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BACKGROUND AND HYPOTHESIS: The human visual system streamlines visual processing by suppressing responses to textures that are similar to their surrounding context. Surround suppression is weaker in individuals with schizophrenia (ISZ); this altered use of visuospatial context may relate to the characteristic visual distortions they experience. STUDY DESIGN: To understand atypical surround suppression in psychotic psychopathology, we investigated neurophysiological responses in ISZ, healthy controls (HC), individuals with bipolar disorder (IBP), and first-degree relatives (ISZR/IBPR). Participants performed a contrast judgment task on a circular target with annular surrounds, with concurrent electroencephalography. Orientation-independent (untuned) suppression was estimated from responses to central targets with orthogonal surrounds; the orientation-dependence of suppression was estimated by fitting an exponential function to the increase in suppression as surrounds became more aligned with the center. RESULTS: ISZ exhibited weakened untuned suppression coupled with enhanced orientation-dependence of suppression. The N1 visual evoked potential was associated with the orientation-dependence of suppression, with ISZ and ISZR (but not IBP or IBPR) showing enhanced orientation-dependence of the N1. Collapsed across orientation conditions, the N1 for ISZ lacked asymmetry toward the right hemisphere; this reduction in N1 asymmetry was associated with reduced untuned suppression, real-world perceptual anomalies, and psychotic psychopathology. The overall amplitude of the N1 was reduced in ISZ and IBP. CONCLUSIONS: Key measures of symptomatology for ISZ are associated with reductions in untuned suppression. Increased sensitivity for ISZ to the relative orientation of suppressive surrounds is reflected in the N1 VEP, which is commonly associated with higher-level visual functions such as allocation of spatial attention or scene segmentation.

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Cortical networks exhibit complex stimulus-response patterns that are based on specific recurrent interactions between neurons. For example, the balance between excitatory and inhibitory currents has been identified as a central component of cortical computations. However, it remains unclear how the required synaptic connectivity can emerge in developing circuits where synapses between excitatory and inhibitory neurons are simultaneously plastic. Using theory and modeling, we propose that a wide range of cortical response properties can arise from a single plasticity paradigm that acts simultaneously at all excitatory and inhibitory connections-Hebbian learning that is stabilized by the synapse-type-specific competition for a limited supply of synaptic resources. In plastic recurrent circuits, this competition enables the formation and decorrelation of inhibition-balanced receptive fields. Networks develop an assembly structure with stronger synaptic connections between similarly tuned excitatory and inhibitory neurons and exhibit response normalization and orientation-specific center-surround suppression, reflecting the stimulus statistics during training. These results demonstrate how neurons can self-organize into functional networks and suggest an essential role for synapse-type-specific competitive learning in the development of cortical circuits.

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Surround suppression was initially identified as a phenomenon at the neural level in which stimuli outside the neuron's receptive field alone cannot activate responses but can modulate neural responses to stimuli covered inside the receptive field. Subsequent studies showed that surround suppression is not only a critical property of neurons across species and brain areas but also has been found in visual perceptions. More importantly, surround suppression varies across individuals and shows significant differences between normal controls and patients with certain mental disorders. Here, we combined results from related literature and summarized the findings derived from physiological and psychophysical evidence. We first outline the basic properties of surround suppression in the visual system and perceptions. Then, we mainly summarize the differences in perceptual surround suppression among different human subjects. Our review suggests that there is no consensus regarding whether the strength of perceptual surround suppression could be used as an effective index to distinguish particular populations. Then, we summarized the similar mechanisms for surround suppression and cognitive impairments to further explore the potential clinical applications of surround suppression. A clearer understanding of the mechanisms of surround suppression in neural responses and perceptions is necessary for facilitating its clinical applications.

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BACKGROUND: Visual biomarkers of Parkinson's disease (PD) are attractive as the retina is an outpouching of the brain. Although inner retinal neurodegeneration in PD is well-established this has overlap with other neurodegenerative diseases and thus outer retinal (photoreceptor) measures warrant further investigation. OBJECTIVE: To examine in a cross-sectional study whether clinically implementable measures targeting outer retinal function and structure can differentiate PD from healthy ageing and whether these are sensitive to intraday levodopa (L-DOPA) dosing. METHODS: Centre-surround perceptual contrast suppression, macular visual field sensitivity, colour discrimination, light-adapted electroretinography and optical coherence tomography (OCT) were tested in PD participants (n = 16) and controls (n = 21). Electroretinography and OCT were conducted before and after midday L-DOPA in PD participants, or repeated after ∼2 hours in controls. RESULTS: PD participants had decreased center-surround contrast suppression (p < 0.01), reduced macular visual field sensitivity (p < 0.05), color vision impairment (p < 0.01) photoreceptor dysfunction (a-wave, p < 0.01) and photoreceptor neurodegeneration (outer nuclear layer thinning, p < 0.05), relative to controls. Effect size comparison between inner and outer retinal parameters showed that photoreceptor metrics were similarly robust in differentiating the PD group from age-matched controls as inner retinal changes. Electroretinography and OCT were unaffected by L-DOPA treatment or time. CONCLUSIONS: We show that outer retinal outcomes of photoreceptoral dysfunction (decreased cone function and impaired color vision) and degeneration (i.e., outer nuclear layer thinning) were equivalent to inner retinal metrics at differentiating PD from healthy age-matched adults. These findings suggest outer retinal metrics may serve as useful biomarkers for PD.

