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Sensory perception in autism

Key Points

  • Sensory symptoms have been observed since early reports of autism spectrum conditions but historically were thought to represent secondary consequences of differences in social-cognitive processing.

  • Developmental research suggests that sensory symptoms manifest early in development and contribute unique variance to the diagnostic criteria of autism.

  • Neuroimaging evidence suggests that sensory symptoms originate from differences in low-level processing in sensory-dedicated regions in the autistic brain and offer insight into circuit-level alterations.

  • Although common behavioural paradigms are not yet in place, sensory-processing differences are evident in genetic animal models of the condition and may represent promising translatable biomarkers of autism.

Abstract

Autism is a complex neurodevelopmental condition, and little is known about its neurobiology. Much of autism research has focused on the social, communication and cognitive difficulties associated with the condition. However, the recent revision of the diagnostic criteria for autism has brought another key domain of autistic experience into focus: sensory processing. Here, we review the properties of sensory processing in autism and discuss recent computational and neurobiological insights arising from attention to these behaviours. We argue that sensory traits have important implications for the development of animal and computational models of the condition. Finally, we consider how difficulties in sensory processing may relate to the other domains of behaviour that characterize autism.

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Figure 1: Trade-off in visual perception in autism.
Figure 2: Neuroimaging evidence for low-level origin of visual symptoms in autism.
Figure 3: Sensory symptoms as translational behavioural markers of autism.

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Acknowledgements

The authors thank M. Cohen, A. Spiegel, G. Choi, N. Kanwisher, A. J. Haskins, and M. Sur for comments on sections of this manuscript and helpful discussion.

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C.E.R. researched the article. C.E.R. and S.B.-C. equally contributed to discussions of the content, writing the article and to review and/or editing of the manuscript before submission.

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Correspondence to Caroline E. Robertson.

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The authors declare no competing financial interests.

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How does sensation fit into the history of autism? (PDF 142 kb)

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Glossary

Cognitive empathy

The ability to understand and respond appropriately to others' mental states and emotions (unlike affective empathy, the ability to respond with an appropriate emotion to others' mental states or feelings).

Joint attention

An early-developing cornerstone of social cognition: the child's ability to use another person's gestures and gaze to direct his or her attention to objects or events in the environment.

Broader autism phenotype

Mild autistic traits (in both social and sensory processing domains) often observed in relatives of individuals with autism in multiplex families.

Multiplex families

Families in which multiple individuals have an autism diagnosis; family members may carry shared genetic risk factors.

Crowding

The breakdown of visual recognition of peripheral stimuli in cluttered visual environments.

Population receptive fields

A model-driven quantitative measurement of the average size and shape of receptive fields contained within a single functional MRI voxel.

Cross-activation

Activation of one sensory-dedicated cortical region by sensory stimulation of another modality.

Synaesthesia

The cross-activation of one sensory modality by stimulation of another.

Cortical minicolumns

Basic anatomical units of the neocortex, in which neurons are arranged in vertical columns across cortical layers of the brain.

Binocular rivalry

A visual phenomenon in which two images, presented simultaneously to the two eyes, alternate in perception as neuronal pools coding for each eye's percept compete for perceptual dominance.

Spatial suppression

A visual phenomenon in which motion discrimination is counter-intuitively attenuated at larger, instead of smaller, stimulus sizes, probably owing to suppressive interactions (centre–surround antagonism or inhibitory feedback).

Critical period

A developmental period during which a neural system (such as vision) is particularly plastic and sensitive to environmental influence.

Divisive normalization

A canonical neural computation in which the activity of a neuron is divided by the total activity of neighbouring neurons to reflect context-dependent responses.

Pre-pulse inhibition

A sensory phenomenon in which the behavioural response to a strong sensory stimulus is dampened by a weak preceding stimulus, probably through feedforward inhibition.

McGurk effect

A perceptual illusion in which a sound (for example, of the syllable /ba/) paired with a visual signal (a mouth pronouncing /ga/) produces a third percept (voice and mouth /da/).

Pragmatics

The ability to use the social context of an utterance to inform and communicate meaning.

Neural motifs

Stereotyped, local neural circuits that are found in multiple regions of the brain and participate in common canonical computations (such as habituation, response normalization or biased competition).

Bayesian perceptual inference

A model of perception in which prior knowledge about a stimulus is combined with noisy, stimulus-evoked sensory signals to infer the percept and generate prediction errors.

Ambiguity resolution

The ability to impose meaning on ambiguous sensory information. Two or more interpretations may be equally viable (as in bistable visual phenomena, such as in binocular rivalry) or can be disambiguated using contextual information.

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Robertson, C., Baron-Cohen, S. Sensory perception in autism. Nat Rev Neurosci 18, 671–684 (2017). https://doi.org/10.1038/nrn.2017.112

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