in which consistent local luminous flux cues were eliminated. In one group of rats, visual cortex removals were performed in two stages with training between the operations. Nine out of the 10 rats were able to relearn the pattern discrimination (median of 344 trials) after the completed bilateral visual cortex lesions in one stage. In agreement with previous studies, none of these animals were able to relearn the discrimination after more than 10 times (550 trial limit) the trials required for original learning. However, several rats with total one-stage lesions could relearn the pattern discrimination if very extended periods of training were given.     

Comparing the effects of auditory deprivation and sign language within the auditory and visual cortex

To investigate neural plasticity resulting from early auditory deprivation and use of American Sign Language, we measured responses to visual stimuli in deaf signers, hearing signers, and hearing nonsigners using functional magnetic resonance imaging. We examined "compensatory hypertrophy" (changes in the responsivity/size of visual cortical areas) and "cross-modal plasticity" (changes in auditory cortex responses to visual stimuli). We measured the volume of early visual areas (V1, V2, V3, V4, and MT+). We also measured the amplitude of responses within these areas, and within the auditory cortex, to a peripheral visual motion stimulus that was attended or ignored. We found no major differences between deaf and hearing subjects in the size or responsivity of early visual areas. In contrast, within the auditory cortex, motion stimuli evoked significant responses in deaf subjects, but not in hearing subjects, in a region of the right auditory cortex corresponding to Brodmann's areas 41, 42, and 22. This hemispheric selectivity may be due to a predisposition for the right auditory cortex to process motion; earlier studies report a right hemisphere bias for auditory motion in hearing subjects. Visual responses within the auditory cortex of deaf subjects were stronger for attended than ignored stimuli, suggesting top-down processes. Hearing signers did not show visual responses in the auditory cortex, indicating that cross-modal plasticity can be attributed to auditory deprivation rather than sign language experience. The largest effects of auditory deprivation occurred within the auditory cortex rather than the visual cortex, suggesting that the absence of normal input is necessary for large-scale cortical reorganization to occur.     

Effects of lateral suprasylvian visual cortex lesions on visual localization, discrimination, and attention in cats

Experiments were carried out to begin to define the behavioral functions of the lateral suprasylvian (LS) visual area of the cat's cortex. Behavioral tasks were chosen for analysis on the basis of previous suggestions in the literature concerning possible functions of LS cortex and its afferent pathways. These tasks included the ability of cats to orient the head and eyes to a stimulus presented in particular locations in the visual field, the ability to learn successive reversals of a two-choice visual pattern discrimination, and the ability to maintain or shift attention between relevant or irrelevant visual form and brightness cues. Eight cats were trained on each of these tasks. Four of the cats then received bilateral lesions of LS cortex, including the AMLS and PMLS regions, and the remaining 4 cats were used to assess normal retention. The LS cortex lesions had no significant effect upon performance of any of the behaviors tested. Thus, this region of cortex appears to play no essential role in simple brightness, form, and pattern discrimination performance, visual reversal learning, maintaining and shifting visual attention, or orienting the head and eyes to stimuli in the visual field. These results are discussed in relation to previous lesion studies involving large regions of the cat's extrastriate cortex and studies in other species. Possible functions of LS cortex, based upon recent electrophysiological studies, are suggested.     

The effects of V4 lesions on the visual abilities of macaques: shape discrimination

Monkeys with bilateral ablation of cortical visual area V4 were compared with unoperated controls for their ability to relearn postoperatively a series of preoperatively acquired two-choice visual discrimination problems. The animals with V4 lesions were impaired on relearning to discriminate between different shapes, and discrimination between identical shapes presented at different orientations was also impaired. Some of the deficits were consistent with disrupting the input to inferotemporal cortex, but discrimination of a subset of the stimuli is known to be unaffected by inferotemporal cortex lesions and could not be explained in the same way. To clarify the nature of the deficit, and to test the hypothesis that shapes differing in orientation are analyzed in the occipitoparietal processing pathway, animals with V4 lesions were also compared to normals on their ability to acquire a version of the landmark task. The V4 animals performed as well as the control animals on this task. The results suggest that V4 is important for the shape discrimination abilities that survive inferotemporal cortex lesions. The role of V4 in shape analysis is discussed in the light of recent evidence that V4 neurones are modulated by visual attention.     

