Advances in cerebellar neuroimaging in autism spectrum disorders

Share this content in WeChat

• Review •

CHEN Miaomiao CHU Yao YU Hao CHEN Yuge CHEN Yueqin

Cite this article as: CHEN M M, CHU Y, YU H, et al. Advances in cerebellar neuroimaging in autism spectrum disorders[J]. Chin J Magn Reson Imaging, 2023, 14(5): 161-165, 185. DOI:10.12015/issn.1674-8034.2023.05.028.

Abstract

[Abstract] Autism Spectrum Disorders (ASD) is a highly heterogeneous neurodevelopmental disorders. Neuroimaging studies have shown that there are structural or functional changes in several brain regions in ASD patients, among which the prefrontal cortex and limbic system have been studied the most. Therefore, ASD-related reviews mainly focus on these brain regions. In addition, several studies have shown that the cerebellum plays an important role in cognition and emotional behavior, which may be one of the key brain regions affecting the core symptoms of ASD patients. However, there are few relevant summary reports.Therefore, by searching the imaging studies related to ASD in recent years and taking the structural and functional changes of the cerebellum as the breakthrough point, the relevant literatures were sorted out, analyzed and reviewed, in order to provide ideas and directions for further revealing the role of the cerebellum in the pathogenesis of ASD.

[Keywords] autism spectrum disorder；neuroimaging；magnetic resonance imaging；positron emission tomography；magnetoencephalography；cerebellum；cerebellar-brain circuit

Contributor Information

CHEN Miaomiao¹ CHU Yao¹ YU Hao² CHEN Yuge² CHEN Yueqin^2*

¹ School of Clinical, Jining Medical University, Jining 272013, China

² Department of Medical Imaging, the Affiliated Hospital of Jining Medical University, Jining 272029, China

Corresponding author: Chen YQ, E-mail: sdjnchenyueqin@163.com

Conflicts of interest None.

Publication Information

ACKNOWLEDGMENTS Natural Science Foundation of Shandong (No. ZR2021MH109); Jining Medical University 2022 High-level Scientific Research Project Cultivation Plan (No. JYGC2022FKJ011).

Received 2022-10-25

Accepted 2023-05-06

DOI: 10.12015/issn.1674-8034.2023.05.028

Text

References

[1]

HYMAN S L, LEVY S E, MYERS S M, et al. Identification, Evaluation, and Management of Children With Autism Spectrum Disorder[J/OL]. Pediatrics, 2020, 145(1): e20193447 [2022-10-25]. https://doi.org/10.1542/peds.2019-3447. DOI: 10.1542/peds.2019-3447">10.1542/peds.2019-3447">10.1542/peds.2019-3447.

[2]

BLOOMER B F, MORALES J J, BOLBECKER A R, et al. Cerebellar Structure and Function in Autism Spectrum Disorder[J/OL]. J Psychiatr Brain Sci, 2022, 7: e220003 [2022-10-25]. https://doi.org/10.20900/jpbs.20220003. DOI: 10.20900/jpbs.20220003">10.20900/jpbs.20220003">10.20900/jpbs.20220003.

[3]

HADDERS-ALGRA M. Emerging signs of autism spectrum disorder in infancy: Putative neural substrate[J]. Dev Med Child Neurol, 2022, 64(11): 1344-1350. DOI: 10.1111/dmcn.15333">10.1111/dmcn.15333">10.1111/dmcn.15333.

[4]

ZHAO X, ZHU S, CAO Y, et al. Regional homogeneity of adolescents with high-functioning autism spectrum disorder and its association with symptom severity[J/OL]. Brain Behav, 2022, 12(8): e2693 [2022-10-25]. https://doi.org/10.1002/brb3.2693. DOI: 10.1002/brb3.2693">10.1002/brb3.2693">10.1002/brb3.2693.

