Duje Tadin

Perceptual consequences of centre-surround antagonism in visual motion processing.

Centre–surround receptive field organization is a ubiquitous property in mammalian visual systems, presumably tailored for extracting image features that are differentially distributed over space. In visual motion, this is evident as antagonistic interactions between centre and surround regions of the receptive fields of many direction-selective neurons in visual cortex. In a series of psychophysical experiments we make the counterintuitive observation that increasing the size of a high-contrast moving pattern renders its direction of motion more difficult to perceive and reduces its effectiveness as an adaptation stimulus. We propose that this is a perceptual correlate of centre–surround antagonism, possibly within a population of neurons in the middle temporal visual area. The spatial antagonism of motion signals observed at high contrast gives way to spatial summation as contrast decreases. Evidently, integration of motion signals over space depends crucially on the visibility of those signals, thereby allowing the visual system to register motion information efficiently and adaptively.

Endogenous attention prolongs dominance durations in binocular rivalry

We investigated the effects of attention on dominance durations during binocular rivalry. In a series of three experiments, observers performed several tasks while viewing rival stimuli to ensure and control deployment of attention. We found that endogenous attention can prolong dominance durations of attended stimulus. We developed a novel single-task procedure where observers responses in an attentional task were used to objectively estimate dominance durations of the attended stimulus. Using this procedure, we showed that paying attention to the stimulus features involved in rivalry is necessary for prolonging dominance durations--mere engagement of attention during rivalry was insufficient. Finally, we were able to simulate the effects of endogenous attention by doubling the contrast of the attended stimulus while it was dominant. Attention may increase the apparent contrast of the attended stimulus, thereby prolonging its dominance duration. Overall, our results indicate that dominance durations in rivalry can be prolonged when observers are performing an attentionally demanding task on the rival stimulus.

Weakened Center-Surround Interactions in Visual Motion Processing in Schizophrenia

Schizophrenia is often accompanied by a range of visual perception deficits, with many involving impairments in motion perception. The presence of perceptual abnormalities may impair neural processes that depend on normal visual analysis, which in turn may affect overall functioning in dynamic visual environments. Here, we examine the integrity of suppressive center-surround mechanisms in motion perception of schizophrenic patients. Center-surround suppression has been implicated in a range of visual functions, including figure–ground segregation and pursuit eye movements, visual functions that are impaired in schizophrenia. In control subjects, evidence of center-surround suppression is found in a reduced ability to perceive motion of a high-contrast stimulus as its size increases. This counterintuitive finding is likely a perceptual correlate of center-surround mechanisms in cortical area MT. We now show that schizophrenic patients exhibit abnormally weak center-surround suppression in motion, an abnormality that is most pronounced in patients with severe negative symptoms. Interestingly, patients with the weakest surround suppression outperformed control subjects in motion discriminations of large high-contrast stimuli. This enhanced motion perception of large high-contrast stimuli is consistent with an MT abnormality in schizophrenia and has a potential to disrupt smooth pursuit eye movements and other visual functions that depend on unimpaired center-surround interactions in motion.

A Substantial and Unexpected Enhancement of Motion Perception in Autism

Atypical perceptual processing in autism spectrum disorder (ASD) is well documented. In addition, growing evidence supports the hypothesis that an excitatory/inhibitory neurochemical imbalance might underlie ASD. Here we investigated putative behavioral consequences of the excitatory/inhibitory imbalance in the context of visual motion perception. As stimulus size increases, typical observers exhibit marked impairments in perceiving motion of high-contrast stimuli. This result, termed “spatial suppression,” is believed to reflect inhibitory motion-processing mechanisms. Motion processing is also affected by gain control, an inhibitory mechanism that underlies saturation of neural responses at high contrast. Motivated by these behavioral correlates of inhibitory function, we investigated motion perception in human children with ASD (n = 20) and typical development (n = 26). At high contrast, both groups exhibited similar impairments in motion perception with increasing stimulus size, revealing no apparent differences in spatial suppression. However, there was a substantial enhancement of motion perception in ASD: children with ASD exhibited a consistent twofold improvement in perceiving motion. Hypothesizing that this enhancement might indicate abnormal weakening of response gain control, we repeated our measurements at low contrast, where the effects of gain control should be negligible. At low contrast, we indeed found no group differences in motion discrimination thresholds. These low-contrast results, however, revealed weaker spatial suppression in ASD, suggesting the possibility that gain control abnormalities in ASD might have masked spatial suppression differences at high contrast. Overall, we report a pattern of motion perception abnormalities in ASD that includes substantial enhancements at high contrast and is consistent with an underlying excitatory/inhibitory imbalance.