Neural substrates of visual perceptual learning of simple and complex stimuli.

OBJECTIVE: The two experiments described here used event-related potentials (ERPs) to investigate whether perceptual learning of different complexities of stimuli involves different levels of visual cortical processing in human adults. METHODS: Reaction times and ERPs were recorded during 3 consecutive training sessions in which subjects discriminated between simple stimuli made of line segments or complex stimuli made of compound shapes. RESULTS: Reaction times in both experiments were shortened across training sessions. For simple stimuli, training resulted in a decreased N1 (125-155ms) and an increased P2 (180-240ms) over the occipital area. For complex stimuli, however, training resulted in a decreased N1 (125-155ms) and N2 (290-340ms) and an increased P3 (350-550ms) over the central/parietal areas. CONCLUSIONS: These findings suggest that perceptual learning modifies the response at different levels of visual cortical processing related to the complexity of the stimulus. SIGNIFICANCE: The neuronal mechanisms involved in perceptual learning may depend on the nature (e.g. the complexity) of the stimuli used in the discrimination task.     

fMRI Measures of perceptual filling-in in the human visual cortex

Filling-in refers to the tendency of stabilized retinal stimuli to fade and become replaced by their background. This phenomenon is a good example of central brain mechanisms that can selectively add or delete information to/from the retinal input. Importantly, such cortical mechanisms may overlap with those that are used more generally in visual perception. In order to identify cortical areas that contribute to perceptual filling-in, we used functional magnetic resonance imaging to image activity in the visual cortex while subjects experienced filling-in. Nine subjects viewed an achromatic disc with slightly higher luminance than the background and indicated the presence or absence of filling-in by a keypress. The disc was placed in either the upper or lower left quadrant. Similar high-contrast stimuli were used to map out the retinotopic representation of the disc. Unexpectedly, the lower-field high-contrast stimulus produced more parietal cortex activation than the upper-field condition, indicating preferential representation of the lower field by attentional control mechanisms. During perceptual filling-in, we observed significant contralateral reductions in activation in lower-tier retinotopic areas V1 and V2. In contrast, increased activation was consistently observed in visual areas V3A and V4v, higher-level cortex in the intraparietal sulcus, posterior superior temporal sulcus, and the ventral occipital-temporal region, as well as the pulvinar. The filling-in activation pattern was remarkably similar for both the upper- and lower-field conditions. Behaviorally, filling-in was reported to be easier for the lower visual field, and filling-in periods were longer for the lower than the upper quadrant. We suggest this behavioral asymmetry may be partially due to the preferential parietal representation of the lower field. The results lead us to propose that perceptual filling-in recruits high-level control mechanisms to reconcile competing percepts, and alters the normal image-related signals at the first stages of cortical processing. Moreover, the overall pattern of activation during filling-in resembles that seen in other studies of perceptually bistable stimuli, including binocular rivalry, indicating common control mechanisms.     

Responses of macaque perirhinal neurons during and after visual stimulus association learning.

Recent lesion studies have implicated the perirhinal cortex in learning that two objects are associated, i.e., visual association learning. In this experiment we tested whether neuronal responses to associated stimuli in perirhinal cortex are altered over the course of learning. Neurons were recorded from monkeys during performance of a visual discrimination task in which a predictor stimulus was followed, after a delay, by a GO or NO-GO choice stimulus. Association learning had two major influences on neuronal responses. First, responses to frequently paired predictor-choice stimuli were more similar to one another than was the case with infrequently paired stimuli. Second, the magnitude of activity during the delay was correlated with the magnitude of responses to both the predictor and choice stimuli. Both of these learning effects were found only for stimulus pairs that had been associated on at least 2 d of training. Early in training, the delay activity was correlated only with the response to the predictor stimuli. Thus, with long-term training, perirhinal neurons tend to link the representations of temporally associated stimuli.     

