Cortico-basal ganglia white matter microstructure is linked to restricted repetitive behavior in autism spectrum disorder.

Publisher: BioMed Central Country of Publication: England NLM ID: 101534222 Publication Model: Electronic Cited Medium: Internet ISSN: 2040-2392 (Electronic) NLM ISO Abbreviation: Mol Autism Subsets: MEDLINE

Original Publication: [London] : BioMed Central

White Matter*/diagnostic imaging ; Autism Spectrum Disorder*/diagnostic imaging; United States ; Adolescent ; Child ; Humans ; Basal Ganglia/diagnostic imaging ; Brain ; Water

Background: Restricted repetitive behavior (RRB) is one of two behavioral domains required for the diagnosis of autism spectrum disorder (ASD). Neuroimaging is widely used to study brain alterations associated with ASD and the domain of social and communication deficits, but there has been less work regarding brain alterations linked to RRB.
Methods: We utilized neuroimaging data from the National Institute of Mental Health Data Archive to assess basal ganglia and cerebellum structure in a cohort of children and adolescents with ASD compared to typically developing (TD) controls. We evaluated regional gray matter volumes from T1-weighted anatomical scans and assessed diffusion-weighted scans to quantify white matter microstructure with free-water imaging. We also investigated the interaction of biological sex and ASD diagnosis on these measures, and their correlation with clinical scales of RRB.
Results: Individuals with ASD had significantly lower free-water corrected fractional anisotropy (FA T ) and higher free-water (FW) in cortico-basal ganglia white matter tracts. These microstructural differences did not interact with biological sex. Moreover, both FA T and FW in basal ganglia white matter tracts significantly correlated with measures of RRB. In contrast, we found no significant difference in basal ganglia or cerebellar gray matter volumes.
Limitations: The basal ganglia and cerebellar regions in this study were selected due to their hypothesized relevance to RRB. Differences between ASD and TD individuals that may occur outside the basal ganglia and cerebellum, and their potential relationship to RRB, were not evaluated.
Conclusions: These new findings demonstrate that cortico-basal ganglia white matter microstructure is altered in ASD and linked to RRB. FW in cortico-basal ganglia and intra-basal ganglia white matter was more sensitive to group differences in ASD, whereas cortico-basal ganglia FA T was more closely linked to RRB. In contrast, basal ganglia and cerebellar volumes did not differ in ASD. There was no interaction between ASD diagnosis and sex-related differences in brain structure. Future diffusion imaging investigations in ASD may benefit from free-water estimation and correction in order to better understand how white matter is affected in ASD, and how such measures are linked to RRB.
(© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.)

