We have previously documented the exquisite motion sensitivity of neurons in extrastriate area MT by studying the relationship between their responses and the direction and strength of visual motion signals delivered to their receptive fields. These results suggested that MT neurons might provide the signals supporting behavioral choice in visual discrimination tasks. To approach this question from another direction, we have now studied the relationship between the discharge of MT neurons and behavioral choice, independently of the effects of visual stimulation. We found that trial-to-trial variability in neuronal signals was correlated with the choices the monkey made. Therefore, when a directionally selective neuron in area MT fires more vigorously, the monkey is more likely to make a decision in favor of the preferred direction of the cell. The magnitude of the relationship was modest, on average, but was highly significant across a sample of 299 cells from four monkeys. The relationship was present for all stimuli (including those without a net motion signal), and for all but the weakest responses. The relationship was reduced or eliminated when the demands of the task were changed so that the directional signal carried by the cell was less informative. The relationship was evident within 50 ms of response onset, and persisted throughout the stimulus presentation. On average, neurons that were more sensitive to weak motion signals had a stronger relationship to behavior than those that were less sensitive. These observations are consistent with the idea that neuronal signals in MT are used by the monkey to determine the direction of stimulus motion. The modest relationship between behavioral choice and the discharge of any one neuron, and the prevalence of the relationship across the population, make it likely that signals from many neurons are pooled to form the data on which behavioral choices are based.

We recorded the responses of single neurons in extrastriate area MST while rhesus monkeys discriminated the direction of motion in a set of stochastic visual displays. By varying systematically the strength of a coherent motion signal within the visual display, we were able to measure simultaneously the monkeys' psychophysical thresholds for direction discrimination and the responses of single neurons to the same motion signals. Neuronal thresholds for reliably signaling the direction of motion in the visual display were calculated from the measured responses using a method based in signal detection theory. Neurons in MST were exquisitely sensitive to motion signals in the display, having thresholds for discriminating the direction of coherent motion that were, on average, equal to the psychophysical thresholds of the monkeys. For many MST neurons, the intensity of the response was correlated with the monkey's psychophysical judgements for repeated presentations of a given near-threshold stimulus; the monkey tended to choose the preferred direction of the neuron under study when that neuron responded more strongly to the stimulus. In both of these respects, MST neurons were indistinguishable from neurons in extrastriate area MT, a major source of afferent input to MST. In a second set of experiments, we found that both of these results held true in the face of pronounced manipulations of the visual stimulus. Severe reductions in stimulus size and speed, for example, compromised neuronal and psychophysical sensitivities by similar amounts so that the average neuronal and psychophysical thresholds remained approximately equal. In addition, the trial-to-trial covariation of neuronal response and perceptual decision was unaffected by our stimulus manipulations. Thus, MST neurons carry signals appropriate for supporting psychophysical performance on our task over an impressively wide range of stimulus configurations.

To localize objects in space, the brain needs to combine information about the position of the stimulus on the retinae with information about the location of the eyes in their orbits. Interaction between these two types of information occurs in several cortical areas, but the role of the primary visual cortex (area V1) in this process has remained unclear. Here we show that, for half the cells recorded in area V1 of behaving monkeys, the classically described visual responses are strongly modulated by gaze direction. Specifically, we find that selectivity for horizontal retinal disparity-the difference in the position of a stimulus on each retina which relates to relative object distance-and for stimulus orientation may be present at a given gaze direction, but be absent or poorly expressed at another direction. Shifts in preferred disparity also occurred in several neurons. These neural changes were most often present at the beginning of the visual response, suggesting a feedforward gain control by eye position signals. Cortical neural processes for encoding information about the three-dimensional position of a stimulus in space therefore start as early as area V1.