Improved Motion Perception and Impaired Spatial Suppression following Disruption of Cortical Area MT/V5

As stimulus size increases, motion direction of high-contrast patterns becomes increasingly harder to perceive. This counterintuitive behavioral result, termed “spatial suppression,” is hypothesized to reflect center–surround antagonism—a receptive field property ubiquitous in sensory systems. Prior research proposed that spatial suppression of motion signals is a direct correlate of center–surround antagonism within cortical area MT. Here, we investigated whether human MT/V5 is indeed causally involved in spatial suppression of motion signals. The key assumption is that a disruption of neural mechanisms that play a critical role in spatial suppression could allow these normally suppressed motion signals to reach perceptual awareness. Thus, our hypothesis was that a disruption of MT/V5 should weaken spatial suppression and, consequently, improve motion perception of large, moving patterns. To disrupt MT/V5, we used offline 1 Hz transcranial magnetic stimulation (TMS)—a method that temporarily attenuates normal functioning of the targeted cortex. Early visual areas were also targeted as a control site. The results supported our hypotheses and showed that disruption of MT/V5 improved motion discrimination of large, moving stimuli, presumably by weakening surround suppression strength. This effect was specific to MT/V5 stimulation and contralaterally presented stimuli. Evidently, the critical neural constraints limiting motion perception of large, high-contrast stimuli involve MT/V5. Additionally, our findings mimic spatial suppression deficits that are observed in several patient populations and implicate impaired MT/V5 processes as likely neural correlates for the reported perceptual abnormalities in the elderly, patients with schizophrenia and those with a history of depression.

A Strong Interactive Link between Sensory Discriminations and Intelligence

Early psychologists, including Galton, Cattell, and Spearman, proposed that intelligence and simple sensory discriminations are constrained by common neural processes, predicting a close link between them. However, strong supporting evidence for this hypothesis remains elusive. Although people with higher intelligence quotients (IQs) are quicker at processing sensory stimuli, these broadly replicated findings explain a relatively modest proportion of variance in IQ. Processing speed alone is, arguably, a poor match for the information processing demands on the neural system. Our brains operate on overwhelming amounts of information, and thus their efficiency is fundamentally constrained by an ability to suppress irrelevant information. Here, we show that individual variability in a simple visual discrimination task that reflects both processing speed and perceptual suppression strongly correlates with IQ. High-IQ individuals, although quick at perceiving small moving objects, exhibit disproportionately large impairments in perceiving motion as stimulus size increases. These findings link intelligence with low-level sensory suppression of large moving patterns--background-like stimuli that are ecologically less relevant. We conjecture that the ability to suppress irrelevant and rapidly process relevant information fundamentally constrains both sensory discriminations and intelligence, providing an information-processing basis for the observed link.

Perceptual and neural consequences of rapid motion adaptation

Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes direction-selective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion.

Adaptive center-surround interactions in human vision revealed during binocular rivalry

We used binocular rivalry as a psychophysical probe to explore center-surround interactions in orientation, motion and color processing. Addition of the surround matching one of the rival targets dramatically altered rivalry dynamics. For all visual sub-modalities tested, predominance of the high-contrast rival target matched to the surround was greatly reduced-a result that disappeared at low contrast. At low contrast, addition of the surround boosted dominance of orientation and motion targets matched to the surround. This contrast-dependent modulation of center-surround interactions seems to be a general property of the visual system and may reflect an adaptive balance between surround suppression and spatial summation.

The effects of transcranial magnetic stimulation on visual rivalry

One extensively investigated form of perceptual bistability is binocular rivalry--When dissimilar patterns are presented one to each eye, these patterns compete for perceptual dominance. Here, we report that transcranial magnetic stimulation (TMS) over early visual areas induces alternations during binocular rivalry. The effect of TMS on binocular rivalry was retinotopic, suggesting that rivalry mechanisms are localized in the cortical representation of visual space. The timing of perturbations was highly dependent on individual differences in rivalry alternation frequencies, with more delayed effects found in slower alternators. This finding suggests that both binocular rivalry and TMS dynamics might be contingent on individual differences among observers. We performed an analogous set of experiments by replacing TMS with transient visual stimulation. The results, however, qualitatively and quantitatively differed from those reported with TMS. Finally, we found that TMS over early visual areas does not produce any time-locked effects on another dynamical process--eye-swapping stimulus rivalry. These findings constitute the first causative evidence that binocular rivalry is contingent on neural activity in early visual areas and suggest that binocular rivalry and stimulus rivalry have different neural correlates, supporting multilevel theories of visual rivalry.

Visual context processing in schizophrenia.

Abnormal perceptual experiences are central to schizophrenia, but the nature of these anomalies remains undetermined. We investigated contextual processing abnormalities across a comprehensive set of visual tasks. For perception of luminance, size, contrast, orientation, and motion, we quantified the degree to which the surrounding visual context altered a center stimulus’s appearance. Healthy participants showed robust contextual effects across all tasks, as evidenced by pronounced misperceptions of center stimuli. Schizophrenia patients exhibited intact contextual modulations of luminance and size but showed weakened contextual modulations of contrast, performing more accurately than controls. Strong motion and orientation context effects correlated with worse symptoms and social functioning. Importantly, the overall strength of contextual modulation across tasks did not differ between controls and schizophrenia patients. In addition, performance measures across contextual tasks were uncorrelated, implying discrete underlying processes. These findings reveal that abnormal contextual modulation in schizophrenia is selective, arguing against the proposed unitary contextual processing dysfunction.