Magn Reson Med. 2009 Sep;62(3):717-30. (PMID: 19623619)
Psychiatry Res. 2009 Nov 30;170(1):43-51. (PMID: 19815296)
Data Brief. 2015 Jul 31;4:577-82. (PMID: 26322322)
J Int Neuropsychol Soc. 2009 May;15(3):331-43. (PMID: 19402919)
CNS Spectr. 2015 Aug;20(4):412-26. (PMID: 26234701)
Neuroimage. 2011 Jan 1;54(1):264-77. (PMID: 20600980)
J Neurosurg. 2014 Apr;120(4):873-81. (PMID: 24490785)
Nat Neurosci. 2014 Aug;17(8):1022-30. (PMID: 25065439)
Biol Psychiatry. 2023 Jul 1;94(1):29-39. (PMID: 36925414)
Brain. 2017 Aug 1;140(8):2183-2192. (PMID: 28899020)
Neuroimage. 2014 May 15;92:356-68. (PMID: 24384150)
Cortex. 2012 Feb;48(2):183-93. (PMID: 21718979)
Biol Psychiatry. 2005 Aug 1;58(3):226-32. (PMID: 15939406)
Cereb Cortex. 2018 May 1;28(5):1685-1699. (PMID: 28334314)
Neurobiol Aging. 2015 Feb;36(2):1097-104. (PMID: 25467638)
J Autism Dev Disord. 2012 Jun;42(6):1236-48. (PMID: 21584849)
Psychiatry Res. 2015 Jul 30;233(1):64-72. (PMID: 26032898)
Autism. 2019 May;23(4):858-868. (PMID: 30047281)
Autism Res. 2017 Nov;10(11):1751-1775. (PMID: 28730641)
Pharmacol Biochem Behav. 2019 Jun;181:110-116. (PMID: 31054946)
Sci Rep. 2017 Apr 11;7:46401. (PMID: 28397802)
Neuroimage. 2006 Jul 15;31(4):1453-74. (PMID: 16571375)
Neuroimage. 2013 Oct 15;80:125-43. (PMID: 23702418)
Brain Imaging Behav. 2020 Dec;14(6):2084-2096. (PMID: 31342238)
Biol Psychiatry. 2021 Mar 1;89(5):424-432. (PMID: 33349451)
Soc Cogn Affect Neurosci. 2018 Jan 1;13(1):32-42. (PMID: 29177509)
Biol Psychiatry. 2011 May 1;69(9):847-56. (PMID: 21195388)
Cerebellum. 2012 Sep;11(3):777-807. (PMID: 22370873)
J Autism Dev Disord. 2014 Mar;44(3):627-35. (PMID: 23989936)
Neuroimage. 2011 Feb 1;54(3):1786-94. (PMID: 20965257)
Autism Res. 2011 Jun;4(3):212-20. (PMID: 21480545)
Dev Cogn Neurosci. 2016 Jun;19:137-43. (PMID: 26999477)
Cortex. 2012 Jan;48(1):58-81. (PMID: 21481342)
Neuroimage. 2010 Feb 1;49(3):2457-66. (PMID: 19818860)
Mol Autism. 2015 Oct 01;6:54. (PMID: 26435832)
Cortex. 2015 Jan;62:158-81. (PMID: 25433958)
Psychiatry Res Neuroimaging. 2016 Jun 30;252:40-45. (PMID: 27179315)
Nat Rev Neurosci. 2018 Jun;19(6):338-350. (PMID: 29643480)
J Comp Neurol. 1989 Aug 15;286(3):353-75. (PMID: 2768563)
Psychol Med. 2013 May;43(5):1093-107. (PMID: 22894768)
Magn Reson Med. 2021 May;85(5):2537-2551. (PMID: 33270935)
Autism Res. 2012 Oct;5(5):289-313. (PMID: 22786754)
Res Dev Disabil. 2005 Nov-Dec;26(6):527-47. (PMID: 15885981)
J Neurosci. 2008 Aug 27;28(35):8785-8. (PMID: 18753380)
Dev Neurobiol. 2018 May;78(5):456-473. (PMID: 29266810)
J Child Psychol Psychiatry. 2009 Sep;50(9):1102-12. (PMID: 19490309)
Mol Autism. 2021 Jun 30;12(1):48. (PMID: 34193257)
J Am Acad Child Adolesc Psychiatry. 2014 Mar;53(3):329-40.e1-3. (PMID: 24565360)
Front Aging Neurosci. 2022 Nov 11;14:1029166. (PMID: 36437999)
J Psychiatr Res. 2014 Jul;54:26-35. (PMID: 24694669)
Behav Brain Res. 2020 Aug 5;391:112708. (PMID: 32461129)
Pediatrics. 2012 May;129(5):e1301-10. (PMID: 22529279)
Front Comput Neurosci. 2018 Nov 26;12:93. (PMID: 30534065)
Brain. 2015 Aug;138(Pt 8):2322-31. (PMID: 25981960)
Neuroimage. 2009 May 15;46(1):39-46. (PMID: 19457380)
Int J Dev Neurosci. 2011 Jun;29(4):461-7. (PMID: 21329752)
Mol Autism. 2016 Jan 19;7:5. (PMID: 26788282)
Psychol Med. 2019 Oct;49(13):2247-2255. (PMID: 30362446)
