Gaze direction controls response gain in primary visual-cortex neurons.

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.

Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1.

1. The influence of viewing distance on disparity selectivity was investigated in area V1 of behaving monkeys. While the animals performed a fixation task, cortical cells were recorded extracellularly in the foveal representation of the visual field. Disparity selectivity was assessed by using static random dot stereograms (RDSs) through red/green filters flashed over the central fixation target. To determine the influence of the viewing distance, a color video monitor was positioned at fixed distances of 20, 40, or 80 cm. The same RDSs with the same angular size of dots were used at the three distances. 2. Disparity sensitivity was tested on 139 cells, of which 78 were analyzed at two or more distances and the rest (61) at a single distance. When disparity selectivity was analyzed at a given distance, about half the cells were found to be selective at 40 or 80 cm, but only a third at 20 cm. Near cells were > or = 1.5 times more common than far cells at all three distances. The latency distribution of the responses of disparity-selective (DS) cells was similar at all three distances, with a mean distribution centered around 60 ms. 3. Changing the viewing distance drastically affected the neural activity of the V1 neurons. The visual responsiveness of 60 of 78 cells (77%) was significantly changed. Disparity selectivity could be present at a given distance and absent at other(s), with often a loss of visual response. This emergence of disparity coding was the strongest effect (28 of 78 or 36%) and occurred more frequently from short to long distances. Among the cells that remained disparity insensitive at all recorded distances (31 of 78 or 40%), about half also showed modulations of the amplitude of the visual response. For cells that remained DS at all recorded distances (13 of 78 or 17%), changing the viewing distance also affected the sharpness (or magnitude) of disparity coding in terms of level of visual responsiveness and those changes were often combined with variations in tuning width. In only two cells did the peak of selectivity type change. Finally, the activity of four DS cells was not affected at all by the viewing distance. 4. Another effect concerned the level of ongoing activity (OA), defined as being the neural activity in darkness preceding the flash of the visual stimulus while the monkey was fixating the small bright target. Changing the viewing distance resulted in significant changes in OA level for more than half of the cells (41 of 78 or 53%). The most common effect was an increase in OA level at the shorter distance. The modulations of both visual responsiveness and OA could occur simultaneously, although they often had opposite signs. Indeed, the two effects were statistically independent of each other, i.e., modulations of visual responses were not related to the level of excitability of the neurons. 5. Control experiments were performed that showed that the effects of changing the viewing distance were not due to the retinal patterns in that the modulations of visual responsiveness were independent of the dot density. Seventeen cells were also tested for a possible effect of vergence by the use of prisms. When there was an effect of distance, it could be closely or partially reproduced by using prisms. These controls, together with the effects observed on OA, strongly suggest that the modulations of neural activity of the V1 neurons by the viewing distance are extraretinal in origin, probably proprioceptive. 6. The modulation of visual responsiveness by the viewing distance in the primary visual cortex indicates that integration of information from both retinal and extraretinal sources can occur early in the visual processing pathway for cortical representation of three-dimensional space. A functional scheme of three-dimensional cortical circuitry is discussed that shows cortical areas where disparity selectivity and modulations of visual activity by the angle of gaze have been described so far.

A relationship between behavioral choice and the visual responses of neurons in macaque MT.

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.

Microstimulation of extrastriate area MST influences performance on a direction discrimination task.