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Surround suppression (SS) is a phenomenon whereby a neuron's response to stimuli in its central receptive field (cRF) is suppressed by stimuli extending to its surround receptive field (sRF). Recent evidence show that top-down influence contributed to SS in the primary visual cortex (V1). However, how the top-down influence from different high-level cortical areas affects SS in V1 has not been comparatively observed. The present study applied transcranial direct current stimulation (tDCS) to modulate the neural activity in area 21a (A21a) and area 7 (A7) of cats and examined the changes in the cRF and sRF of V1 neurons. We found that anode-tDCS at A21a reduced V1 neurons' cRF size and increased their response to visual stimuli in cRF, causing an improved SS strength. By contrast, anode-tDCS at A7 increased V1 neurons' sRF size and response to stimuli in cRF, also enhancing the SS. Modeling analysis based on DoG function indicated that the increased SS of V1 neurons after anode-tDCS at A21a could be explained by a center-only mechanism, whereas the improved SS after anode-tDCS at A7 might be mediated through a combined center and surround mechanism. In conclusion, A21a and A7 may affect the SS of V1 neurons through different mechanisms.

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Recent results have shown that males have lower duration thresholds for motion direction discrimination than females. Measuring contrast thresholds, a previous study has shown that males have a greater sensitivity to fine details and fast flickering stimuli than females, and that females have a higher sensitivity to low spatial frequencies modulated at low temporal frequencies. Here, we present the data of a contrast-detection motion discrimination experiment and a reanalysis of four different motion discrimination experiments where we compare duration thresholds for males and females using different spatial frequencies, stimulus sizes, contrasts, and temporal frequencies (in two experiments, motion surround suppression was measured). Results from the main experiment and the reanalysis show that, in general, the association between sex and contrast and duration thresholds for motion discrimination is not significant, with males and females showing similar data patterns. Only the reanalysis of one out of four studies revealed different duration thresholds between males and females paired with a strong effect size supporting previous results in the literature, although motion surround suppression was identical between groups. Importantly, most of our results do not show significant differences between males and females in contrast and duration thresholds, suggesting that the sex variable may not be as relevant as previously claimed when testing visual motion discrimination.

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Anomalies of attentional selection have been repeatedly described in individuals with schizophrenia spectrum disorders. However, a precise analysis of their ability to inhibit irrelevant visual information during attentional selection is not documented. Recent behavioral as well as neurophysiological and computational evidence showed that attentional search among different competing stimuli elicits an area of suppression in the immediate surrounding of the attentional focus. In the present study, the strength and spatial extension of this surround suppression were tested in individuals with schizophrenia and neurotypical controls. Participants were asked to report the orientation of a visual "pop-out" target, which appeared in different positions within a peripheral array of non-target stimuli. In half of the trials, after the target appeared, a probe circle circumscribed a non-target stimulus at various target-to-probe distances; in this case, participants were asked to report the probe orientation instead. Results suggest that, as compared to neurotypical controls, individuals with schizophrenia showed stronger and spatially more extended filtering of visual information in the areas surrounding their attentional focus. This increased filtering of visual information outside the focus of attention might potentially hamper their ability to integrate different elements into coherent percepts and influence higher order behavioral, affective, and cognitive domains.

