Abstract
Excitation/Inhibition (E/I) imbalance in neural networks is now considered among the core neural underpinnings of autism psychopathology. In motion perception at least two phenomena critically depend on E/I balance in visual cortex: spatial suppression (SS), and spatial facilitation (SF) corresponding to impoverished or improved motion perception with increasing stimuli size, respectively. While SS is dominant at high contrast, SF is evident for low contrast stimuli, due to the prevalence of inhibitory contextual modulations in the former, and excitatory ones in the latter case. Only one previous study (Foss-Feig et al., 2013) investigated SS and SF in Autism Spectrum Disorder (ASD). Our study aimed to replicate previous findings, and to explore the putative contribution of deficient inhibitory influences into an enhanced SF index in ASD—a cornerstone for interpretation proposed by Foss-Feig et al. (2013). The SS and SF were examined in 40 boys with ASD, broad spectrum of intellectual abilities (63 < IQ < 127) and 44 typically developing (TD) boys, aged 6–15 years. The stimuli of small (1°) and large (12°) radius were presented under high (100%) and low (1%) contrast conditions. Social Responsiveness Scale and Sensory Profile Questionnaire were used to assess the autism severity and sensory processing abnormalities. We found that the SS index was atypically reduced, while SF index abnormally enhanced in children with ASD. The presence of abnormally enhanced SF in children with ASD was the only consistent finding between our study and that of Foss-Feig et al. While the SS and SF indexes were strongly interrelated in TD participants, this correlation was absent in their peers with ASD. In addition, the SF index but not the SS index correlated with the severity of autism and the poor registration abilities. The pattern of results is partially consistent with the idea of hypofunctional inhibitory transmission in visual areas in ASD. Nonetheless, the absence of correlation between SF and SS indexes paired with a strong direct link between abnormally enhanced SF and autism symptoms in our ASD sample emphasizes the role of the enhanced excitatory influences by themselves in the observed abnormalities in low-level visual phenomena found in ASD.
Highlights
Autism Spectrum Disorder (ASD) is a neurodevelopmental disorder diagnosed by behavioral impairments in three functional domains: social relatedness, social communication and stereotyped behavior with unusually narrow interests (American Psychiatric Association, 2013)
The authors hypothesized that de-coupling between binocular rivalry and GABA concentration in ASD may arise from perturbations in key components of the GABAergic pathway in primary visual cortex
Considering the wide age range of our participants (6–15 years of age), we checked for a possible age-dependence of the motion direction discrimination thresholds and the SS and the spatial facilitation (SF) indexes in the typically developing (TD) and the ASD groups
Summary
ASD is a neurodevelopmental disorder diagnosed by behavioral impairments in three functional domains: social relatedness, social communication and stereotyped behavior with unusually narrow interests (American Psychiatric Association, 2013). In neurotypical people GABA concentration in visual cortex correlated with the psychophysical measure of the dynamics of binocular rivalry - duration during which one of the two competing images presented to each eye was fully suppressed from visual awareness (Robertson et al, 2016). Most importantly, this relationship was completely absent in ASD individuals. The E/I imbalance in ASD may be present in social, emotional, and language systems and in purely sensory areas of the brain and might play an important role in different aspects of visual perception, for example, through disturbed divisive normalization of neural population activity (Rosenberg et al, 2015). Divisive normalization is the process by which neural responses are scaled according to the total amount of neural activity in the respective neural network and acts to optimize visual processing under changing stimulation conditions (Isaacson and Scanziani, 2011)
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