To investigate the importance of feedback loops in visual information processing, we have analyzed the dynamic aspects of neuronal responses to oriented gratings in cortical area V1 of the awake primate. If recurrent feedback is important in generating orientation selectivity, the initial part of the neuronal response should be relatively poorly selective, and full orientation selectivity should only appear after a delay. Thus, by examining the dynamics of the neuronal responses it should be possible to assess the importance of feedback processes in the development of orientation selectivity. The results were base on a sample of 259 cells recorded in two monkeys, of which 89% were visually responsive. Of these, approximately two-thirds were orientation selective. Response latency varied considerably between neurons, ranging from a minimum of 41 ms to over 150 ms, although most had latencies of 50–70 ms. Orientation tuning (defined as the bandwidth at half-height) ranged from 16 deg to over 90 deg, with a mean value of around 55 deg. By examining the selectivity of these different neurons by 10-ms time slices, starting at the onset of the neuronal response, we found that the orientation selectivity of virtually every neuron was fully developed at the very start of the neuronal response. Indeed, many neurons showed a marked tendency to respond at somewhat longer latencies to stimuli that were nonoptimally oriented, with the result that orientation selectivity was highest at the very start of the neuronal response. Furthermore, there was no evidence that the neurons with the shortest onset latencies were less selective. Such evidence is inconsistent with the hypothesis that recurrent intracortical feedback plays an important role in the generation of orientation selectivity. Instead, we suggest that orientation selectivity is primarily generated using feedforward mechanisms, including feedforward inhibition. Such a strategy has the advantage of allowing orientation to be computed rapidly, and avoids the initially poorly selective neuronal responses that characterize processing involving recurrent loops.

Background: Visual, tactile and auditory information is processed from the periphery to the cortical level through separate channels that target primary sensory cortices, from which it is further distributed to functionally specialized areas. Multisensory integration is classically assigned to higher hierarchical cortical areas, but there is growing electrophysiological evidence in man and monkey of multimodal interactions in areas thought to be unimodal, interactions that can occur at very short latencies. Such fast timing of multisensory interactions rules out the possibility of an origin in the polymodal areas mediated through back projections, but is rather in favor of heteromodal connections such as the direct projections observed in the monkey, from auditory areas (including the primary auditory cortex AI) directly to the primary visual cortex V1. Based on the existence of such AI to V1 projections, we looked for modulation of neuronal visual responses in V1 by an auditory stimulus in the awake behaving monkey.

The electrophysiological properties of sensory neurons in the adult cortex are not immutable but can change in response to alterations of sensory input caused by manipulation of afferent pathways in the nervous system or by manipulation of the sensory environment. Such plasticity creates great potential for flexible processing of sensory information, but the actual effects of neuronal plasticity on perceptual performance are poorly understood. The link between neuronal plasticity and performance was explored here by recording the responses of directionally selective neurons in the visual cortex while rhesus monkeys practiced a familiar task involving discrimination of motion direction. Each animal experienced a short-term improvement in perceptual sensitivity during daily experiments; sensitivity increased by an average of 19 percent over a few hundred trials. The increase in perceptual sensitivity was accompanied by a short-term improvement in neuronal sensitivity that mirrored the perceptual effect both in magnitude and in time course, which suggests that improved psychophysical performance can result directly from increased neuronal sensitivity within a sensory pathway.

Accurate binocular depth perception requires information about both stereopsis (relative depth) and distance (absolute depth). It is unclear how these two types of information are integrated in the visual system. In alert, behaving monkeys the responsiveness of a large majority of neurons in the primary visual cortex (area V1) was modulated by the viewing distance. This phenomenon affected particularly disparity-related activity and background activity and was not dependent on the pattern of retinal stimulation. Therefore, extraretinal factors, probably related to ocular vergence or accommodation, or both, can affect processing early in the visual pathway. Such modulations could be useful for (i) judging true distance and (ii) scaling retinal disparity to give information about three-dimensional shape.

Gaze direction modulates the gain of neurons in most of the visual cortex, including the primary visual (V1) area. These gain modulations are thought to support a mechanism involved in the spatial localization of objects. In the present study, we show that part of them may reflect an additional function: enhancing the visual processing of the objects located straight ahead. Using single- and multiunit recordings in behaving macaques, we found that in peripheral V1, the gain of most neurons increases as their receptive fields (RF) are brought closer to the straight-ahead direction by changing the direction of gaze. No such tendency was observed in central V1, although the influence of gaze direction is similar in term of strength. This previously unknown organization of the gaze-related gain modulations might insure that objects located straight ahead still receive a privileged processing during eccentric fixation, reflecting the ecological importance of this particular egocentric direction.