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The perceived contrast of a central stimulus is supressed when it is embedded in a higher contrast surround, centre-surround suppression of contrast. Local brightness induction effects between the two stimulus regions have been proposed to account for conflicting results when relative grating phases were different. Here, suppression and brightness induction effects are dissociated using a centre-surround arrangement with moving gratings. Four experienced observers were involved in experiments, utilising two-interval forced-choice contrast matching tasks. The stimuli were drifting sinusoidal grating patterns with surrounds (95% contrast) differing in direction of motion and orientation relative to the 40% contrast centre grating. First a 90°-phase-offset same direction surround condition was compared to both same direction (phase aligned) and opposing direction conditions. The reduction in the suppression for the phase-offset condition suggested a reduction in brightness induction influences. Then suppression was examined when surround directions varied and where phase was either fixed or randomised. For small changes in the motion direction between centre and surround (0° to 26.6°) the amount of brightness induction varied sinusoidally with the difference in phase introduced by the direction difference. Finally, the spatial separation between the centre and surround was varied to determine the reduction of suppression and brightness induction with increasing spatial distance. We found both fit an exponential decay function, with surround suppression producing the larger range of influence. Our findings quantify both brightness induction and suppression effects and validate the use of phase randomisation to remove effects of brightness induction when evaluating surround suppression.

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BACKGROUND: Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or "attentional suppressive surround" predicted by the Selective Tuning model of visual attention. However, previously reported effects of feature-based attention on neuronal responses are linear, e.g., feature-similarity gain. Here, we investigated this apparent contradiction by neurophysiological and psychophysical approaches. RESULTS: Responses of motion direction-selective neurons in area MT/MST of monkeys were recorded during a motion task. When attention was allocated to a stimulus moving in the neurons' preferred direction, response tuning curves showed its minimum for directions 60-90° away from the preferred direction, an attentional suppressive surround. This effect was modeled via the interaction of two Gaussian fields representing excitatory narrowly tuned and inhibitory widely tuned inputs into a neuron, with feature-based attention predominantly increasing the gain of inhibitory inputs. We further showed using a motion repulsion paradigm in humans that feature-based attention produces a similar non-linearity on motion discrimination performance. CONCLUSIONS: Our results link the gain modulation of neuronal inputs and tuning curves examined through the feature-similarity gain lens to the attentional impact on neural population responses predicted by the Selective Tuning model, providing a unified framework for the documented effects of feature-based attention on neuronal responses and behavior.

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The input from the two eyes is combined in the brain. In this combination, the relative strength of the input from each eye is determined by the ocular dominance. Recent work has shown that this dominance can be temporarily shifted. Covering one eye with an eye patch for a few hours makes its contribution stronger. It has been proposed that this shift can be enhanced by exercise. Here, we test this hypothesis using a dichoptic surround suppression task, and with exercise performed according to American College of Sport Medicine guidelines. We measured detection thresholds for patches of sinusoidal grating shown to one eye. When an annular mask grating was shown simultaneously to the other eye, thresholds were elevated. The difference in the elevation found in each eye is our measure of relative eye dominance. We made these measurements before and after 120 min of monocular deprivation (with an eye patch). In the control condition, subjects rested during this time. For the exercise condition, 30 min of exercise were performed at the beginning of the patching period. This was followed by 90 min of rest. We find that patching results in a shift in ocular dominance that can be measured using dichoptic surround suppression. However, we find no effect of exercise on the magnitude of this shift. We further performed a meta-analysis on the four studies that have examined the effects of exercise on the dominance shift. Looking across these studies, we find no evidence for such an effect.

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Spatial integration of visual information is an important function in the brain. However, neural computation for spatial integration in the visual cortex remains unclear. In this study, we recorded laminar responses in V1 of awake monkeys driven by visual stimuli with grating patches and annuli of different sizes. We find three important response properties related to spatial integration that are significantly different between input and output layers: neurons in output layers have stronger surround suppression, smaller receptive field (RF), and higher sensitivity to grating annuli partially covering their RFs. These interlaminar differences can be explained by a descriptive model composed of two global divisions (normalization) and a local subtraction. Our results suggest suppressions with cascaded normalizations (CNs) are essential for spatial integration and laminar processing in the visual cortex. Interestingly, the features of spatial integration in convolutional neural networks, especially in lower layers, are different from our findings in V1.

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OBJECTIVE: Vitamins B6 and B12 are involved in metabolic processes that decrease neural excitation and increase inhibition. This double-blind study investigated the effects of supplementation for 1 month with a high-dose of B6 or B12, compared to placebo, on a range of behavioural outcome measures connected to the balance between neural inhibition and excitation. METHODS: 478 young adults were recruited over five linked phases. Self-reported anxiety (N = 265) and depression (N = 146) were assessed at baseline and after supplementation. Several sensory measures acted as assays of inhibitory function and were assessed post-supplementation only; these were surround suppression of visual contrast detection (N = 307), binocular rivalry reversal rate (N = 172), and a battery of tactile sensitivity tests (N = 180). RESULTS: Vitamin B6 supplementation reduced self-reported anxiety and induced a trend towards reduced depression, as well as increased surround suppression of visual contrast detection, but did not reliably influence the other outcome measures. Vitamin B12 supplementation produced trends towards changes in anxiety and visual processing. CONCLUSIONS: Our results suggest that high-dose Vitamin B6 supplementation increases inhibitory GABAergic neural influences, which is consistent with its known role in the synthesis of GABA.

