A fundamental task of the visual system is to infer depth by using binocular disparity. To encode binocular disparity, the visual cortex performs two distinct computations: one detects matched patterns in paired images (matching computation); the other constructs the cross-correlation between the images (correlation computation). How the two computations are used in stereoscopic perception is unclear. We dissociated their contributions in near/far discrimination by varying the magnitude of the disparity across separate sessions. For small disparity (0.03°), subjects performed at chance level to a binocularly opposite-contrast (anti-correlated) random-dot stereogram (RDS) but improved their performance with the proportion of contrast-matched (correlated) dots. For large disparity (0.48°), the direction of perceived depth reversed with an anti-correlated RDS relative to that for a correlated one. Neither reversed nor normal depth was perceived when anti-correlation was applied to half of the dots. We explain the decision process as a weighted average of the two computations, with the relative weight of the correlation computation increasing with the disparity magnitude. We conclude that matching computation dominates fine depth perception, while both computations contribute to coarser depth perception. Thus, stereoscopic depth perception recruits different computations depending on the disparity magnitude.

SUMMARY Gamma components of the local field potential (LFP) are elevated during cognitive and perceptual processes. It has been suggested that gamma power indicates the strength of neuronal population synchrony, which influences the relaying of signals between cortical areas. However, the relationship between coordinated spiking activity and gamma remains unclear, and the influence on corticocortical signaling largely untested. We investigated these issues by recording from neuronal populations in areas V1 and V2 of anesthetized macaque monkeys. We found that visual stimuli that induce a strong, coherent gamma rhythm result in enhanced pairwise and higher-order V1 synchrony. This is associated with stronger coupling of V1-V2 spiking activity, in a retinotopically specific manner. Coupling is more strongly related to the gamma modulation of V1 firing than to the downstream V2 rhythm. Our results thus show that elevated gamma power is associated with stronger coordination of spiking activity both within and between cortical areas.

Numerous studies have shown that neuronal responses are modulated by stimulus properties, and also by the state of the local network. However, little is known about how activity fluctuations of neuronal populations modulate the sensory tuning of cells and affect their encoded information. We found that fluctuations in ongoing and stimulus-evoked population activity in primate visual cortex modulate the tuning of neurons in a multiplicative and additive manner. While distributed on a continuum, neurons with stronger multiplicative effects tended to have less additive modulation, and vice versa. The information encoded by multiplicatively-modulated neurons increased with greater population activity, while that of additively-modulated neurons decreased. These effects offset each other, so that population activity had little effect on total information. Our results thus suggest that intrinsic activity fluctuations may act as a `traffic light' that determines which subset of neurons are most informative.

A plane lying in depth is vividly perceived by viewing a random-dot stereogram (RDS) with a slight binocular disparity. Perception of a plane-in-depth is lost by reversing the contrast of dots seen by one of the eyes to generate an anticorrelated RDS. From a computational perspective, the visual system cannot find a globally consistent solution for matching the left and right eye images of an anticorrelated RDS. The neural representation of a global match should therefore be insensitive to binocular disparity in an anticorrelated RDS. Most neurons in the striate cortex (V1) respond to binocular disparity in anticorrelated RDSs, suggesting that further cortical processing in extrastriate areas is necessary to fully account for the matching computation. We examined neural responses to dynamic RDSs, both normal (correlated) and anticorrelated, in area V4 of the monkey visual cortex. More than half of the V4 cells were sensitive to the horizontal disparity embedded in a correlated RDS. Most of them greatly attenuated their selectivity for disparity when the RDS was anticorrelated. This attenuation was apparent from the response onset, and the degree of attenuation did not correlate with neuronal response latencies. Unlike the disparity tuning of V1 neurons to anticorrelated RDSs, that of V4 neurons was not an inversion of tuning to normal RDSs. Our results suggest that responses to false matches between contrast-reversed dots in the left and right eye images elicited in V1 are substantially reduced by the stage of V4.

