When a new perceptual task is learned, plasticity occurs in the brain to mediate improvements in performance with training. How do these changes affect the neural substrates of previously learned tasks? We addressed this question by examining the effect of fine discrimination training on the causal contribution of area MT to coarse depth discrimination. When monkeys are trained to discriminate between two coarse absolute disparities (near vs. far) embedded in noise, reversible inactivation of area MT devastates performance. In contrast, after animals are trained to discriminate fine differences in relative disparity, MT inactivation no longer impairs coarse depth discrimination. This effect does not result from changes in the disparity tuning of MT neurons, suggesting plasticity in the flow of disparity signals to decision circuitry. These findings show that the contribution of particular brain area to task performance can change dramatically as a result of learning new tasks.

The process of stereoscopic depth perception is thought to begin with the analysis of absolute binocular disparity, the difference in position of corresponding features in the left and right eye images with respect to the points of fixation. Our sensitivity to depth, however, is greater when depth judgments are based on relative disparity, the difference between two absolute disparities, compared to when they are based on absolute disparity. Therefore, the visual system is thought to compute relative disparities for fine depth discrimination. Functional magnetic resonance imaging studies in humans and monkeys have suggested that visual areas V3 and V3A may be specialized for stereoscopic depth processing based on relative disparities. In this study, we measured absolute and relative disparity tuning of neurons in V3 and V3A of alert fixating monkeys and we compared their basic tuning properties with those published previously for other visual areas. We found that neurons in V3 and V3A predominantly encode absolute, not relative, disparities. We also found that basic parameters of disparity tuning in V3 and V3A are similar to those from other extrastriate visual areas. Finally, by comparing single-unit activity with multi-unit activity measured at the same recording site, we demonstrate that neurons with similar disparity selectivity are clustered in both V3 and V3A. We conclude that areas V3 and V3A are not particularly specialized for processing stereoscopic depth information compared to other early visual areas, at least with respect to the tuning properties that we have examined.

In a search phase of echolocation, big brown bats, Eptesicus fuscus, emit biosonar pulses at a rate of 10/s and listen to echoes. When a short acoustic stimulus was repetitively delivered at this rate, the reorganization of the frequency map of the primary auditory cortex took place at and around the neurons tuned to the frequency of the acoustic stimulus. Such reorganization became larger when the acoustic stimulus was paired with electrical stimulation of the cortical neurons tuned to the frequency of the acoustic stimulus. This reorganization was mainly due to the decrease in the best frequencies of the neurons that had best frequencies slightly higher than those of the electrically stimulated cortical neurons or the frequency of the acoustic stimulus. Neurons with best frequencies slightly lower than those of the acoustically and/or electrically stimulated neurons slightly increased their best frequencies. These changes resulted in the over-representation of repetitively delivered acoustic stimulus. Because the over-representation resulted in under-representation of other frequencies, the changes increased the contrast of the neural representation of the acoustic stimulus. Best frequency shifts for over-representation were associated with sharpening of frequency-tuning curves of 25% of the neurons studied. Because of the increases in both the contrast of neural representation and the sharpness of tuning, the over-representation of the acoustic stimulus is accompanied with an improvement of analysis of the acoustic stimulus.

Recent studies have described vestibular responses in the dorsal medial superior temporal area (MSTd), a region of extrastriate visual cortex thought to be involved in self-motion perception. The pathways by which vestibular signals are conveyed to area MSTd are currently unclear, and one possibility is that vestibular signals are already present in areas that are known to provide visual inputs to MSTd. Thus, we examined whether selective vestibular responses are exhibited by single neurons in the middle temporal area (MT), a visual motion-sensitive region that projects heavily to area MSTd. We compared responses in MT and MSTd to three-dimensional rotational and translational stimuli that were either presented using a motion platform (vestibular condition) or simulated using optic flow (visual condition). When monkeys fixated a visual target generated by a projector, half of MT cells (and most MSTd neurons) showed significant tuning during the vestibular rotation condition. However, when the fixation target was generated by a laser in a dark room, most MT neurons lost their vestibular tuning whereas most MSTd neurons retained their selectivity. Similar results were obtained for free viewing in darkness. Our findings indicate that MT neurons do not show genuine vestibular responses to self-motion; rather, their tuning in the vestibular rotation condition can be explained by retinal slip due to a residual vestibulo-ocular reflex. Thus, the robust vestibular signals observed in area MSTd do not arise through inputs from area MT.

Many neurons in the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas of the macaque brain are multisensory, responding to both optic flow and vestibular cues to self-motion. The heading tuning of visual and vestibular responses can be either congruent or opposite, but only congruent cells have been implicated in cue integration for heading perception. Because of the geometric properties of motion parallax, however, both congruent and opposite cells could be involved in coding self-motion when observers fixate a world-fixed target during translation, if congruent cells prefer near disparities and opposite cells prefer far disparities. We characterized the binocular disparity selectivity and heading tuning of MSTd and VIP cells using random-dot stimuli. Most (70%) MSTd neurons were disparity-selective with monotonic tuning, and there was no consistent relationship between depth preference and congruency of visual and vestibular heading tuning. One-third of disparity-selective MSTd cells reversed their depth preference for opposite directions of motion (direction-dependent disparity tuning, DDD), but most of these cells were unisensory with no tuning for vestibular stimuli. Inconsistent with previous reports, the direction preferences of most DDD neurons do not reverse with disparity. By comparison to MSTd, VIP contains fewer disparity-selective neurons (41%) and very few DDD cells. On average, VIP neurons also preferred higher speeds and nearer disparities than MSTd cells. Our findings are inconsistent with the hypothesis that visual/vestibular congruency is linked to depth preference, and also suggest that DDD cells are not involved in multisensory integration for heading perception.