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Here we investigate how the extent of spatial attention affects center-surround interaction in visual motion processing. To do so, we measured motion direction discrimination thresholds in humans using drifting gratings and two attention conditions. Participants were instructed to limit their attention to the central part of the stimulus under the narrow attention condition, and to both central and surround parts under the wide attention condition. We found stronger surround suppression under the wide attention condition. The magnitude of the attention effect increased with the size of the surround when the stimulus had low contrast, but did not change when it had high contrast. Results also showed that attention had a weaker effect when the center and surround gratings drifted in opposite directions. Next, to establish a link between the behavioral results and the neuronal response characteristics, we performed computer simulations using the divisive normalization model. Our simulations showed that using smaller versus larger multiplicative attentional gain and parameters derived from the medial temporal (MT) area of the cortex, the model can successfully predict the observed behavioral results. These findings reveal the critical role of spatial attention on surround suppression and establish a link between neuronal activity and behavior. Further, these results also suggest that the reduced surround suppression found in certain clinical disorders (e.g., schizophrenia and autism spectrum disorder) may be caused by abnormal attention mechanisms.

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Predictive coding is an important candidate theory of self-supervised learning in the brain. Its central idea is that sensory responses result from comparisons between bottom-up inputs and contextual predictions, a process in which rates and synchronization may play distinct roles. We recorded from awake macaque V1 and developed a technique to quantify stimulus predictability for natural images based on self-supervised, generative neural networks. We find that neuronal firing rates were mainly modulated by the contextual predictability of higher-order image features, which correlated strongly with human perceptual similarity judgments. By contrast, V1 gamma (γ)-synchronization increased monotonically with the contextual predictability of low-level image features and emerged exclusively for larger stimuli. Consequently, γ-synchronization was induced by natural images that are highly compressible and low-dimensional. Natural stimuli with low predictability induced prominent, late-onset beta (ß)-synchronization, likely reflecting cortical feedback. Our findings reveal distinct roles of synchronization and firing rates in the predictive coding of natural images.

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Surround modulation has been abundantly studied in several mammalian brain areas, including the primary visual cortex, lateral geniculate nucleus, and superior colliculus (SC), but systematic analysis is lacking in the avian optic tectum (OT, homologous to mammal SC). Here, multi-units were recorded from pigeon (Columba livia) OT, and responses to different sizes of moving, flashed squares, and bars were compared. The statistical results showed that most tectal neurons presented suppressed responses to larger stimuli in both moving and flashed paradigms, and suppression induced by flashed squares was comparable with moving ones when the stimuli center crossed the near classical receptive field (CRF) center, which corresponded to the full surrounding condition. Correspondingly, the suppression grew weaker when the stimuli center moved across the CRF border, equivalent to partially surrounding conditions. Similarly, suppression induced by full surrounding flashed squares was more intense than by partially surrounding flashed bars. These results suggest that inhibitions performed on tectal neurons appear to be full surrounding rather than locally lateral. This study enriches the understanding of surround modulation properties of avian tectum neurons and provides possible hypotheses about the arrangement of inhibitions from other nuclei, both of which are important for clarifying the mechanism of target detection against clutter background performed by avians.

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Cerebral visual impairment (CVI) is associated with a wide range of visual perceptual deficits including global motion processing. However, the underlying neurophysiological basis for these impairments remain poorly understood. We investigated global motion processing abilities in individuals with CVI compared to neurotypical controls using a combined behavioral and multi-modal neuroimaging approach. We found that CVI participants had a significantly higher mean motion coherence threshold (determined using a random dot kinematogram pattern simulating optic flow motion) compared to controls. Using functional magnetic resonance imaging (fMRI), we investigated activation response profiles in functionally defined early (i.e. primary visual cortex; area V1) and higher order (i.e. middle temporal cortex; area hMT+) stages of motion processing. In area V1, responses to increasing motion coherence were similar in both groups. However, in the CVI group, activation in area hMT+ was significantly reduced compared to controls, and consistent with a surround facilitation (rather than suppression) response profile. White matter tract reconstruction obtained from high angular resolution diffusion imaging (HARDI) revealed evidence of increased mean, axial, and radial diffusivities within cortico-cortical (i.e. V1-hMT+), but not thalamo-hMT+ connections. Overall, our results suggest that global motion processing deficits in CVI may be associated with impaired signal integration and segregation mechanisms, as well as white matter integrity at the level of area hMT+.

