Signs of enhanced formation of gist memory in children with autism spectrum disorder - a study of memory functions of sleep.
Autism Spectrum Disorder
/ physiopathology
Child
Cross-Over Studies
Emotions
/ physiology
Humans
Male
Memory Consolidation
/ physiology
Mental Recall
/ physiology
Pattern Recognition, Visual
/ physiology
Polysomnography
Recognition, Psychology
/ physiology
Retention, Psychology
/ physiology
Sleep
/ physiology
Autism spectrum disorder
Deese-Roediger-McDermott
emotional memory
gist abstraction
memory consolidation
sleep
Journal
Journal of child psychology and psychiatry, and allied disciplines
ISSN: 1469-7610
Titre abrégé: J Child Psychol Psychiatry
Pays: England
ID NLM: 0375361
Informations de publication
Date de publication:
08 2019
08 2019
Historique:
accepted:
20
02
2019
pubmed:
26
3
2019
medline:
12
9
2020
entrez:
26
3
2019
Statut:
ppublish
Résumé
Autism spectrum disorder (ASD) is characterized by impaired cognitive and social skills, including emotional dysregulation, and symptoms have been suspected to partly arise from impaired formation of memory representations regulating these behaviours. Sleep, which is subjectively impaired in ASD, is critical for forming long-term memories and abstracted gist-based representations. We expected a generally reduced memory benefit from sleep in children with ASD, and a diminished enhancement of gist representations, in particular. We compared effects of sleep on memory consolidation between boys (9-12 years) with ASD (n = 21) and typically developing (TD, n = 20) boys, matched for age and IQ, in a within-subjects crossover design. We employed an emotional picture recognition task and the Deese-Roediger-McDermott (DRM) word list task for assessing gist memory formation in the emotional and nonemotional domain, respectively. Learning took place before retention intervals of nocturnal sleep and daytime wakefulness, and retrieval was tested afterwards. Surprisingly, on the DRM task, children with ASD showed an enhanced sleep-dependent formation of gist-based memory (i.e. more recall of 'critical lure words' after sleep compared to wakefulness) than TD children, with this effect occurring on top of a diminished veridical word memory. On the picture recognition task, children with ASD also showed a stronger emotional enhancement in memory (i.e. relatively better memory for negative than neutral pictures) than TD children, with this enhancement occurring independent of sleep. Sleep polysomnography was remarkably comparable between groups. Children with ASD show well-preserved sleep-dependent memory consolidation. Enhanced gist memory formation in these children might reflect a compensatory response for impairments at earlier stages of memory processing, that is during encoding.
Sections du résumé
BACKGROUND
Autism spectrum disorder (ASD) is characterized by impaired cognitive and social skills, including emotional dysregulation, and symptoms have been suspected to partly arise from impaired formation of memory representations regulating these behaviours. Sleep, which is subjectively impaired in ASD, is critical for forming long-term memories and abstracted gist-based representations. We expected a generally reduced memory benefit from sleep in children with ASD, and a diminished enhancement of gist representations, in particular.
METHODS
We compared effects of sleep on memory consolidation between boys (9-12 years) with ASD (n = 21) and typically developing (TD, n = 20) boys, matched for age and IQ, in a within-subjects crossover design. We employed an emotional picture recognition task and the Deese-Roediger-McDermott (DRM) word list task for assessing gist memory formation in the emotional and nonemotional domain, respectively. Learning took place before retention intervals of nocturnal sleep and daytime wakefulness, and retrieval was tested afterwards.
RESULTS
Surprisingly, on the DRM task, children with ASD showed an enhanced sleep-dependent formation of gist-based memory (i.e. more recall of 'critical lure words' after sleep compared to wakefulness) than TD children, with this effect occurring on top of a diminished veridical word memory. On the picture recognition task, children with ASD also showed a stronger emotional enhancement in memory (i.e. relatively better memory for negative than neutral pictures) than TD children, with this enhancement occurring independent of sleep. Sleep polysomnography was remarkably comparable between groups.
CONCLUSIONS
Children with ASD show well-preserved sleep-dependent memory consolidation. Enhanced gist memory formation in these children might reflect a compensatory response for impairments at earlier stages of memory processing, that is during encoding.
Identifiants
pubmed: 30908649
doi: 10.1111/jcpp.13048
pmc: PMC6850042
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
907-916Informations de copyright
© 2019 The Authors. Journal of Child Psychology and Psychiatry published by John Wiley & Sons Ltd on behalf of Association for Child and Adolescent Mental Health.
