Abstract
Progress in our understanding of autism spectrum disorder (ASD) has recently been sought by characterising how systematic differences in canonical neural computations employed across the sensory cortex might contribute to clinical symptoms in diverse sensory, cognitive, and social domains. A key proposal is that ASD is characterised by reduced divisive normalisation of sensory responses. This provides a bridge between genetic and molecular evidence for an increased ratio of cortical excitation to inhibition in ASD and the functional characteristics of sensory coding that are relevant for understanding perception and behaviour. Here we tested this hypothesis in the context of gaze processing (i.e., the perception of other people's direction of gaze), a domain with direct relevance to the core diagnostic features of ASD. We show that reduced divisive normalisation in gaze processing is associated with specific predictions regarding the psychophysical effects of sensory adaptation to gaze direction, and test these predictions in adults with ASD. We report compelling evidence that both divisive normalisation and sensory adaptation occur robustly in adults with ASD in the context of gaze processing. These results have important theoretical implications for defining the types of divisive computations that are likely to be intact or compromised in this condition (e.g., relating to local vs distal control of cortical gain). These results are also a strong testament to the typical sensory coding of gaze direction in ASD, despite the atypical responses to others' gaze that are a hallmark feature of this diagnosis.
Highlights
Autism spectrum disorder (ASD) is a heterogeneous developmental condition, characterised by differences in social interaction, a strong preference for routine, repetitive motor behaviours, and sensory sensitivities (American Psychiatric Association, 2013; Lai, Lombardo, & Baron-Cohen, 2014)
Our results indicated that the effects of sensory adaptation were explained well by a model in which perceived gaze direction was coded in terms of the relative activation across three sensory channels tuned broadly to leftwards gaze, direct gaze, and rightwards gaze, and in which the encoded gaze direction was normalised to the summed activation across these sensory channels
The data that we report here provide a clear picture of there being both typical normalisation and typical adaptation of sensory responses in adults with autism spectrum disorder (ASD), in the context of gaze processing
Summary
Autism spectrum disorder (ASD) is a heterogeneous developmental condition, characterised by differences in social interaction, a strong preference for routine, repetitive motor behaviours, and sensory sensitivities (American Psychiatric Association, 2013; Lai, Lombardo, & Baron-Cohen, 2014). A key proposal is that symptoms in ASD, across sensory, cognitive, and social domains, reflect a widespread reduction of divisive normalisation in neural processing (Rosenberg et al, 2015) This hypothesis is attractive in its potential to link our expanding knowledge of the complex biological underpinnings of this condition to functional characteristics of sensory coding, and thereby perception and behaviour. We find compelling evidence that the adaptive coding of others' gaze direction occurs as robustly in adults with ASD as in NT controls, including in the divisive normalisation of sensory responses These results further our understanding of how information about others' gaze is processed in ASD, and help to adjudicate between recent computational accounts of this condition that emphasise problems in local versus distal gain control in sensory function (Lawson, Friston, & Rees, 2015)
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