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Center-surround antagonism, as a ubiquitous feature in visual processing, usually leads to inferior perception for a large stimulus compared to a small one. For example, it is more difficult to judge the motion direction of a large high-contrast pattern than that of a small one. However, this spatial suppression in the motion dimension was only reported for luminance motion, and was not found for chromatic motion. Given that center-surround suppression only occurs for strong visual inputs, we hypothesized that previous failure in finding spatial suppression of chromatic motion might be due to weak chromatic motion being induced with stimuli of limited parameters. In this study, we used phase-shift discrimination and motion-direction discrimination tasks to measure motion spatial suppression induced by stimuli of two spatial frequencies (0.5 and 2 cpd) and two contrasts (low and high). We found that spatial suppression of the chromatic motion was stably observed for stimuli of high spatial frequency (2 cpd) and high contrast and spatial summation occurred for stimuli of low spatial frequency (0.5 cpd). Intriguingly, there was no correlations between the motion spatial suppressions of luminance motion and chromatic motion, implying that the two types of spatial suppression are not originated from the same neural processing. Our findings indicate that spatial suppression also exists for chromatic motion, and the mechanisms underlying the spatial suppression of chromatic motion is different from that of luminance motion.

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Moderate alcohol consumption is considered to enhance the cortical GABA-ergic inhibitory system and it also variously affects visual perception. However, little behavioral evidence indicates changes of visual perception due to V1 modulated by alcohol intoxication. In this study, we investigated this issue by using center-surround tilt illusion (TI) as a probe of V1 inhibitory interactions, by taking into account possible higher-order effects. Participants conducted TI measures under sober, moderate alcohol intoxication, and placebo states. We found alcohol significantly increased repulsive TI effect and weakened orientation discrimination performance, which is consistent with the increase of lateral inhibition between orientation sensitive V1 neurons caused by alcohol intoxication. We also observed no visible changes in the data for global orientation processing but a presence of global attentional modulation. Thus, our results provide psychophysics evidence that alcohol changed V1 processing, which affects visual perception of contextual stimuli.

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PURPOSE: Following reports that an index of visual surround suppression (SI) may serve as a biomarker for an imbalance of cortical excitation and inhibition in different psychiatric and neurological disorders including epilepsy, we evaluated whether SI is associated with seizure susceptibility, seizure spread, and inhibitory effects of antiseizure medication (ASM). METHODS: In this prospective controlled study, we examined SI with a motion discrimination task in people with genetic generalized epilepsy (GGE) and focal epilepsy with and without focal to bilateral tonic-clonic seizures. Cofactors such as GABAergic ASM, attentional-executive functioning, and depression were taken into account. RESULTS: Data of 45 patients were included in the final analysis. Suppression index was not related to epilepsy or seizure type, GABAergic ASM treatment or mood. However, SI correlated with attentional-executive functioning (r = 0.32), which in turn was associated with ASM load (r = -0.38). Repeated task administration (N = 7) proved a high stability over a one-week interval (rtt = 0.89). CONCLUSIONS: Our results do not support the hypothesis that SI is a reliable biomarker for mechanisms related to inhibition of seizure spread or seizure frequency, i.e., it does not seem to reflect inhibitory capacities in epilepsy. Likewise, SI did not differentiate GGE from focal epilepsy, nor was it influenced by ASM load or mode of action. Thus, in epilepsy, no added value of including SI to routine diagnostics can be concluded.

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When observers view a perceptually bistable stimulus, their perception changes stochastically. Various studies have shown across-observer correlations in the percept durations for different bistable stimuli including binocular rivalry stimuli and bistable moving plaids. Previous work on binocular rivalry posits that neural inhibition in the visual hierarchy is a factor involved in the perceptual fluctuations in that paradigm. Here, in order to investigate whether between-observer variability in cortical inhibition underlies correlated percept durations between binocular rivalry and bistable moving plaid perception, we used center-surround suppression as a behavioral measure of cortical inhibition. We recruited 217 participants in a test battery that included bistable perception paradigms as well as a center-surround suppression paradigm. While we were able to successfully replicate the correlations between binocular rivalry and bistable moving plaid perception, we did not find a correlation between center-surround suppression strength and percept durations for any form of bistable perception. Moreover, the results from a mediation analysis indicate that center-surround suppression is not the mediating factor in the correlation between binocular rivalry and bistable moving plaids. These results do not support the idea that cortical inhibition can explain the between-observer correlation in mean percept duration between binocular rivalry and bistable moving plaid perception.