Relationship between sensory characteristics and cortical thickness/volume in autism spectrum disorders.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
06 12 2021
06 12 2021
Historique:
received:
25
07
2021
accepted:
24
11
2021
revised:
17
11
2021
entrez:
7
12
2021
pubmed:
8
12
2021
medline:
1
2
2022
Statut:
epublish
Résumé
Individuals with autism spectrum disorders (ASDs) exhibit atypical sensory characteristics, impaired social skills, deficits in verbal and nonverbal communication, and restricted and repetitive behaviors. The relationship between sensory characteristics and brain morphological changes in ASD remains unclear. In this study, we investigated the association between brain morphological changes and sensory characteristics in individuals with ASD using brain image analysis and a sensory profile test. Forty-three adults with ASD and 84 adults with typical development underwent brain image analysis using FreeSurfer. The brain cortex was divided into 64 regions, and the cortical thickness and volume of the limbic system were calculated. The sensory characteristics of the participants were evaluated using the Adolescent/Adult Sensory Profile (AASP). Correlation analysis was performed for cortical thickness, limbic area volume, and AASP scores. In the ASD group, there was a significant positive correlation between visual sensory sensitivity scores and the right lingual cortical thickness (r = 0.500). There were also significant negative correlations between visual sensation avoiding scores and the right lateral orbitofrontal cortical thickness (r = -0.513), taste/smell sensation avoiding scores and the right hippocampal volume (r = -0.510), and taste/smell sensation avoiding scores and the left hippocampal volume (r = -0.540). The study identified associations among the lingual cortical thickness, lateral orbitofrontal cortical thickness, and hippocampal volume and sensory characteristics. These findings suggest that brain morphological changes may trigger sensory symptoms in adults with ASD.
Identifiants
pubmed: 34873147
doi: 10.1038/s41398-021-01743-7
pii: 10.1038/s41398-021-01743-7
pmc: PMC8648722
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
616Informations de copyright
© 2021. The Author(s).
Références
American Psychiatric Association. DSM-5 Diagnostic Classification. In: Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association, 2013 https://doi.org/10.1176/appi.books.9780890425596.x00diagnosticclassification .
Leekam SR, Nieto C, Libby SJ, Wing L, Gould J. Describing the sensory abnormalities of children and adults with autism. J Autism Dev Disord. 2007;37:894–910.
pubmed: 17016677
doi: 10.1007/s10803-006-0218-7
Suarez MA. Sensory processing in children with autism spectrum disorders and impact on functioning. Pediatr Clin North Am. 2012;59:203–14.
pubmed: 22284803
doi: 10.1016/j.pcl.2011.10.012
Howe FEJ, Stagg SD. How sensory experiences affect adolescents with an autistic spectrum condition within the classroom. J Autism Dev Disord. 2016;46:1656–68.
pubmed: 26791372
pmcid: 4826419
doi: 10.1007/s10803-015-2693-1
Baranek GT, David FJ, Poe MD, Stone WL, Watson LR. Sensory experiences questionnaire: discriminating sensory features in young children with autism, developmental delays, and typical development. J Child Psychol Psychiatry Allied Discip. 2006;47:591–601.
doi: 10.1111/j.1469-7610.2005.01546.x
Catana Brown, Winnie Dunn. The adolescent/adult sensory profile: user’s mannual. The Psychological Corporation: San Antonio, TX, 2002.
Jao Keehn RJ, Sanchez SS, Stewart CR, Zhao W, Grenesko-Stevens EL, Keehn B, et al. Impaired downregulation of visual cortex during auditory processing is associated with autism symptomatology in children and adolescents with autism spectrum disorder. Autism Res. 2017;10:130–43.
pubmed: 27205875
doi: 10.1002/aur.1636
Kuiper MWM, Verhoeven EWM, Geurts HM. Stop Making Noise! Auditory sensitivity in adults with an autism spectrum disorder diagnosis: physiological habituation and subjective detection thresholds. J Autism Dev Disord. 2019;49:2116–28.
pubmed: 30680585
pmcid: 6483953
doi: 10.1007/s10803-019-03890-9
Fukuyama H, Kumagaya SI, Asada K, Ayaya S, Kato M. Autonomic versus perceptual accounts for tactile hypersensitivity in autism spectrum disorder. Sci Rep. 2017;7:1–12.