[5]

D'MELLO A M, STOODLEY C J. Cerebro-cerebellar circuits in autism spectrum disorder[J/OL]. Front Neurosci, 2015, 9: 408 [2022-10-25]. https://doi.org/10.3389/fnins.2015.00408. DOI: 10.3389/fnins.2015.00408">10.3389/fnins.2015.00408">10.3389/fnins.2015.00408.

[6]

SU L D, XU F X, WANG X T, et al. Cerebellar Dysfunction, Cerebro-cerebellar Connectivity and Autism Spectrum Disorders[J]. Neuroscience, 2021, 462: 320-327. DOI: 10.1016/j.neuroscience.2020.05.028">10.1016/j.neuroscience.2020.05.028">10.1016/j.neuroscience.2020.05.028.

[7]

SYDNOR L M, ALDINGER K A. Structure, Function, and Genetics of the Cerebellum in Autism[J/OL]. J Psychiatr Brain Sci, 2022, 7(5): e220008 [2022-10-25]. https://doi.org/10.20900/jpbs.20220008. DOI: 10.20900/jpbs.20220008">10.20900/jpbs.20220008">10.20900/jpbs.20220008.

[8]

TSAI P T. Autism and cerebellar dysfunction: Evidence from animal models[J]. Semin Fetal Neonatal Med, 2016, 21(5): 349-355. DOI: 10.1016/j.siny.2016.04.009">10.1016/j.siny.2016.04.009">10.1016/j.siny.2016.04.009.

[9]

YAO T T, CHEN Z M, WANG M, et al. Characteristics of magnetic resonance spectra from the cerebella of autistic children[J]. Chin J Phys Med Rehabil, 2020, 42(6): 546-549. DOI: 10.3760/cma.j.issn.0254-1424.2020.06.015">10.3760/cma.j.issn.0254-1424.2020.06.015">10.3760/cma.j.issn.0254-1424.2020.06.015.

[10]

VAN DER HEIJDEN M E, GILL J S, SILLITOE R V. Abnormal Cerebellar Development in Autism Spectrum Disorders[J]. Dev Neurosci, 2021, 43(3-4): 181-190. DOI: 10.1159/000515189">10.1159/000515189">10.1159/000515189.

[11]

YANG X, YIN H, WANG X, et al. Social Deficits and Cerebellar Degeneration in Purkinje Cell Scn8a Knockout Mice[J/OL]. Front Mol Neurosci, 2022, 15: 822129 [2022-10-25]. https://doi.org/10.3389/fnmol.2022.822129. DOI: 10.3389/fnmol.2022.822129">10.3389/fnmol.2022.822129">10.3389/fnmol.2022.822129.

[12]

MAPELLI L, SODA T, D'ANGELO E, et al. The Cerebellar Involvement in Autism Spectrum Disorders: From the Social Brain to Mouse Models[J/OL]. Int J Mol Sci, 2022, 23(7): 3894 [2022-10-25]. https://doi.org/10.3390/ijms23073894. DOI: 10.3390/ijms23073894">10.3390/ijms23073894">10.3390/ijms23073894.

[13]

HU S, LI H, ZHANG Y Q, et al. Advances in neuroimaging studies of childhood autism[J]. Chin J Magn Reson Imaging, 2021, 12(11): 105-108. DOI: 10.12015/issn.1674-8034.2021.11.026">10.12015/issn.1674-8034.2021.11.026">10.12015/issn.1674-8034.2021.11.026.

[14]

BECKINGHAUSEN J, SILLITOE R V. Insights into cerebellar development and connectivity[J]. Neurosci Lett, 2019, 688: 2-13. DOI: 10.1016/j.neulet.2018.05.013">10.1016/j.neulet.2018.05.013">10.1016/j.neulet.2018.05.013.