Stereoscopic vision is characterized by greater visual acuity when a background feature serves as a reference. When a reference is present, the perceived depth of an object is predominantly dependent on this reference. Neural representations of stereoscopic depth are expected to have a relative frame of reference. The conversion of absolute disparity encoded in area V1 to relative disparity begins in area V2, although the information encoded in this area appears to be insufficient for stereopsis. This study examines whether relative disparity is encoded in a higher cortical area. We recorded the responses of V4 neurons from macaque monkeys to various combinations of the absolute disparities of two features: the center patch and surrounding annulus of a dynamic random-dot stereogram. We analyzed the effects of the disparity of the surrounding annulus on the tuning for the disparity of the center patch; the tuning curves of relative-disparity-selective neurons for disparities of the center patch should shift with changes in the disparity of the surrounding annulus. Most V4 tuning curves exhibited significant shifts. The magnitudes of the shifts were larger than those reported for V2 neurons and smaller than that expected for an ideal relative-disparity-selective cell. No correlation was found between the shift magnitude and the degree of size suppression, suggesting that the two phenomena are not the result of a common mechanism. Our results suggest that the coding of relative disparity advances as information flows along the cortical pathway that includes areas V2 and V4.

Primates are capable of discriminating depth with remarkable precision using binocular disparity. Neurons in area V4 are selective for relative disparity, which is the crucial visual cue for discrimination of fine disparity. Here, we investigated the contribution of V4 neurons to fine disparity discrimination. Monkeys discriminated whether the center disk of a dynamic random-dot stereogram was in front of or behind its surrounding annulus. We first behaviorally tested the reference frame of the disparity representation used for performing this task. After learning the task with a set of surround disparities, the monkey generalized its responses to untrained surround disparities, indicating that the perceptual decisions were generated from a disparity representation in a relative frame of reference. We then recorded single-unit responses from V4 while the monkeys performed the task. On average, neuronal thresholds were higher than the behavioral thresholds. The most sensitive neurons reached thresholds as low as the psychophysical thresholds. For subthreshold disparities, the monkeys made frequent errors. The variable decisions were predictable from the fluctuation in the neuronal responses. The predictions were based on a decision model in which each V4 neuron transmits the evidence for the disparity it prefers. We finally altered the disparity representation artificially by means of microstimulation to V4. The decisions were systematically biased when microstimulation boosted the V4 responses. The bias was toward the direction predicted from the decision model. We suggest that disparity signals carried by V4 neurons underlie precise discrimination of fine stereoscopic depth.

Stereo processing begins in the striate cortex and involves several extrastriate visual areas. We quantitatively analyzed the disparity-tuning characteristics of neurons in area V4 of awake, fixating monkeys. Approximately half of the analyzed V4 cells were tuned for horizontal binocular disparities embedded in dynamic random-dot stereograms (RDSs). Their response preferences were strongly biased for crossed disparities. To characterize the disparity-tuning profile, we fitted a Gabor function to the disparity-tuning data. The distribution of V4 cells showed a single dense cluster in a joint parameter space of the center and the phase parameters of the fitted Gabor function; most V4 neurons were maximally sensitive to fine stereoscopic depth increments near zero disparity. Comparing single-cell responses with background multiunit responses at the same sites showed that disparity-sensitive cells were clustered within V4 and that nearby cells possessed similar preferred disparities. Consistent with a recent report by Hegdé and Van Essen, the disparity tuning for an RDS drastically differed from that for a solid-figure stereogram (SFS). Disparity-tuning curves were generally broader for SFSs than for RDSs, and there was no correlation between the fitted Gabor functions' amplitudes, widths, or peaks for the two types of stereograms. The differences were partially attributable to shifts in the monocular images of an SFS. Our results suggest that the representation of stereoscopic depth in V4 is suited for detecting fine structural features protruding from a background. The representation is not generic and differs when the stimulus is broad-band noise or a solid figure.

Binocular disparity is an important visual cue that gives rise to the perception of depth. Disparity signals are widely spread across the visual cortex, but their relative role is poorly understood. Here, we addressed the correlation between the responses of disparity-selective neurons in the occipitotemporal (ventral) visual pathway and the behavioral discrimination of stereoscopic depth. We recorded activity of disparity-selective neurons in the inferior temporal cortex (IT) while monkeys were engaged in a fine stereoscopic depth discrimination (stereoacuity) task. We found that trial-to-trial fluctuations in neuronal responses correlated with the monkey's perceptual choice. We suggest that disparity signals in the IT, located in the ventral visual pathway, are functionally linked to the discrimination of fine-grain depth.