Donaldson CK, Stauder JEA, Donkers FCL. Increased sensory processing atypicalities in parents of multiplex ASD families versus typically developing and simplex ASD families. J Autism Dev Disord. 2017;47:535–48.
pubmed: 27538965
doi: 10.1007/s10803-016-2888-0
Wigham S, Rodgers J, South M, McConachie H, Freeston M. The interplay between sensory processing abnormalities, intolerance of uncertainty, anxiety and restricted and repetitive behaviours in autism spectrum disorder. J Autism Dev Disord. 2015;45:943–52.
pubmed: 25261248
doi: 10.1007/s10803-014-2248-x
Dunlop WA, Enticott PG, Rajan R. Speech discrimination difficulties in high-functioning autism spectrum disorder are likely independent of auditory hypersensitivity. Front Hum Neurosci. 2016;10:12.
doi: 10.3389/fnhum.2016.00401
Foss-Feig JH, Heacock JL, Cascio CJ. Tactile responsiveness patterns and their association with core features in autism spectrum disorders. Res Autism Spectr Disord. 2012;6:337–44.
pubmed: 22059092
pmcid: 3207504
doi: 10.1016/j.rasd.2011.06.007
Simmons DR, Robertson AE, McKay LS, Toal E, McAleer P, Pollick FE. Vision in autism spectrum disorders. Vis Res. 2009;49:2705–39.
pubmed: 19682485
doi: 10.1016/j.visres.2009.08.005
Bennetto L, Kuschner ES, Hyman SL. Olfaction and taste processing in autism. Biol Psychiatry. 2007;62:1015–21.
pubmed: 17572391
pmcid: 2063511
doi: 10.1016/j.biopsych.2007.04.019
Hilton CL, Harper JD, Kueker RH, Lang AR, Abbacchi AM, Todorov A, et al. Sensory responsiveness as a predictor of social severity in children with high functioning autism spectrum disorders. J Autism Dev Disord. 2010;40:937–45.
pubmed: 20108030
doi: 10.1007/s10803-010-0944-8
Hilton CL, Harper JD, Kueker RH, Lang AR, Abbacchi AM, Todorov A, et al. Sensory responsiveness as a predictor of social severity in children with high functioning autism spectrum disorders. J Autism Dev Disord. 2010;40:937–45.
pubmed: 20108030
doi: 10.1007/s10803-010-0944-8
Bonny JM, Sinding C, Thomas-Danguin T Functional MRI and Sensory Perception of Food. In: Modern Magnetic Resonance. Springer International Publishing, 2017, pp 1–20.
Yoshimura S, Sato W, Kochiyama T, Uono S, Sawada R, Kubota Y, et al. Gray matter volumes of early sensory regions are associated with individual differences in sensory processing. Hum Brain Mapp. 2017;38:6206–17.
pubmed: 28940867
pmcid: 6867006
doi: 10.1002/hbm.23822
Green SA, Hernandez L, Tottenham N, Krasileva K, Bookheimer SY, Dapretto M. Neurobiology of sensory overresponsivity in youth with autism spectrum disorders. JAMA Psychiatry. 2015;72:778–86.
pubmed: 26061819
pmcid: 4861140
doi: 10.1001/jamapsychiatry.2015.0737
Doyle-Thomas KAR, Duerden EG, Taylor MJ, Lerch JP, Soorya LV, Wang AT, et al. Effects of age and symptomatology on cortical thickness in autism spectrum disorders. Res Autism Spectr Disord. 2013;7:141–50.
pubmed: 23678367
pmcid: 3652338
doi: 10.1016/j.rasd.2012.08.004
Wallace GL, Eisenberg IW, Robustelli B, Dankner N, Kenworthy L, Giedd JN, et al. Longitudinal cortical development during adolescence and young adulthood in autism spectrum disorder: Increased cortical thinning but comparable surface area changes. J Am Acad Child Adolesc Psychiatry. 2015;54:464–9.
pubmed: 26004661
pmcid: 4540060
doi: 10.1016/j.jaac.2015.03.007
Owen JP, Marco EJ, Desai S, Fourie E, Harris J, Hill SS, et al. Abnormal white matter microstructure in children with sensory processing disorders. NeuroImage Clin. 2013;2:844–53.
pubmed: 24179836
pmcid: 3778265
doi: 10.1016/j.nicl.2013.06.009
Fischl B. FreeSurfer. Neuroimage. 2012;62:774–81.
pubmed: 22248573
doi: 10.1016/j.neuroimage.2012.01.021
Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–55.
pubmed: 11832223
doi: 10.1016/S0896-6273(02)00569-X
Fischl B, Salat DH, Van Der Kouwe AJW, Makris N, Ségonne F, Quinn BT, et al. Sequence-independent segmentation of magnetic resonance images. Neuroimage. 2004;23:69–84.
doi: 10.1016/j.neuroimage.2004.07.016
Jung M, Tu Y, Lang CA, Ortiz A, Park J, Jorgenson K, et al. Decreased structural connectivity and resting-state brain activity in the lateral occipital cortex is associated with social communication deficits in boys with autism spectrum disorder. Neuroimage. 2019;190:205–12.
pubmed: 28927730
doi: 10.1016/j.neuroimage.2017.09.031
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80.
pubmed: 16530430
doi: 10.1016/j.neuroimage.2006.01.021
Lowry R Significance of the difference between two correlation coefficients. Vassarstats. net. 2001; http://vassarstats.net/rdiff.html .