The importance of the rat hippocampus for learning the structure of visual arrays

It has been assumed that the integrity of the rodent hippocampus is required for learning the spatial distribution of visual elements in an array. Formally assessing this assumption is, however, far from straightforward as standard tests are amenable to alternative strategies. In order to provide a stringent test of this ability rats were trained on three concurrent visual discriminations in a water tank in which the stimuli in each pair of discriminations contained exactly the same elements but they differed in their spatial arrangement e.g. A|B vs. its mirror image B/A. Such 'structural' discriminations are a specific subtype of 'configural' or 'nonlinear' tasks. Following acquisition half of the rats received hippocampal lesions and all rats were retrained on the structural discriminations. Hippocampal lesions impaired the ability to relearn these 'structural' discriminations. In contrast, two other groups of rats with similar hippocampal lesions showed no impairment on relearning two non-structural, configural discriminations: transverse patterning and biconditional learning. All three tasks used the same apparatus, the same stimulus elements, and similar training regimes. Superior performance by the rats with hippocampal lesions during a generalization decrement probe showed that hippocampal lesions had diminished sensitivity to 'structural' features on the biconditional task. While the rat hippocampus need not be required for all configural learning, it is important for the special case when the spatial arrangements of the elements are critical. This ability may be a prerequisite for the creation of mental snapshots, which underlie episodic memory.     

Images of illusory motion in primary visual cortex

Illusory motion can be generated by successively flashing a stationary visual stimulus in two spatial locations separated by several degrees of visual angle. In appropriate conditions, the apparent motion is indistinguishable from real motion: The observer experiences a luminous object traversing a continuous path from one stimulus location to the other through intervening positions where no physical stimuli exist. The phenomenon has been extensively investigated for nearly a century but little is known about its neurophysiological foundation. Here we present images of activations in the primary visual cortex in response to real and apparent motion. The images show that during apparent motion, a path connecting the cortical representations of the stimulus locations is filled in by activation. The activation along the path of apparent motion is similar to the activation found when a stimulus is presented in real motion between the two locations.     

The topography of the scalp-recorded visual N700.

OBJECTIVE: To describe the topography of the N700 component of the scalp-recorded visual event-related potential (ERP) and to provide fundamental knowledge of the conditions under which it occurs. METHODS: We examined the time-course of visual ERP in response to the short (100ms) and prolonged (7s) presentation of simple salient visual stimuli separated by long interstimulus intervals employing high-resolution 64-channel DC-EEG. Current source density (CSD) mapping and spatio-temporal dipole source analysis were performed. RESULTS: CSD analysis revealed highly significant bilateral current sinks over occipito-temporal areas from about 450ms up to 1s after stimulus offset (visual N700). CSD topography and dipole source analysis suggested late prolonged activation of extrastriate visual areas which did not depend merely upon a stimulus offset response, afterimages or blinking, as confirmed by control conditions. CONCLUSIONS: Our findings provide basic knowledge about the time-course of sensory activation. We found that passive watching of rare salient short stimuli automatically evoked sustained activity in the extrastriate visual cortex up to 1s after stimulus offset. SIGNIFICANCE: Visual N700 provides a promising tool for important insights into the cortical mechanisms of stimulus post-processing. Its role in associative learning of temporally non-overlapping stimuli (automatic ultra-short-term sensory memory) should be explored.     

