Some neurons in the visual cortex alter their spiking rate according to the perceptual interpretation of an observed stimulus, rather than its physical structure alone. Experiments in monkeys have suggested that, although the proportion of neurons showing this effect differs greatly between cortical areas, this proportion remains similar across different stimuli. These findings have raised the intriguing questions of whether the same neurons always participate in the disambiguation of sensory patterns and whether such neurons might represent a special class of cortical cells that relay perceptual signals to higher cortical areas. Here we explore this question by measuring activity in the middle temporal cortex of monkeys and asking to what degree the percept-related responses of individual neurons depend upon the specific sensory input. In contrast to our expectations, we found that even small differences in the stimuli led to significant changes in the signaling of the perceptual state by single neurons. We conclude that nearly all feature-responsive neurons in this area, rather than a select subset, can contribute to the resolution of sensory conflict, and that the role of individual cells in signaling the perceptual outcome is tightly linked to the fine details of the stimuli involved.

In the primary visual cortex (V1), the responses of neurons to stimuli presented in their classical receptive fields (CRFs) are modulated by another stimulus concurrently presented in their surround (receptive field surround, SRF). We studied the nature of the modulatory effects of SRF stimulation with respect to stimulus contrast in cat V1. In 51 V1 neurons studied, large SRF stimuli (40 degreesx30 degrees ) induced only the suppression of responses to CRF stimulation and the suppressive effects became stronger as the contrast for SRF stimulation increased. The contrast sensitivity of SRF suppression did not correlate with that of CRF responses. By independently controlling contrast of CRF and SRF stimuli, we studied whether SRF effects vary with CRF response magnitude. Increasing contrast for CRF stimulation caused an upward shift of the range of effective contrasts for SRF stimulation, indicating that a high contrast for SRF stimulation is required for suppressing strong responses to CRF stimulation at high contrasts. To assess the possible origin of the suppressive SRF effect on V1 neurons, we also investigated the contrast dependency of SRF effects in 28 neurons from the lateral geniculate nucleus. Our results suggest that SRF effects obtained at the subcortical level strongly contribute to those in V1. Taken together, we conclude that along the thalamocortical projections, SRF modulation exhibits a gain-control mechanism that scales the suppressive SRF effect depending on the contrast for CRF stimulation. In addition, SRF effects can be facilitatory at low stimulus contrasts potentially due to the enlargement of the summation field.

Contextual modulations of receptive field properties by distal stimulus configurations have been shown for a variety of stimulus paradigms. A survey of excitatory contextual modulation data for V1 shows the maximum scale of interactions, measured in terms of distance in V1, to be between 10 mm and 30 mm. Different types of excitatory contextual modulation in V1 occur throughout the interval of 40–250 ms after stimulus delivery. This window provides opportunity for global propagation of visual contextual information to a subset of V1 neurons, via several routes within the visual system. We propose a number of experiments and analyses to confirm the results from this empirical survey.

The segregation of figure from ground is arguably one of the most fundamental operations in human vision. Neural signals reflecting this operation appear in cortex as early as 50 ms and as late as 300 ms after presentation of a visual stimulus, but it is not known when these signals are used by the brain to construct the percepts of figure and ground. We used psychophysical reverse correlation to identify the temporal window for figure-ground signals in human perception, and found it to lie within the range 100-160 ms. Figure enhancement within this narrow temporal window was transient, rather than sustained as may be expected from measurements in single neurons. These psychophysical results prompt and guide further electrophysiological investigations.

Extraclassical receptive field phenomena in V1 are commonly attributed to long-range lateral connections and/or extrastriate feedback. We address 2 such phenomena: surround suppression and receptive field expansion at low contrast. We present rigorous computational support for the hypothesis that the phenomena largely result from local short-range (<0.5 mm) cortical connections and lateral geniculate nucleus input. The neural mechanisms of surround suppression in our simulations operate via (A) enhancement of inhibition, (B) reduction of excitation, or (C) action of both simultaneously. Mechanisms (B) and (C) are substantially more prevalent than (A). We observe, on average, a growth in the spatial summation extent of excitatory and inhibitory synaptic inputs for low-contrast stimuli. However, we find this is neither sufficient nor necessary to explain receptive field expansion at low contrast, which usually involves additional changes in the relative gain of these inputs.