[15]

BRADY R O, Jr, BEERMANN A, NYE M, et al. Cerebellar-Cortical Connectivity Is Linked to Social Cognition Trans-Diagnostically[J/OL]. Front Psychiatry, 2020, 11: 573002 [2022-10-25]. https://doi.org/10.3389/fpsyt.2020.573002. DOI: 10.3389/fpsyt.2020.573002">10.3389/fpsyt.2020.573002">10.3389/fpsyt.2020.573002.

[16]

WANG D H, LIN X J, ZHU D L, et al. Research progress in the association of cerebellum and cognition[J]. J Clin Neuro, 2020, 33(1): 73-76.

[17]

STOODLEY C J, D'MELLO A M, ELLEGOOD J, et al. Altered cerebellar connectivity in autism and cerebellar-mediated rescue of autism-related behaviors in mice[J]. Nat Neurosci, 2017, 20(12): 1744-1751. DOI: 10.1038/s41593-017-0004-1">10.1038/s41593-017-0004-1">10.1038/s41593-017-0004-1.

[18]

CHAO O Y, MARRON FERNANDEZ DE VELASCO E, PATHAK S S, et al. Targeting inhibitory cerebellar circuitry to alleviate behavioral deficits in a mouse model for studying idiopathic autism[J]. Neuropsychopharmacology, 2020, 45(7): 1159-1170. DOI: 10.1038/s41386-020-0656-5">10.1038/s41386-020-0656-5">10.1038/s41386-020-0656-5.

[19]

SHEN L P, LI W, PEI L Z, et al. Oxytocin Receptor in Cerebellar Purkinje Cells Does Not Engage in Autism-Related Behaviors[J/OL]. Cerebellum, 2022 [2022-10-25]. https://doi.org/10.1007/s12311-022-01466-5. DOI: 10.1007/s12311-022-01466-5">10.1007/s12311-022-01466-5">10.1007/s12311-022-01466-5.

[20]

D'URSO G, TOSCANO E, SANGES V, et al. Cerebellar Transcranial Direct Current Stimulation in Children with Autism Spectrum Disorder: A Pilot Study on Efficacy, Feasibility, Safety, and Unexpected Outcomes in Tic Disorder and Epilepsy[J/OL]. J Clin Med, 2021, 11(1): 143 [2022-10-25]. https://doi.org/10.3390/jcm11010143. DOI: 10.3390/jcm11010143">10.3390/jcm11010143">10.3390/jcm11010143.

[21]

HADOUSH H, HADOUSH A. Modulation of Resting-State Brain Complexity After Bilateral Cerebellar Anodal Transcranial Direct Current Stimulation in Children with Autism Spectrum Disorders: a Randomized Controlled Trial Study[J/OL]. Cerebellum, 2022 [2022-10-25]. https://doi.org/10.1007/s12311-022-01481-6. DOI: 10.1007/s12311-022-01481-6">10.1007/s12311-022-01481-6">10.1007/s12311-022-01481-6.

[22]

FROSCH I R, MITTAL V A, D'MELLO A M. Cerebellar Contributions to Social Cognition in ASD: A Predictive Processing Framework[J/OL]. Front Integr Neurosci, 2022, 16: 810425 [2022-10-25]. https://doi.org/10.3389/fnint.2022.810425. DOI: 10.3389/fnint.2022.810425">10.3389/fnint.2022.810425">10.3389/fnint.2022.810425.

[23]

POTE I, WANG S, SETHNA V, et al. Familial risk of autism alters subcortical and cerebellar brain anatomy in infants and predicts the emergence of repetitive behaviors in early childhood[J]. Autism Res, 2019, 12(4): 614-627. DOI: 10.1002/aur.2083">10.1002/aur.2083">10.1002/aur.2083.

[24]

D'MELLO A M, CROCETTI D, MOSTOFSKY S H, et al. Cerebellar gray matter and lobular volumes correlate with core autism symptoms[J]. Neuroimage Clin, 2015, 7: 631-639. DOI: 10.1016/j.nicl.2015.02.007">10.1016/j.nicl.2015.02.007">10.1016/j.nicl.2015.02.007.