Dynamics of population response to changes of motion direction in primary visual cortex

The visual system is thought to represent the direction of moving objects in the relative activity of large populations of cortical neurons that are broadly tuned to the direction of stimulus motion, but how changes in the direction of a moving stimulus are represented in the population response remains poorly understood. Here we take advantage of the orderly mapping of direction selectivity in ferret primary visual cortex (V1) to explore how abrupt changes in the direction of a moving stimulus are encoded in population activity using voltage-sensitive dye imaging. For stimuli moving in a constant direction, the peak of the V1 population response accurately represented the direction of stimulus motion, but following abrupt changes in motion direction, the peak transiently departed from the direction of stimulus motion in a fashion that varied with the direction offset angle and was well predicted from the response to the component directions. We conclude that cortical dynamics and population coding mechanisms combine to place constraints on the accuracy with which abrupt changes in direction of motion can be represented by cortical circuits.     

Posttraining transcranial magnetic stimulation of striate cortex disrupts consolidation early in visual skill learning

Practice-induced improvements in skilled performance reflect "offline " consolidation processes extending beyond daily training sessions. According to visual learning theories, an early, fast learning phase driven by high-level areas is followed by a late, asymptotic learning phase driven by low-level, retinotopic areas when higher resolution is required. Thus, low-level areas would not contribute to learning and offline consolidation until late learning. Recent studies have challenged this notion, demonstrating modified responses to trained stimuli in primary visual cortex (V1) and offline activity after very limited training. However, the behavioral relevance of modified V1 activity for offline consolidation of visual skill memory in V1 after early training sessions remains unclear. Here, we used neuronavigated transcranial magnetic stimulation (TMS) directed to a trained retinotopic V1 location to test for behaviorally relevant consolidation in human low-level visual cortex. Applying TMS to the trained V1 location within 45 min of the first or second training session strongly interfered with learning, as measured by impaired performance the next day. The interference was conditional on task context and occurred only when training in the location targeted by TMS was followed by training in a second location before TMS. In this condition, high-level areas may become coupled to the second location and uncoupled from the previously trained low-level representation, thereby rendering consolidation vulnerable to interference. Our data show that, during the earliest phases of skill learning in the lowest-level visual areas, a behaviorally relevant form of consolidation exists of which the robustness is controlled by high-level, contextual factors.     

Decision-related activity in the macaque dorsal visual pathway.

Brain areas at higher levels of cortical organization are thought to be more involved in decision processes than are earlier, i.e. lower, sensory areas. Hence, neuronal activity correlated with decisions should vary with an area's position in the cortical hierarchy. To test this proposal, we investigated whether a change in neuronal activity during error trials depends in a systematic way on cortical hierarchical position. While macaque monkeys discriminated the direction of moving visual stimuli, the activity of direction-selective neurons was recorded in four extrastriate visual areas: V3A, the middle temporal area, the middle superior temporal area and the posterior part of the superior temporal polysensory area. Neuronal activity was significantly reduced in all areas when the monkeys made errors in judging the direction of stimuli moving in the preferred direction with low and intermediate luminance contrast. The amount of activity reduction was approximately 50% in all of the visual areas. Thus, the activity on error trials is reduced in early visual processing, independent of the hierarchy in the dorsal visual pathway. The activity reduction depended on stimulus contrast and the direction of the decision relative to the stimulus motion. It was profound and significant in all areas at low stimulus contrast. However, it was nonsignificant at high stimulus contrast. Our data suggest that activity reduction on error trials is due to lack of attention in association with stimulus expectation.     

The path to memory is guided by strategy: distinct networks are engaged in associative encoding under visual and verbal strategy and influence memory performance in healthy and impaired individuals

Given the diversity of stimuli encountered in daily life, a variety of strategies must be used for learning new information. Relating and encoding visual and verbal stimuli into memory has been probed using various tasks and stimulus types. Engagement of specific subsequent memory and cortical processing regions depends on the stimulus modality of studied material; however, it remains unclear whether different encoding strategies similarly influence regional activity when stimulus type is held constant. In this study, participants encoded object pairs using a visual or verbal associative strategy during fMRI, and subsequent memory was assessed for pairs encoded under each strategy. Each strategy elicited distinct regional processing and subsequent memory effects: middle/superior frontal, lateral parietal, and lateral occipital for visually associated pairs and inferior frontal, medial frontal, and medial occipital for verbally associated pairs. This regional selectivity mimics the effects of stimulus modality, suggesting that cortical involvement in associative encoding is driven by strategy and not simply by stimulus type. The clinical relevance of these findings, probed in a patient with a recent aphasic stroke, suggest that training with strategies utilizing unaffected cortical regions might improve memory ability in patients with brain damage.     