It has been proposed that sensory neurons are adapted to the statistical structure of the natural environment in order to encode natural stimuli efficiently. While spatiotemporal correlations in luminance signals may be decorrelated by neurons in early visual processing stages, higher-order correlations, such as those in the orientation domain, are likely to persist in the input representation until the cortical level. In this study, we first examine orientation correlations in natural stimuli across brief time intervals and across nearby regions of space, and find strong correlations in both domains. We then examine contextual modulation of orientation tuning. We find that both temporal and spatial contexts exert a common influence on orientation tuning, shifting tuning away from the orientation of either the adapting (temporal) or surrounding (spatial) grating. Finally, we incorporate this context-mediated repulsive shift in orientation tuning into a model of cortical responses. We find that a direct result of the shift is a reduction of the redundancy in the population responses evoked by the orientation configurations that are most common in natural stimuli. Thus, cortical neurons may be adapted to the statistics of orientation in natural stimuli in order to increase the efficiency of natural stimulus representation.

In natural behavioral situations, saccadic eye movements not only introduce new stimuli into V1 receptive fields, they also cause changes in the background. We recorded in awake macaque V1 using a fixation paradigm and compared evoked activity to small stimuli when the background was either static or changing as with a saccade. When a stimulus was shown on a static background, as in most previous experiments, the initial response was orientation selective and contrast was inversely correlated with response latency. When a stimulus was introduced with a background change, V1 neurons showed a qualitatively different temporal response pattern in which information about stimulus orientation and contrast was delayed. The delay in the representation of visual information was found with three different types of background change-luminance increment, luminance decrement, and a pattern change with fixed mean luminance. We also found that with a background change, V1 off responses were suppressed and had a shorter time course compared with the static-background situation. Our results suggest that the distribution of temporal changes across the visual field plays a fundamental role in determining V1 responses. In the static-background condition, temporal change in the visual input occurs only in a small portion of the visual field. In the changing-background condition, and presumably in natural vision, temporal changes are widely distributed. Thus a delayed representation of visual information may be more representative of natural visual situations.

The spatial focus of attention has traditionally been envisioned as a simple spatial gradient of enhanced activity that falls off monotonically with increasing distance. Here, we show with high-density magnetoencephalographic recordings in human observers that the focus of attention is not a simple monotonic gradient but instead contains an excitatory peak surrounded by a narrow inhibitory region. To demonstrate this center-surround profile, we asked subjects to focus attention onto a color pop-out target and then presented probe stimuli at various distances from the target. We observed that the electromagnetic response to the probe was enhanced when the probe was presented at the location of the target, but the probe response was suppressed in a narrow zone surrounding the target and then recovered at more distant locations. Withdrawing attention from the pop-out target by engaging observers in a demanding foveal task eliminated this pattern, confirming a truly attention-driven effect. These results indicate that neural enhancement and suppression coexist in a spatially structured manner that is optimal to attenuate the most deleterious noise during visual object identification.

Visual context often plays a crucial role in visual processing. In the domain of visual motion processing, the response to a stimulus presented to a neuron's classical receptive field can be modulated by presenting stimuli to its surround. The nature of these center-surround interactions is often inhibitory; the neural response decreases when the same direction of motion is presented to center and surround. Here we use binocular rivalry as a tool to study center-surround interactions. We show that magnitude of surround suppression varies as a function of luminance contrast and surround width. Increasing the size of surround motion increased surround suppression at high contrast. Furthermore, large, high-contrast surrounds facilitated opposite-direction motion in the center. For stimuli presented at low contrast, surround suppression peaked at a smaller surround width. In addition, we provide evidence that surround inhibition occurs at multiple levels of visual processing: Surround inhibition in motion processing is likely to originate from both monocular and binocular processing stages.

We studied the effects of various patterns as contextual stimuli on human orientation discrimination, and on responses of neurons in V1 of alert monkeys. When a target line is presented along with various contextual stimuli (masks), human orientation discrimination is impaired. For most V1 neurons, responses elicited by a line in the receptive field (RF) center are suppressed by these contextual patterns. Orientation discrimination thresholds of human observers are elevated slightly when the target line is surrounded by orthogonal lines. For randomly oriented lines, thresholds are elevated further and even more so for lines parallel to the target. Correspondingly, responses of most V1 neurons to a line are suppressed. Although contextual lines inhibit the amplitude of orientation tuning functions of most V1 neurons, they do not systematically alter the tuning width. Elevation of human orientation discrimination thresholds decreases with increasing curvature of masking lines, so does the inhibition of V1 neuronal responses. A mask made of straight lines yields the strongest interference with human orientation discrimination and produces the strongest suppression of neuronal responses. Elevation of human orientation discrimination thresholds is highest when a mask covers only the immediate vicinity of the target line. Increasing the masking area results in less interference. On the contrary, suppression of neuronal responses in V1 increases with increasing mask size. Our data imply that contextual interference observed in human orientation discrimination is in part directly related to contextual inhibition of neuronal activity in V1. However, the finding that interference with orientation discrimination is weaker for larger masks suggests a figure-ground segregation process that is not located in V1