Children (Basel). 2021 Apr 22;8(5):. (PMID: 33922236)
Behav Brain Res. 2015 Jan 1;276:45-58. (PMID: 25052167)
Hum Brain Mapp. 2019 Dec 1;40(17):5094-5107. (PMID: 31403737)
Neuroimage. 2008 Feb 1;39(3):956-65. (PMID: 17988895)
Res Dev Disabil. 2005 Nov-Dec;26(6):548-64. (PMID: 16303583)
Lancet Digit Health. 2019 Sep;1(5):e222-e231. (PMID: 32259098)
Harv Rev Psychiatry. 2015 Jul-Aug;23(4):223-44. (PMID: 26146755)
Med Image Comput Comput Assist Interv. 2012;15(Pt 2):305-12. (PMID: 23286062)
Cereb Cortex. 2021 Jul 5;31(8):3962-3972. (PMID: 33791751)
Behav Brain Res. 2005 Feb 28;157(2):363-8. (PMID: 15639187)
Neuroimage. 2019 Oct 15;200:302-312. (PMID: 31260838)
Mol Autism. 2017 Mar 4;8:8. (PMID: 28316772)
Alzheimers Dement (Amst). 2023 May 17;15(2):e12425. (PMID: 37213219)
AJNR Am J Neuroradiol. 2012 Jan;33(1):83-9. (PMID: 22173769)
NPJ Parkinsons Dis. 2023 Jun 5;9(1):85. (PMID: 37277372)
Am J Psychiatry. 2023 Jan 1;180(1):50-64. (PMID: 36415971)
MMWR Surveill Summ. 2023 Mar 24;72(2):1-14. (PMID: 36952288)
Dev Neurosci. 2017;39(5):355-360. (PMID: 28750400)
Mol Autism. 2021 Mar 1;12(1):19. (PMID: 33648569)
JAMA Psychiatry. 2013 Aug;70(8):869-79. (PMID: 23803651)
Behav Brain Res. 2010 Jun 26;210(1):116-22. (PMID: 20178817)
Prog Neuropsychopharmacol Biol Psychiatry. 1999 May;23(4):613-24. (PMID: 10390720)
Front Hum Neurosci. 2013 Aug 06;7:430. (PMID: 23964221)
Brain Struct Funct. 2020 Jan;225(1):427-439. (PMID: 31894407)
Mol Autism. 2015 May 13;6:26. (PMID: 25973163)
J Autism Dev Disord. 2000 Jun;30(3):237-43. (PMID: 11055459)
Neurosci Biobehav Rev. 2018 Sep;92:152-171. (PMID: 29802854)
Cerebellum. 2013 Oct;12(5):645-56. (PMID: 23564050)
PLoS One. 2010 Nov 04;5(11):e13848. (PMID: 21079814)
Neuroimage Clin. 2021;31:102719. (PMID: 34153690)
Biol Psychiatry Cogn Neurosci Neuroimaging. 2019 Jan;4(1):50-61. (PMID: 30446435)
BMC Psychiatry. 2006 Dec 13;6:56. (PMID: 17166273)
Cereb Cortex. 2011 Oct;21(10):2233-43. (PMID: 21378114)
Phys Med Biol. 2023 Oct 26;68(21):. (PMID: 37816373)
Neuroimage Clin. 2022;34:103022. (PMID: 35489192)
Brain. 2016 Feb;139(Pt 2):495-508. (PMID: 26705348)
Nat Neurosci. 2017 Dec;20(12):1744-1751. (PMID: 29184200)
J Child Psychol Psychiatry. 2022 Aug;63(8):855-870. (PMID: 34762311)
Br J Psychiatry. 1999 Nov;175:444-51. (PMID: 10789276)
JAMA Pediatr. 2013 Nov;167(11):1045-52. (PMID: 24061784)
Psychol Med. 2018 Mar;48(4):654-668. (PMID: 28745267)
Behav Brain Res. 2016 Feb 15;299:122-31. (PMID: 26620495)
Autism Res. 2019 Feb;12(2):274-283. (PMID: 30561911)
Dev Sci. 2016 Mar;19(2):284-305. (PMID: 25845529)
Biol Psychiatry. 2014 Sep 1;76(5):405-11. (PMID: 24090791)
Nat Rev Neurosci. 2009 Sep;10(9):659-69. (PMID: 19672274)
Mol Autism. 2022 Dec 19;13(1):48. (PMID: 36536467)
Mov Disord. 2017 Oct;32(10):1457-1464. (PMID: 28714593)
Neurosci Lett. 2007 May 29;419(2):113-8. (PMID: 17485168)
Commun Biol. 2021 May 14;4(1):574. (PMID: 33990680)

UL1 TR001427 United States TR NCATS NIH HHS; UL1TR001427 United States TR NCATS NIH HHS

Keywords: Autism spectrum disorder; Basal ganglia; Cerebellum; Cortico-basal ganglia; Diffusion tensor imaging; Free-water; Gray matter; Restricted repetitive behavior; White matter

059QF0KO0R (Water)

Date Created: 20240123 Date Completed: 20240124 Latest Revision: 20241023

20241023

PMC10804694

10.1186/s13229-023-00581-2

38254158