Atypicalities in sleep and semantic consolidation in autism

Fay E Fletcher; Victoria Knowland; Sarah Walker; M Gareth Gaskell; Courtenay Norbury; Lisa M Henderson

doi:10.1111/desc.12906

Atypicalities in sleep and semantic consolidation in autism

Fay E Fletcher, Victoria Knowland, Sarah Walker, M Gareth Gaskell, Courtenay Norbury, Lisa M Henderson

Psychology

Research output: Contribution to journal › Article › peer-review

Abstract

Sleep is known to support the neocortical consolidation of declarative memory, including the acquisition of new language. Autism spectrum disorder (ASD) is often characterised by both sleep and language learning difficulties, but few studies have explored a potential connection between the two. Here, 54 children with and without ASD (matched on age, nonverbal ability and vocabulary) were taught nine rare animal names (e.g., pipa). Memory was assessed via definitions, naming and speeded semantic decision tasks immediately after learning (pre-sleep), the next day (post-sleep, with a night of polysomnography between pre- and post-sleep tests) and roughly one month later (follow-up). Both groups showed comparable performance at pre-test and similar levels of overnight change on all tasks; but at follow-up children with ASD showed significantly greater forgetting of the unique features of the new animals (e.g., pipa is a flat frog). Children with ASD had significantly lower central non-rapid-eye-movement (NREM) sigma power. Associations between spindle properties and overnight changes in speeded semantic decisions differed by group. For the TD group, spindle duration predicted overnight changes in responses to novel animals but not familiar animals, reinforcing a role for sleep in the stabilisation of new semantic knowledge. For the ASD group, sigma power and spindle duration were associated with improvements in responses to novel and particularly familiar animals, perhaps reflecting more general sleep associated improvements in task performance. Plausibly, microstructural sleep atypicalities in children with ASD and differences in how information is prioritised for consolidation may lead to cumulative consolidation difficulties, compromising the quality of newly formed semantic representations in long-term memory.

Original language	English
Article number	e12906
Journal	Developmental Science
Early online date	30 Sept 2019
DOIs	https://doi.org/10.1111/desc.12906
Publication status	E-pub ahead of print - 30 Sept 2019

Bibliographical note

© 2019 John Wiley & Sons Ltd. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.

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10.1111/desc.12906

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© 2019 John Wiley & Sons Ltd. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.
Accepted author manuscript, 218 KBLicence: Unspecified

Cite this

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title = "Atypicalities in sleep and semantic consolidation in autism",

abstract = "Sleep is known to support the neocortical consolidation of declarative memory, including the acquisition of new language. Autism spectrum disorder (ASD) is often characterised by both sleep and language learning difficulties, but few studies have explored a potential connection between the two. Here, 54 children with and without ASD (matched on age, nonverbal ability and vocabulary) were taught nine rare animal names (e.g., pipa). Memory was assessed via definitions, naming and speeded semantic decision tasks immediately after learning (pre-sleep), the next day (post-sleep, with a night of polysomnography between pre- and post-sleep tests) and roughly one month later (follow-up). Both groups showed comparable performance at pre-test and similar levels of overnight change on all tasks; but at follow-up children with ASD showed significantly greater forgetting of the unique features of the new animals (e.g., pipa is a flat frog). Children with ASD had significantly lower central non-rapid-eye-movement (NREM) sigma power. Associations between spindle properties and overnight changes in speeded semantic decisions differed by group. For the TD group, spindle duration predicted overnight changes in responses to novel animals but not familiar animals, reinforcing a role for sleep in the stabilisation of new semantic knowledge. For the ASD group, sigma power and spindle duration were associated with improvements in responses to novel and particularly familiar animals, perhaps reflecting more general sleep associated improvements in task performance. Plausibly, microstructural sleep atypicalities in children with ASD and differences in how information is prioritised for consolidation may lead to cumulative consolidation difficulties, compromising the quality of newly formed semantic representations in long-term memory.",

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