[25]

WANG Y, XU Q, ZUO C, et al. Longitudinal Changes of Cerebellar Thickness in Autism Spectrum Disorder[J/OL]. Neurosci Lett, 2020, 728: 134949 [2022-10-25]. https://doi.org/10.1016/j.neulet.2020.134949. DOI: 10.1016/j.neulet.2020.134949">10.1016/j.neulet.2020.134949">10.1016/j.neulet.2020.134949.

[26]

D'MELLO A M, MOORE D M, CROCETTI D, et al. Cerebellar gray matter differentiates children with early language delay in autism[J]. Autism Res, 2016, 9(11): 1191-1204. DOI: 10.1002/aur.1622">10.1002/aur.1622">10.1002/aur.1622.

[27]

MCKINNEY W S, KELLY S E, UNRUH K E, et al. Cerebellar Volumes and Sensorimotor Behavior in Autism Spectrum Disorder[J/OL]. Front Integr Neurosci, 2022 [2022-10-25]. https://doi.org/10.3389/fnint.2022.821109. DOI: 10.3389/fnint.2022.821109">10.3389/fnint.2022.821109">10.3389/fnint.2022.821109.

[28]

VIJAYAKUMAR N, BALL G, SEAL M L, et al. The development of structural covariance networks during the transition from childhood to adolescence[J/OL]. Sci Rep, 2021, 11(1): 9451 [2022-10-25]. https://doi.org/10.1038/s41598-021-88918-w. DOI: 10.1038/s41598-021-88918-w">10.1038/s41598-021-88918-w">10.1038/s41598-021-88918-w.

[29]

CHEN Q, WANG X, CAO M Q, et al. Visual fixation patterns during basic facial emotion recognition and its correlation with social impairment among children with high-functioning autism spectrum disorder[J]. Chin J Pediatr, 2021, 59(6): 484-488. DOI: 10.3760/cma.j.cn112140-20210106-00014">10.3760/cma.j.cn112140-20210106-00014">10.3760/cma.j.cn112140-20210106-00014.

[30]

HANAIE R, MOHRI I, KAGITANI-SHIMONO K, et al. Altered microstructural connectivity of the superior cerebellar peduncle is related to motor dysfunction in children with autistic spectrum disorders[J]. Cerebellum, 2013, 12(5): 645-656. DOI: 10.1007/s12311-013-0475-x">10.1007/s12311-013-0475-x">10.1007/s12311-013-0475-x.

[31]

KIM J I, BANG S, YANG J J, et al. Classification of Preschoolers with Low-Functioning Autism Spectrum Disorder Using Multimodal MRI Data[J/OL]. J Autism Dev Disord, 2022 [2022-10-25]. https://doi.org/10.1007/s10803-021-05368-z. DOI: 10.1007/s10803-021-05368-z">10.1007/s10803-021-05368-z">10.1007/s10803-021-05368-z.

[32]

IPSER J C, SYAL S, BENTLEY J, et al. 1H-MRS in autism spectrum disorders: a systematic meta-analysis[J]. Metab Brain Dis, 2012, 27(3): 275-287. DOI: 10.1007/s11011-012-9293-y">10.1007/s11011-012-9293-y">10.1007/s11011-012-9293-y.

[33]

KANG Q Q, LI X, TONG G L, et al. Magnetic resonance spectroscopy features of the thalamus and the cerebellum and their association with clinical features in children with autism spectrum disorder: a prospective study[J]. Chin J Contemp Pediatr, 2021, 23(12): 1250-1255. DOI: 10.7499/j.issn.1008-8830.2108137">10.7499/j.issn.1008-8830.2108137">10.7499/j.issn.1008-8830.2108137.