Robertson CE, Baron-Cohen S. Sensory perception in autism. Nat Rev Neurosci 2017;18:671–84.
pubmed: 28951611
doi: 10.1038/nrn.2017.112
Williams ZJ, Abdelmessih PG, Key AP, Woynaroski TG. Cortical auditory processing of simple stimuli is altered in autism: a meta-analysis of auditory evoked responses. Biol Psychiatry Cogn Neurosci Neuroimaging. 2021;6:767–81.
pubmed: 33229245
Beker S, Foxe JJ, Molholm S. Ripe for solution: Delayed development of multisensory processing in autism and its remediation. Neurosci Biobehav Rev. 2018;84:182–92.
pubmed: 29162518
doi: 10.1016/j.neubiorev.2017.11.008
Case-Smith J, Weaver LL, Fristad MA. A systematic review of sensory processing interventions for children with autism spectrum disorders. Autism. 2015;19:133–48.
pubmed: 24477447
doi: 10.1177/1362361313517762
Thye MD, Bednarz HM, Herringshaw AJ, Sartin EB, Kana RK. The impact of atypical sensory processing on social impairments in autism spectrum disorder. Dev Cogn Neurosci 2018;29:151–67.
pubmed: 28545994
doi: 10.1016/j.dcn.2017.04.010
Hardan AY, Libove RA, Keshavan MS, et al. A preliminary longitudinal MRI study of brain volume and cortical thickness in autism. Biol Psychiatry 2009; i:320–6.
Zielinski BA, Prigge MBD, Nielsen JA, Froehlich AL, Abildskov TJ, Anderson JS, et al. Longitudinal changes in cortical thickness in autism and typical development. Brain. 2014;137:1799–812.
pubmed: 24755274
pmcid: 4032101
doi: 10.1093/brain/awu083
Turnbull A, Garfinkel SN, Ho NSP, Critchley HD, Bernhardt BC, Jefferies E, et al. Word up – Experiential and neurocognitive evidence for associations between autistic symptomology and a preference for thinking in the form of words. Cortex. 2020;128:88–106.
pubmed: 32325277
doi: 10.1016/j.cortex.2020.02.019
Amaral DG, Schumann CM, Nordahl CW. Neuroanatomy of autism. Trends Neurosci. 2008;31:137–45.
pubmed: 18258309
doi: 10.1016/j.tins.2007.12.005
Liu X, Bautista J, Liu E, Zikopoulos B. Imbalance of laminar-specific excitatory and inhibitory circuits of the orbitofrontal cortex in autism. Mol Autism. 2020;11:1–19.
doi: 10.1186/s13229-020-00390-x
Hardan AY, Girgis RR, Lacerda ALT, Yorbik O, Kilpatrick M, Keshavan MS, et al. Magnetic resonance imaging study of the orbitofrontal cortex in autism. J Child Neurol. 2006;21:866–71.
pubmed: 17005103
doi: 10.1177/08830738060210100701
Van Rooij D, Anagnostou E, Arango C, Auzias G, Behrmann M, Busatto GF, et al. Cortical and subcortical brain morphometry differences between patients with autism spectrum disorder and healthy individuals across the lifespan: results from the ENIGMA ASD working group. Am J Psychiatry. 2018;175:359–69.
pubmed: 29145754
doi: 10.1176/appi.ajp.2017.17010100
Ishitobi M, Kosaka H, Omori M, Matsumura Y, Munesue T, Mizukami K, et al. Differential amygdala response to lower face in patients with autistic spectrum disorders: An fMRI study. Res Autism Spectr Disord. 2011;5:910–9.
doi: 10.1016/j.rasd.2010.10.005
Golarai G, Grill-Spector K, Reiss AL. Autism and the development of face processing. Clin Neurosci Res. 2006;6:145–60.
pubmed: 18176635
pmcid: 2174902
doi: 10.1016/j.cnr.2006.08.001
Sharvit G, Lin E, Vuilleumier P, Corradi-Dell’Acqua C. Does inappropriate behavior hurt or stink? The interplay between neural representations of somatic experiences and moral decisions. Sci Adv. 2020;6:eaat4390.
pubmed: 33067240
pmcid: 7567598
doi: 10.1126/sciadv.aat4390
Marigliano V, Gualdi G, Servello A, Marigliano B, Volpe LD, Fioretti A, et al. Olfactory deficit and hippocampal volume loss for early diagnosis of Alzheimer disease: A pilot study. Alzheimer Dis Assoc Disord. 2014;28:194–7.
pubmed: 23314063
doi: 10.1097/WAD.0b013e31827bdb9f
Smitka M, Puschmann S, Buschhueter D, Gerber JC, Witt M, Honeycutt N, et al. Is there a correlation between hippocampus and amygdala volume and olfactory function in healthy subjects? Neuroimage. 2012;59:1052–7.
pubmed: 21967725
doi: 10.1016/j.neuroimage.2011.09.024
Groen W, Teluij M, Buitelaar J, Tendolkar I. Amygdala and hippocampus enlargement during adolescence in autism. J Am Acad Child Adolesc Psychiatry. 2010;49:552–60.
pubmed: 20494265