Références
Neuron. 2015 Oct 7;88(1):20-32
pubmed: 26447570
J Clin Exp Neuropsychol. 2007 Aug;29(6):610-6
pubmed: 17691033
Sci Rep. 2017 Feb 17;7:42950
pubmed: 28211489
Psychol Sci. 2006 Oct;17(10):891-8
pubmed: 17100790
Sleep. 2014 Sep 01;37(9):1501-12
pubmed: 25142558
J Exp Psychol Gen. 2007 May;136(2):169-83
pubmed: 17500644
J Neurosci. 2002 Dec 15;22(24):10941-7
pubmed: 12486189
Res Dev Disabil. 2012 Sep-Oct;33(5):1408-17
pubmed: 22522199
Neurobiol Learn Mem. 2017 Jan;137:101-106
pubmed: 27913294
Int J Psychophysiol. 2015 Jul;97(1):58-65
pubmed: 25958790
Front Psychol. 2015 Mar 04;6:182
pubmed: 25788890
Emotion. 2015 Apr;15(2):176-86
pubmed: 25706830
Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8734-7
pubmed: 10900024
Trends Cogn Sci. 2011 Aug;15(8):343-51
pubmed: 21764357
Autism Res. 2008 Apr;1(2):91-6
pubmed: 19360655
J Sleep Res. 2014 Jun;23(3):302-8
pubmed: 24329882
Nat Rev Neurosci. 2010 Feb;11(2):114-26
pubmed: 20046194
J Exp Child Psychol. 2009 Sep;104(1):132-9
pubmed: 19251274
Memory. 2002 Jan;10(1):1-6
pubmed: 11747571
Neurobiol Learn Mem. 2017 Nov;145:181-189
pubmed: 29030296
J Child Psychol Psychiatry. 2015 Aug;56(8):893-902
pubmed: 25418509
J Child Psychol Psychiatry. 2015 Aug;56(8):903-13
pubmed: 25442191
Behav Cogn Neurosci Rev. 2002 Dec;1(4):251-63
pubmed: 17712983
Dev Sci. 2014 Nov;17(6):858-71
pubmed: 24636285
Biol Psychiatry. 2006 Oct 1;60(7):788-90
pubmed: 16806090
Sleep Med Rev. 2009 Dec;13(6):403-11
pubmed: 19398354
Behav Brain Res. 2010 Apr 2;208(2):425-9
pubmed: 20035789
Sleep. 2015 Dec 01;38(12):1955-63
pubmed: 26194566
Dev Psychol. 2016 Dec;52(12):2118-2129
pubmed: 27893249
Neuropsychologia. 2008;46(9):2336-43
pubmed: 18440037
J Autism Dev Disord. 2006 Jan;36(1):5-25
pubmed: 16450045
Sleep. 2008 Feb;31(2):197-203
pubmed: 18274266
Neuropsychologia. 2018 Aug;117:84-91
pubmed: 29782873
J Behav Ther Exp Psychiatry. 1994 Mar;25(1):49-59
pubmed: 7962581
Neurobiol Learn Mem. 2009 Oct;92(3):327-34
pubmed: 19348959
Curr Biol. 2017 Aug 7;27(15):2374-2380.e3
pubmed: 28756948
Psychol Sci. 2007 Mar;18(3):208-11
pubmed: 17444912
J Autism Dev Disord. 2009 Jul;39(7):1031-8
pubmed: 19296212
Nat Commun. 2015 Jan 29;6:6004
pubmed: 25633407
Neuropsychologia. 2007 May 15;45(9):2125-34
pubmed: 17321555
J Autism Dev Disord. 2017 Jan;47(1):68-79
pubmed: 27838805
Autism Res. 2017 Sep;10(9):1523-1532
pubmed: 28448695
J Adolesc. 2018 Jul;66:55-70
pubmed: 29783103
Arch Pediatr Adolesc Med. 2010 Nov;164(11):1032-7
pubmed: 21041596
Psychol Bull. 2012 May;138(3):458-96
pubmed: 22409507
J Autism Dev Disord. 2010 Mar;40(3):358-70
pubmed: 19885725
Psychol Sci. 2008 Aug;19(8):781-8
pubmed: 18816285
Neurology. 2018 Jul 10;91(2):e112-e122
pubmed: 29875224
Sleep. 2015 Jun 01;38(6):951-9
pubmed: 25325488
Nature. 2004 Jan 22;427(6972):352-5
pubmed: 14737168
J Exp Psychol. 1959 Jul;58(1):17-22
pubmed: 13664879
Nat Neurosci. 2013 Apr;16(4):391-3
pubmed: 23434910
J Autism Dev Disord. 2014 Sep;44(9):2087-95
pubmed: 24777286