[34]

HEGARTY J P, WEBER D J, CIRSTEA C M, et al. Cerebro-Cerebellar Functional Connectivity is Associated with Cerebellar Excitation-Inhibition Balance in Autism Spectrum Disorder[J]. J Autism Dev Disord, 2018, 48(10): 3460-3473. DOI: 10.1007/s10803-018-3613-y">10.1007/s10803-018-3613-y">10.1007/s10803-018-3613-y.

[35]

FAN L, WANG D H, SHI J P, et al. Characteristics of cognitive function changes in patients with cerebellar infarction[J]. Chin J Neuromed, 2019, 18(7): 662-667. DOI: 10.3760/cma.j.issn.1671-8925.2019.07.003">10.3760/cma.j.issn.1671-8925.2019.07.003">10.3760/cma.j.issn.1671-8925.2019.07.003.

[36]

LEPPING R J, MCKINNEY W S, MAGNON G C, et al. Visuomotor brain network activation and functional connectivity among individuals with autism spectrum disorder[J]. Hum Brain Mapp, 2022, 43(2): 844-859. DOI: 10.1002/hbm.25692">10.1002/hbm.25692">10.1002/hbm.25692.

[37]

UNRUH K E, MARTIN L E, MAGNON G, et al. Cortical and subcortical alterations associated with precision visuomotor behavior in individuals with autism spectrum disorder[J]. J Neurophysiol, 2019, 122(4): 1330-1341. DOI: 10.1152/jn.00286.2019">10.1152/jn.00286.2019">10.1152/jn.00286.2019.

[38]

SUPEKAR K, RYALI S, MISTRY P, et al. Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism[J/OL]. Nat Commun, 2021, 12(1): 3537 [2022-10-25]. https://doi.org/10.1038/s41467-021-23822-5. DOI: 10.1038/s41467-021-23822-5">10.1038/s41467-021-23822-5">10.1038/s41467-021-23822-5.

[39]

OLDEHINKEL M, MENNES M, MARQUAND A, et al. Altered Connectivity Between Cerebellum, Visual, and Sensory-Motor Networks in Autism Spectrum Disorder: Results from the EU-AIMS Longitudinal European Autism Project[J]. Biol Psychiatry Cogn Neurosci Neuroimaging, 2019, 4(3): 260-270. DOI: 10.1016/j.bpsc.2018.11.010">10.1016/j.bpsc.2018.11.010">10.1016/j.bpsc.2018.11.010.

[40]

TRIMARCO E, MIRINO P, CALIGIORE D. Cortico-Cerebellar Hyper-Connections and Reduced Purkinje Cells Behind Abnormal Eyeblink Conditioning in a Computational Model of Autism Spectrum Disorder[J/OL]. Front Syst Neurosci, 2021, 15: 666649 [2022-10-25]. https://doi.org/10.3389/fnsys.2021.666649. DOI: 10.3389/fnsys.2021.666649">10.3389/fnsys.2021.666649">10.3389/fnsys.2021.666649.

[41]

BEDNARZ H M, KANA R K. Patterns of Cerebellar Connectivity with Intrinsic Connectivity Networks in Autism Spectrum Disorders[J]. J Autism Dev Disord, 2019, 49(11): 4498-4514. DOI: 10.1007/s10803-019-04168-w">10.1007/s10803-019-04168-w">10.1007/s10803-019-04168-w.

[42]

KHAN A J, NAIR A, KEOWN C L, et al. Cerebro-cerebellar Resting-State Functional Connectivity in Children and Adolescents with Autism Spectrum Disorder[J]. Biol Psychiatry, 2015, 78(9): 625-634. DOI: 10.1016/j.biopsych.2015.03.024">10.1016/j.biopsych.2015.03.024">10.1016/j.biopsych.2015.03.024.

[43]

YEH C H, TSENG R Y, NI H C, et al. White matter microstructural and morphometric alterations in autism: implications for intellectual capabilities[J/OL]. Mol Autism, 2022, 13(1): 21 [2022-10-25]. https://doi.org/10.1186/s13229-022-00499-1. DOI: 10.1186/s13229-022-00499-1">10.1186/s13229-022-00499-1">10.1186/s13229-022-00499-1.