1. Evidence from single-unit recordings suggests that neurons in the medial superior temporal visual area (MST) carry directional signals that influence psychophysical judgements of motion direction. We tested this hypothesis by electrically stimulating clusters of directionally selective neurons in MST (the dorsomedial subdivision, primarily) while rhesus monkeys performed a two-alternative, forced-choice direction discrimination task. 2. We performed forty-six microstimulation experiments on two rhesus monkeys. The visual stimuli were dynamic random dot patterns in which the strength of a coherent motion signal could be varied continuously about psychophysical threshold. The monkeys were rewarded for reporting correctly the direction of the coherent motion signal. Microstimulation was applied on half the trials, selected randomly, and the psychophysical data were analyzed to determine whether stimulation of MST neurons influenced the monkeys' choices. 3. Microstimulation influenced the monkeys' performance in a statistically significant manner in 67% of the experiments. In all but one of the significant experiments, microstimulation biased the monkeys' choices toward the direction of motion encoded by MST neurons at the stimulation site. Microstimulation had little effect on the slopes of the psychometric functions, suggesting that the stimulation-induced neural activity resembled a relatively pure motion "signal" rather than "noise." 4. Microstimulation exerted strong effects on the monkeys' behavior only when the visual stimulus was located within the multiunit receptive field measured at the stimulation site. This kind of spatial specificity has also been observed in the middle temporal visual area (MT), but receptive fields in MST are typically much larger than those in MT. Thus MST microstimulation effects are characterized by a coarser spatial scale: stimulation of a single site in MST can influence judgements over a much larger portion of the visual field than equivalent stimulation in MT. 5. Microstimulation was often most effective when visual stimuli were placed within a particularly responsive subregion of the receptive field (a "hot spot"). 6. The results show that MST neurons, like MT neurons, can strongly influence performance on a direction discrimination task. Whether MT and MST influence the decision process in parallel or in series remains to be determined.

Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey.

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.

Neuronal plasticity that underlies improvement in perceptual performance.

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.

Dynamics of orientation coding in area V1 of the awake primate.

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.

Long-term dysfunctions of neural stereoscopic mechanisms after unilateral extraocular muscle proprioceptive deafferentation.

1. Neural correlates of the permanent deficits in depth perception that occur when extraocular muscle proprioceptive (EMP) afferents are interrupted unilaterally in kittens were investigated by performing extracellular recordings in the primary visual cortex (area 17) in adulthood. Unilateral section of the ophthalmic branch of the trigeminal nerve (V1 nerve) were performed in 11 cats when they were between 5 and 12 weeks of age (uni-V1 group). Electrophysiological results were compared with those obtained in 17 normal adult cats (control group). 2. Binocular interactions were assessed by testing the sensitivity of cortical neurons to dichoptic presentations of moving sine-wave gratings whose interocular positional phase relationship was randomly varied. The amplitude modulation between the minimum and the maximum binocular responses defined the dynamic range. The degree of binocular suppression or facilitation was assessed by comparing these binocular response limits with the optimal monocular responses evoked through either eye at the best spatial frequency. The variability of both monocular and binocular responses was estimated by using the variation coefficient. 3. In uni-V1 cats, both the dynamic range and the degree of binocular suppression were significantly less pronounced than in controls, whereas binocular facilitation was not affected. The variability of the binocular responses was significantly increased, unlike monocular responses, whose variability was similar to control values. 4. From Fourier analysis of the poststimulus time histograms, two clear-cut categories of cells emerged that were differentially affected in the uni-V1 group. The "modulated" cells showed significantly less binocular suppression than in controls, and the "unmodulated" cells had binocular responses that were significantly more variable than in controls. Results from "simple" cells were similar to those of modulated cells, and results from "complex" cells were similar to those of unmodulated cells. However, in the unmodulated population, which was composed of both simple and complex cells, it was shown that the increase of variability was due to that of complex cells. 5. A nonparametric statistical test was applied on the interocular phase shift tuning curves to determine the minimum stimulus change necessary to elicit a significant change in the neural response. Two categories of cells were determined: the "discriminative" cells (80% in controls but 45% in uni-V1 cats) combined pronounced binocular suppression and dynamic range with relatively low variability. The reverse was true in the case of "nondiscriminative" cells (20% in controls and 55% in uni-V1 cats). 6. In uni-V1 cats, about half of the cells were monocularly activated.(ABSTRACT TRUNCATED AT 400 WORDS)

Modulation of neural stereoscopic processing in primate area V1 by the viewing distance.

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.

Neuronal stereoscopic processing following extraocular proprioception deafferentation.

In adult cats, after section of extraocular muscle proprioceptive (EOMP) afferents during the 'critical period', most cortical area 17 cells loose their ability to discriminate changes in binocular spatial disparity. After unilateral section this loss depends on whether or not cortical cells modulate their responses to the presentation of sinusoidal gratings linearly. For 'modulated cells', this loss is due to a reduction of binocular suppression while for 'unmodulated cells', it is due to a selective increase in the variability of the binocular response. These permanent neural dysfunctions show that balance in EOMP inflow plays a crucial role in cortical processing of binocular depth discrimination.