Perceptual experience modulates cortical circuits involved in visual awareness

Successful interactions with the environment entail interpreting ambiguous sensory information. To address this challenge it has been suggested that the brain optimizes performance through experience. Here we used functional magnetic resonance imaging (fMRI) to investigate whether perceptual experience modulates the cortical circuits involved in visual awareness. Using ambiguous visual stimuli (binocular rivalry or ambiguous structure‐from‐motion) we were able to disentangle the co‐occurring influences of stimulus repetition and perceptual repetition. For both types of ambiguous stimuli we observed that the mere repetition of the stimulus evoked an entirely different pattern of activity modulations than the repetition of a particular perceptual interpretation of the stimulus. Regarding stimulus repetition, decreased fMRI responses were evident during binocular rivalry but weaker during 3‐D motion rivalry. Perceptual repetition, on the other hand, entailed increased activity in stimulus‐specific visual brain regions – for binocular rivalry in the early visual regions and for ambiguous structure‐from‐motion in both early as well as higher visual regions. This indicates that the repeated activation of a visual network mediating a particular percept facilitated its later reactivation. Perceptual repetition was also associated with a response change in the parietal cortex that was similar for the two types of ambiguous stimuli, possibly relating to the temporal integration of perceptual information. We suggest that perceptual repetition is associated with a facilitation of neural activity within and between percept‐specific visual networks and parietal networks involved in the temporal integration of perceptual information, thereby enhancing the stability of previously experienced percepts.     

Integration of distributed cortical systems by reentry: a computer simulation of interactive functionally segregated visual areas

A computer model based on visual cortex has been constructed to analyze how the operations of multiple, functionally segregated cortical areas can be coordinated and integrated to yield a unified perceptual response. We propose that cortical integration arises through the process of reentry--the ongoing, parallel, recursive signaling between separate maps along ordered anatomical connections. To test the efficacy of this reentrant cortical integration (RCI) model, we have carried out detailed computer simulations of 3 interconnected cortical areas in the striate and extrastriate cortex of the macaque. The simulated networks contained a total of over 222,000 units and 8.5 million connections. The 3 modeled areas, called VOR, VOC, and VMO, incorporate major anatomical and physiological properties of cortical areas V1, V3, and V5 but are vastly simplified compared with monkey visual cortex. Simulated area VOR contains both orientation and directionally selective units; simulated area VMO discriminates the direction of motion of arbitrarily oriented objects; and simulated area VOC responds to both luminance and occlusion boundaries in the stimulus. Area VOC is able to respond to illusory contours (Kanizsa, 1979) by means of the same neural architecture used for the discrimination of occlusion boundaries. This architecture also generates responses to structure-from-motion by virtue of reentrant connections from VMO to VOC. The responses of the simulated networks to these illusions are consistent with the perceptual responses of humans and other species presented with these stimuli. The networks also respond in a consistent manner to a novel illusion that combines illusory contours and structure-from-motion. The response synthesized to this combined illusion provides a strong argument supporting the need for a recursive reentrant process in the cortex. Functional integration of the simulated areas in the RCI model were found to depend upon the combined action of 3 reentrant processes: (1) conflicting responses among segregated areas are competitively eliminated, (2) outputs of each area are used by other areas in their own operations, and (3) outputs of an area are "reentered" back to itself (through lower areas) and can thus be used iteratively to synthesize responses to complex or illusory stimuli. Transection of the reentrant connections selectively abolished these integrative processes and led to failure of figural synthesis. The proposed model of reentry suggests a basis for understanding how multiple visual areas as well as other cortical areas may be integrated within a distributed system.