Perceptual learning and dynamic changes in primary visual cortex

Perceptual learning is the improved performance that follows practice in a perceptual task. In this issue of Neuron, Yotsumoto et al. use fMRI to show that stimuli presented at the location used in training initially evoke greater activation in primary visual cortex than stimuli presented elsewhere, but this difference disappears once learning asymptotes.     

Perceptual and neuronal correspondence in primary visual cortex

Recent findings from the study of primary visual cortex in humans and animals blur the distinction between early and late visual processing. Under some conditions, the activity of neurons in primary visual cortex appears as close or closer to perception than activity in 'higher' visual areas.     

Adaptation to contingencies in macaque primary visual cortex.

We tested the hypothesis that neurons in the primary visual cortex (V1) adapt selectively to contingencies in the attributes of visual stimuli. We recorded from single neurons in macaque V1 and measured the effects of adaptation either to the sum of two gratings (compound stimulus) or to the individual gratings. According to our hypothesis, there would be a component of adaptation that is specific to the compound stimulus. In a first series of experiments, the two gratings differed in orientation. One grating had optimal orientation and the other was orthogonal to it, and therefore did not activate the neuron under study. These experiments provided evidence in favour of our hypothesis. In most cells adaptation to the compound stimulus reduced responses to the compound stimulus more than it reduced responses to the optimal grating, and the responses to the compound stimulus were reduced more by adaptation to the compound stimulus than by adaptation to the individual gratings. This suggests that a component of adaptation was specific to (and caused by) the simultaneous presence of the two orientations in the compound stimulus. To test whether V1 neurons could adapt to other contingencies in the stimulus attributes, we performed a second series of experiments, in which the component gratings were parallel but differed in spatial frequency, and were both effective in activating the neuron under study. These experiments failed to reveal convincing contingent effects of adaptation, suggesting that neurons cannot adapt equally well to all types of contingency.     

Perceptual learning and decision-making in human medial frontal cortex

The dominant view that perceptual learning is accompanied by changes in early sensory representations has recently been challenged. Here we tested the idea that perceptual learning can be accounted for by reinforcement learning involving changes in higher decision-making areas. We trained subjects on an orientation discrimination task involving feedback over 4 days, acquiring fMRI data on the first and last day. Behavioral improvements were well explained by a reinforcement learning model in which learning leads to enhanced readout of sensory information, thereby establishing noise-robust representations of decision variables. We find stimulus orientation encoded in early visual and higher cortical regions such as lateral parietal cortex and anterior cingulate cortex (ACC). However, only activity patterns in the ACC tracked changes in decision variables during learning. These results provide strong evidence for perceptual learning-related changes in higher order areas and suggest that perceptual and reward learning are based on a common neurobiological mechanism.     

Representation of color stimuli in awake macaque primary visual cortex

We investigated the responses of single neurons in primary visual cortex (area V1) of awake monkeys to chromatic stimuli. Chromatic tuning properties, determined for homogeneous color patches presented on a neutral gray background, varied strongly between cells. The continuum of preferred chromaticities and tuning widths indicated a distributed representation of color signals in V1. When stimuli were presented on colored backgrounds, chromatic tuning was different in most neurons, and the changes in tuning were consistent with some degree of sensitivity of the neurons to the chromatic contrast between stimulus and background. Quantitatively, the average response changes matched the magnitudes of color induction effects measured in human subjects under corresponding stimulus conditions.     

Lateral connectivity and contextual interactions in macaque primary visual cortex

Two components of cortical circuits could mediate contour integration in primary visual cortex (V1): intrinsic horizontal connections and feedback from higher cortical areas. To distinguish between these, we combined functional mapping with a new technique for labeling axons, a recombinant adenovirus bearing the gene for green fluorescent protein (GFP), to determine the extent, density, and orientation specificity of V1 intrinsic connections and V2 to V1 feedback. Both connections cover portions of V1 representing regions of visual space up to eight times larger than receptive fields as classically defined, though the intrinsic connections are an order of magnitude denser than the feedback. Whereas the intrinsic connections link similarly oriented domains in V1, V2 to V1 feedback displays no such specificity. These findings suggest that V1 intrinsic horizontal connections provide a more likely substrate for contour integration.     

Multisensory integration in macaque visual cortex depends on cue reliability

Responses of multisensory neurons to combinations of sensory cues are generally enhanced or depressed relative to single cues presented alone, but the rules that govern these interactions have remained unclear. We examined integration of visual and vestibular self-motion cues in macaque area MSTd in response to unimodal as well as congruent and conflicting bimodal stimuli in order to evaluate hypothetical combination rules employed by multisensory neurons. Bimodal responses were well fit by weighted linear sums of unimodal responses, with weights typically less than one (subadditive). Surprisingly, our results indicate that weights change with the relative reliabilities of the two cues: visual weights decrease and vestibular weights increase when visual stimuli are degraded. Moreover, both modulation depth and neuronal discrimination thresholds improve for matched bimodal compared to unimodal stimuli, which might allow for increased neural sensitivity during multisensory stimulation. These findings establish important new constraints for neural models of cue integration.     

