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      Practising orientation identification improves orientation coding in V1 neurons.

      Nature
      Animals, Electrophysiology, Learning, physiology, Macaca mulatta, Male, Neuronal Plasticity, Neurons, Visual Cortex, cytology, Visual Perception

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          Abstract

          The adult brain shows remarkable plasticity, as demonstrated by the improvement in fine sensorial discriminations after intensive practice. The behavioural aspects of such perceptual learning are well documented, especially in the visual system. Specificity for stimulus attributes clearly implicates an early cortical site, where receptive fields retain fine selectivity for these attributes; however, the neuronal correlates of a simple visual discrimination task remained unidentified. Here we report electrophysiological correlates in the primary visual cortex (V1) of monkeys for learning orientation identification. We link the behavioural improvement in this type of learning to an improved neuronal performance of trained compared to naive neurons. Improved long-term neuronal performance resulted from changes in the characteristics of orientation tuning of individual neurons. More particularly, the slope of the orientation tuning curve that was measured at the trained orientation increased only for the subgroup of trained neurons most likely to code the orientation identified by the monkey. No modifications of the tuning curve were observed for orientations for which the monkey had not been trained. Thus training induces a specific and efficient increase in neuronal sensitivity in V1.

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          Most cited references26

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          Task difficulty and the specificity of perceptual learning.

          Practising simple visual tasks leads to a dramatic improvement in performing them. This learning is specific to the stimuli used for training. We show here that the degree of specificity depends on the difficulty of the training conditions. We find that the pattern of specificities maps onto the pattern of receptive field selectivities along the visual pathway. With easy conditions, learning generalizes across orientation and retinal position, matching the spatial generalization of higher visual areas. As task difficulty increases, learning becomes more specific with respect to both orientation and position, matching the fine spatial retinotopy exhibited by lower areas. Consequently, we enjoy the benefits of learning generalization when possible, and of fine grain but specific training when necessary. The dynamics of learning show a corresponding feature. Improvement begins with easy cases (when the subject is allowed long processing times) and only subsequently proceeds to harder cases. This learning cascade implies that easy conditions guide the learning of hard ones. Taken together, the specificity and dynamics suggest that learning proceeds as a countercurrent along the cortical hierarchy. Improvement begins at higher generalizing levels, which, in turn, direct harder-condition learning to the subdomain of their lower-level inputs. As predicted by this reverse hierarchy model, learning can be effective using only difficult trials, but on condition that learning onset has previously been enabled. A single prolonged presentation suffices to initiate learning. We call this single-encounter enabling effect 'eureka'.
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            Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys.

            Previous studies have shown that the tonotopic organization of primary auditory cortex is altered subsequent to restricted cochlear lesions (Robertson and Irvine, 1989) and that the topographic reorganization of the primary somatosensory cortex is correlated with changes in the perceptual acuity of the animal (Recanzone et al., 1992a-d). Here we report an increase in the cortical area of representation of a restricted frequency range in primary auditory cortex of adult owl monkeys that is correlated with the animal's performance at a frequency discrimination task. Monkeys trained for several weeks to discriminate small differences in the frequency of sequentially presented tonal stimuli revealed a progressive improvement in performance with training. At the end of the training period, the tonotopic organization of Al was defined by recording multiple-unit responses at 70-258 cortical locations. These responses were compared to those derived from three normal monkeys and from two monkeys that received the same auditory stimuli but that were engaged in a tactile discrimination task. The cortical representation, the sharpness of tuning, and the latency of the response were greater for the behaviorally relevant frequencies of trained monkeys when compared to the same frequencies of control monkeys. The cortical area of representation was the only studied parameter that was correlated with behavioral performance. These results demonstrate that attended natural stimulation can modify the tonotopic organization of Al in the adult primate, and that this alteration is correlated with changes in perceptual acuity.
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              An emergent model of orientation selectivity in cat visual cortical simple cells.

              It is well known that visual cortical neurons respond vigorously to a limited range of stimulus orientations, while their primary afferent inputs, neurons in the lateral geniculate nucleus (LGN), respond well to all orientations. Mechanisms based on intracortical inhibition and/or converging thalamocortical afferents have previously been suggested to underlie the generation of cortical orientation selectivity; however, these models conflict with experimental data. Here, a 1:4 scale model of a 1700 microns by 200 microms region of layer IV of cat primary visual cortex (area 17) is presented to demonstrate that local intracortical excitation may provide the dominant source of orientation-selective input. In agreement with experiment, model cortical cells exhibit sharp orientation selectivity despite receiving strong iso-orientation inhibition, weak cross-orientation inhibition, no shunting inhibition, and weakly tuned thalamocortical excitation. Sharp tuning is provided by recurrent cortical excitation. As this tuning signal arises from the same pool of neurons that it excites, orientation selectivity in the model is shown to be an emergent property of the cortical feedback circuitry. In the model, as in experiment, sharpness of orientation tuning is independent of stimulus contrast and persists with silencing of ON-type subfields. The model also provides a unified account of intracellular and extracellular inhibitory blockade experiments that had previously appeared to conflict over the role of inhibition. It is suggested that intracortical inhibition acts nonspecifically and indirectly to maintain the selectivity of individual neurons by balancing strong intracortical excitation at the columnar level.
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                Author and article information

                Journal
                11484056
                10.1038/35087601

                Chemistry
                Animals,Electrophysiology,Learning,physiology,Macaca mulatta,Male,Neuronal Plasticity,Neurons,Visual Cortex,cytology,Visual Perception

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