[44]

HANAIE R, MOHRI I, KAGITANI-SHIMONO K, et al. Aberrant Cerebellar-Cerebral Functional Connectivity in Children and Adolescents With Autism Spectrum Disorder[J/OL]. Front Hum Neurosci, 2018, 12: 454 [2022-10-25]. https://doi.org/10.3389/fnhum.2018.00454. DOI: 10.3389/fnhum.2018.00454.

[45]

WANG Q, LI H Y, LI Y D, et al. Resting-state abnormalities in functional connectivity of the default mode network in autism spectrum disorder: a meta-analysis[J]. Brain Imaging Behav, 2021, 15(5): 2583-2592. DOI: 10.1007/s11682-021-00460-5.

[46]

OLIVITO G, CLAUSI S, LAGHI F, et al. Resting-State Functional Connectivity Changes Between Dentate Nucleus and Cortical Social Brain Regions in Autism Spectrum Disorders[J]. Cerebellum, 2017, 16(2): 283-292. DOI: 10.1007/s12311-016-0795-8.

[47]

IGELSTROM K M, WEBB T W, GRAZIANO M S A. Functional Connectivity Between the Temporoparietal Cortex and Cerebellum in Autism Spectrum Disorder[J]. Cereb Cortex, 2017, 27(4): 2617-2627. DOI: 10.1093/cercor/bhw079.

[48]

ARNOLD ANTERAPER S, GUELL X, D'MELLO A, et al. Disrupted Cerebrocerebellar Intrinsic Functional Connectivity in Young Adults with High-Functioning Autism Spectrum Disorder: A Data-Driven, Whole-Brain, High-Temporal Resolution Functional Magnetic Resonance Imaging Study[J]. Brain Connect, 2019, 9(1): 48-59. DOI: 10.1089/brain.2018.0581.

[49]

XIN X, FENG Y, LOU Y, et al. Abnormal dynamics of brain functional networks in children with Tourette syndrome[J]. J Psychiatr Res, 2023, 159: 249-257. DOI: 10.1016/j.jpsychires.2023.01.046.

[50]

GUELL X. Functional Gradients of the Cerebellum: a Review of Practical Applications[J]. Cerebellum, 2022, 21(6): 1061-1072. DOI: 10.1007/s12311-021-01342-8.

[51]

G B, JK K, MA U, et al. Cerebral hypoperfusion in autism spectrum disorder[J]. Acta Neurobiol Exp (Wars), 2018, 78(1): 21-29. DOI: 10.21307/ane-2018-005.

[52]

KOWALEWSKA B, DROZDZ W, KOWALEWSKI L. Positron emission tomography (PET) and single-photon emission computed tomography (SPECT) in autism research: literature review[J]. Ir J Psychol Med, 2022, 39(3): 272-286. DOI: 10.1017/ipm.2021.15.

[53]

ZHAN F C, CAO C Y, CAO L. Advances in magnetoencephalogram studies of episodic diseases of the nervous system[J]. J Shanghai Jiaotong Univ (Med Sci), 2018, 38(8): 980-983, 979. DOI: 10.3969/j.issn.1674-8115.2018.08.020.

[54]

STYLIADIS C, LEUNG R, OZCAN S, et al. Atypical spatiotemporal activation of cerebellar lobules during emotional face processing in adolescents with autism[J]. Hum Brain Mapp, 2021, 42(7): 2099-2114. DOI: 10.1002/hbm.25349.

PREV Research progress of MRI on pathological changes and cognitive impairment of radiation-induced brain injury

NEXT Research progress of coronary artery calcification and cognitive impairment and brain magnetic resonance imaging

LINK

Tel & Fax: +8610-67113815 E-mail: editor@cjmri.cn