Cortisol reduces plasticity in the kitten visual cortex

We investigated the effect of elevated levels of cortisol on plasticity in the visual cortex of the cat. Animals were given daily injections of cortisol i.m. for 20 days starting around 35 days of age. After 10 days they were monocularly deprived, and after an additional 10 days recordings were made from the visual cortex to construct an ocular dominance histogram. The results were compared with those from normal animals of the same age, and with animals monocularly deprived for the same period but not treated with cortisol. Cortisol reduced the ocular dominance shift in a dose-dependent manner, but did not totally abolish it even at the highest doses used. Two other series of animals were recorded, one slightly later in the critical period and one slightly earlier, with care taken to give cortisol before the animals were exposed to light in the morning. In both cases, cortisol reduced the ocular dominance shift but did not abolish it. To interpret these results, we measured levels of plasma cortisol in normal cats of various ages. Average levels were fairly constant between birth and 12 months of age (0.5–1 μg/dl), and increased slightly after that, but there was a large variation between animals. Thus elevated levels of cortisol can have a substantial effect on plasticity in the visual cortex of the cat, but the decline of the critical period for plasticity between 6 weeks and 3–5 months of age does not seem to be due to a rise in cortisol levels during this time.     

Perceptual stability reflected in neuronal pattern similarities in human visual cortex

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A neuronal basis of iconic memory in macaque primary visual cortex

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Two-dimensional substructure of stereo and motion interactions in macaque visual cortex

The analysis of object motion and stereoscopic depth are important tasks that are begun at early stages of the primate visual system. Using sparse white noise, we mapped the receptive field substructure of motion and disparity interactions in neurons in V1 and MT of alert monkeys. Interactions in both regions revealed subunits similar in structure to V1 simple cells. For both motion and stereo, the scale and shape of the receptive field substructure could be predicted from conventional tuning for bars or dot-field stimuli, indicating that the small-scale interactions were repeated across the receptive fields. We also found neurons in V1 and in MT that were tuned to combinations of spatial and temporal binocular disparities, suggesting a possible neural substrate for the perceptual Pulfrich phenomenon. Our observations constrain computational and developmental models of motion-stereo integration.     

Cortisol reduces plasticity in the kitten visual cortex.

We investigated the effect of elevated levels of cortisol on plasticity in the visual cortex of the cat. Animals were given daily injections of cortisol i.m. for 20 days starting around 35 days of age. After 10 days they were monocularly deprived, and after an additional 10 days recordings were made from the visual cortex to construct an ocular dominance histogram. The results were compared with those from normal animals of the same age, and with animals monocularly deprived for the same period but not treated with cortisol. Cortisol reduced the ocular dominance shift in a dose-dependent manner, but did not totally abolish it even at the highest doses used. Two other series of animals were recorded, one slightly later in the critical period and one slightly earlier, with care taken to give cortisol before the animals were exposed to light in the morning. In both cases, cortisol reduced the ocular dominance shift but did not abolish it. To interpret these results, we measured levels of plasma cortisol in normal cats of various ages. Average levels were fairly constant between birth and 12 months of age (0.5-1 microgram/dl), and increased slightly after that, but there was a large variation between animals. Thus elevated levels of cortisol can have a substantial effect on plasticity in the visual cortex of the cat, but the decline of the critical period for plasticity between 6 weeks and 3-5 months of age does not seem to be due to a rise in cortisol levels during this time.     

Different origins of gamma rhythm and high-gamma activity in macaque visual cortex

During cognitive tasks electrical activity in the brain shows changes in power in specific frequency ranges, such as the alpha (8-12 Hz) or gamma (30-80 Hz) bands, as well as in a broad range above ～80 Hz, called the high-gamma band. The role or significance of this broadband high-gamma activity is unclear. One hypothesis states that high-gamma oscillations serve just like gamma oscillations, operating at a higher frequency and consequently at a faster timescale. Another hypothesis states that high-gamma power is related to spiking activity. Because gamma power and spiking activity tend to co-vary during most stimulus manipulations (such as contrast modulations) or cognitive tasks (such as attentional modulation), it is difficult to dissociate these two hypotheses. We studied the relationship between high-gamma power, gamma rhythm, and spiking activity in the primary visual cortex (V1) of awake monkeys while varying the stimulus size, which increased the gamma power but decreased the firing rate, permitting a dissociation. We found that gamma power became anti-correlated with the high-gamma power, suggesting that the two phenomena are distinct and have different origins. On the other hand, high-gamma power remained tightly correlated with spiking activity under a wide range of stimulus manipulations. We studied this relationship using a signal processing technique called Matching Pursuit and found that action potentials are associated with sharp transients in the LFP with broadband power, which is visible at frequencies as low as ～50 Hz. These results distinguish broadband high-gamma activity from gamma rhythms as an easily obtained and reliable electrophysiological index of neuronal firing near the microelectrode. Further, they highlight the importance of making a careful dissociation between gamma rhythms and spike-related transients that could be incorrectly decomposed as rhythms using traditional signal processing methods.     

Perceptual organization of local elements into global shapes in the human visual cortex

The question of how local image features on the retina are integrated into perceived global shapes is central to our understanding of human visual perception. Psychophysical investigations have suggested that the emergence of a coherent visual percept, or a "good-Gestalt", is mediated by the perceptual organization of local features based on their similarity. However, the neural mechanisms that mediate unified shape perception in the human brain remain largely unknown. Using human fMRI, we demonstrate that not only higher occipitotemporal but also early retinotopic areas are involved in the perceptual organization and detection of global shapes. Specifically, these areas showed stronger fMRI responses to global contours consisting of collinear elements than to patterns of randomly oriented local elements. More importantly, decreased detection performance and fMRI activations were observed when misalignment of the contour elements disturbed the perceptual coherence of the contours. However, grouping of the misaligned contour elements by disparity resulted in increased performance and fMRI activations, suggesting that similar neural mechanisms may underlie grouping of local elements to global shapes by different visual features (orientation or disparity). Thus, these findings provide novel evidence for the role of both early feature integration processes and higher stages of visual analysis in coherent visual perception.     

Perceptual learning: visual function improved by LTP/LTD-like stimulation

A new behavioral training approach has been found significantly to improve visual function; the results further attest to the high degree of plasticity in sensory systems.