Faculty Bibliography

Early experience affects the development of the visual system. Ocular misalignment or unilateral blur often causes amblyopia, a disorder that has become a standard for understanding developmental plasticity. Neurophysiological studies of amblyopia have focused almost entirely on the first stage of cortical processing in striate cortex. Here we provide the first extensive study of how amblyopia affects extrastriate cortex in nonhuman primates. We studied macaque monkeys (Macaca nemestrina) for which we have detailed psychophysical data, directly comparing physiological findings to perceptual capabilities. Because these subjects showed deficits in motion discrimination, we focused on area MT/V5, which plays a central role in motion processing. Most neurons in normal MT respond equally to visual stimuli presented through either eye; most recorded in amblyopes strongly preferred stimulation of the nonamblyopic (fellow) eye. The pooled responses of neurons driven by the amblyopic eye showed reduced sensitivity to coherent motion and preferred higher speeds, in agreement with behavioral measurements. MT neurons were more limited in their capacity to integrate motion information over time than expected from behavioral performance; neurons driven by the amblyopic eye had even shorter integration times than those driven by the fellow eye. We conclude that some, but not all, of the motion sensitivity deficits associated with amblyopia can be explained by abnormal development of MT

Analysis of the movement of a complex visual stimulus is expressed in the responses of pattern-direction-selective neurons in area MT, which depend in turn on directionally selective inputs from area V1. How do MT neurons integrate their inputs? Pattern selectivity in MT breaks down when the gratings comprising a moving plaid are presented to non-overlapping regions of the (monocular) receptive field. Here we ask an analogous question, is pattern selectivity maintained when the component gratings are presented dichoptically to binocular MT neurons? We recorded from single units in area MT, measuring responses to monocular gratings and plaids, and to dichoptic plaids in which the components are presented separately to each eye. Neurons that are pattern selective when tested monocularly lose this selectivity when stimulated with dichoptic plaids. When human observers view these same stimuli, dichoptic plaids induce binocular rivalry. Yet motion signals from each eye can be integrated despite rivalry, revealing a dissociation of form and motion perception. These results reveal the role of monocular mechanisms in the computation of pattern motion in single neurons, and demonstrate that the perception of motion is not fully represented by the responses of individual MT neurons

Neural responses are typically characterized by computing the mean firing rate, but response variability can exist across trials. Many studies have examined the effect of a stimulus on the mean response, but few have examined the effect on response variability. We measured neural variability in 13 extracellularly recorded datasets and one intracellularly recorded dataset from seven areas spanning the four cortical lobes in monkeys and cats. In every case, stimulus onset caused a decline in neural variability. This occurred even when the stimulus produced little change in mean firing rate. The variability decline was observed in membrane potential recordings, in the spiking of individual neurons and in correlated spiking variability measured with implanted 96-electrode arrays. The variability decline was observed for all stimuli tested, regardless of whether the animal was awake, behaving or anaesthetized. This widespread variability decline suggests a rather general property of cortex, that its state is stabilized by an input

Retinal image motion is produced with each eye movement, yet we usually do not perceive this self-produced 'reafferent' motion, nor are motion judgments much impaired when the eyes move. To understand the neural mechanisms involved in processing reafferent motion and distinguishing it from the motion of objects in the world, we studied the visual responses of single cells in middle temporal (MT) and medial superior temporal (MST) areas during steady fixation and smooth-pursuit eye movements in awake, behaving macaques. We measured neuronal responses to random-dot patterns moving at different speeds in a stimulus window that moved with the pursuit target and the eyes. This allowed us to control retinal image motion at all eye velocities. We found the expected high proportion of cells selective for the direction of visual motion. Pursuit tracking changed both response amplitude and preferred retinal speed for some cells. The changes in preferred speed were on average weakly but systematically related to the speed of pursuit for area MST cells, as would be expected if the shifts in speed selectivity were compensating for reafferent input. In area MT, speed tuning did not change systematically during pursuit. Many cells in both areas also changed response amplitude during pursuit; the most common form of modulation was response suppression when pursuit was opposite in direction to the cell's preferred direction. These results suggest that some cells in area MST encode retinal image motion veridically during eye movements, whereas others in both MT and MST contribute to the suppression of visual responses to reafferent motion

In this issue of Neuron, Chowdhury and DeAngelis report that training monkeys to perform a fine depth discrimination abolishes the contribution of signals from area MT to the execution of a different, coarse depth discrimination. This result calls into question the principle of associating particular visual areas with particular visual functions, by showing that such associations are modifiable by experience

In this issue of Neuron, Ajemian et al. present a computational model of the activity of neurons in primary motor cortex (M1) during isometric movements in different postures. By modeling the output of M1 neurons in terms of their influence on muscles, they find each M1 neuron maps its output into a particular pattern of muscle actions

We experience the visual world as phenomenally invariant to eye position, but almost all cortical maps of visual space in monkeys use a retinotopic reference frame, that is, the cortical representation of a point in the visual world is different across eye positions. It was recently reported that human cortical area MT (unlike monkey MT) represents stimuli in a reference frame linked to the position of stimuli in space, a 'spatiotopic' reference frame. We used visuotopic mapping with blood oxygen level-dependent functional magnetic resonance imaging signals to define 12 human visual cortical areas, and then determined whether the reference frame in each area was spatiotopic or retinotopic. We found that all 12 areas, including MT, represented stimuli in a retinotopic reference frame. Although there were patches of cortex in and around these visual areas that were ostensibly spatiotopic, none of these patches exhibited reliable stimulus-evoked responses. We conclude that the early, visuotopically organized visual cortical areas in the human brain (like their counterparts in the monkey brain) represent stimuli in a retinotopic reference frame