Abstract
Motor disturbance and altered motor networks are commonly reported in individuals with autism spectrum disorder (ASD). It has been suggested that electroencephalogram (EEG) can be used to provide exquisite temporal resolution for understanding motor control processes in ASD. However, the variability of study design and EEG approaches can impact our interpretation. Here, we conducted a systematic review on recent 11 EEG studies that involve motor observation and/or execution tasks and evaluated how these findings help us understand motor difficulties in ASD. Three behavior paradigms with different EEG analytic methods were demonstrated. The main findings were quite mixed: children with ASD did not always show disrupted neuronal activity during motor observation. Additionally, they might have intact ability for movement execution but have more difficulties in neuronal modulation during movement preparation. We would like to promote discussions on how methodological selections of behavioral tasks and data analytic approaches impact our interpretation of motor deficits in ASD. Future EEG research addressing the inconsistency across methodological approaches is necessary to help us understand neurophysiological mechanism of motor abnormalities in ASD.
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Abbreviations
- AD:
-
Asperger’s Disorder
- ADI-R:
-
Autism Diagnostic Interview-Revised
- ADOS:
-
Autism Diagnostic Observation Schedule
- ADOS-G:
-
Autism Diagnostic Observation Schedule-Generic
- AP:
-
Absolute power
- APA:
-
American Psychology Association
- ASD:
-
Autism spectrum disorder
- BA:
-
Brodmann
- BEM:
-
Boundary element model
- BOLD:
-
Blood-oxygen-level-dependent
- CBCL:
-
The Child Behavior Checklist
- CSD:
-
Current source density
- CG:
-
Comparison group
- EEG:
-
Electroencephalogram
- DBD:
-
The Disruptive Behavior Disorder Rating Scale
- DMN:
-
Default Mode Network
- DICA-IV:
-
Diagnostic Interview for children and Adolescents-Fourth Edition
- DSM-IV:
-
Diagnostic and Statistical Manual of Mental Disorders-Fourth Edition
- DSM-IV-TR:
-
Diagnostic and Statistical Manual of Mental Disorders-Fourth Edition-Text Revision
- DSM-V:
-
Diagnostic and Statistical Manual of Mental Disorders-Fifth Edition
- EEG:
-
Electroencephalography
- ERD:
-
Event-related desynchronization
- ERP:
-
Event-related potential
- ERS:
-
Event-related synchronization
- ERSP:
-
Event-related spectral perturbations
- EOG:
-
Electro-oculograms
- FSIQ:
-
Full-scale intelligence quotient
- FFTs:
-
Fast Fourier Transforms
- FL:
-
Frontal left
- HFA:
-
High-functioning autism
- IC:
-
Intrinsic connectivity
- ICA:
-
Independent component analysis
- ICN:
-
Intrinsic connectivity network
- LRP:
-
Lateralized readiness potential
- LC:
-
Left central
- LP:
-
Left parietal
- PANESS:
-
The physical Neurological Subtle signs
- K-SADS:
-
Schedule for Affective Disorder and Schizophrenia for School-Age Children
- M1:
-
Primary motor cortex
- MEG:
-
Magnetoencephalography
- MNS:
-
Mirror Neuron System
- MRP:
-
Movement related potential
- PB:
-
Parietal bilateral
- PMI:
-
Parietal midline
- PM:
-
Premotor area
- PANESS:
-
Physical neurological subtle signs
- PCP:
-
Principle component analysis
- PRISMA-P:
-
Preferred reporting items for systematic review and meta-analysis protocols
- ROI:
-
Region of interest
- SCQ:
-
The Social Communication Questionnaire
- SD:
-
Standard deviation
- SMA:
-
Supplemental motor area
- SRS:
-
The Social Responsiveness Scale
- STFT:
-
Short-time Fourier transform
- STS:
-
Superior temporal sulcus
- TL:
-
Temporal left
- TR:
-
Temporal right
- WASI:
-
The Weschler Abbreviated Scale of Intelligence
- WAIS-R:
-
Wechsler Adult Intelligence Scale—Revised
- WPPSI-IV:
-
Wechsler Preschool and Primary Scale of Intelligence—Fourth Edition
- WISC-III:
-
Wechsler Intelligence Scale for Children-Third Edition
- WISC-IV:
-
Weschler Intelligence Scale for Children-Fourth Edition
References
Allen G (2006) Cerebellar contributions to autism spectrum disorders. Clin Neurosci Res 6:195–207. https://doi.org/10.1016/j.cnr.2006.06.002
American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders IV-TR, 4th edn. American Psychiatric Association, Washington, D.C.
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders – 5. 5th edn. American Psychiatric Association, Washington D.C.
Bastos AM, Schoffelen JM (2016) A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front Syst Neurosci 9:175. https://doi.org/10.3389/FNSYS.2015.00175/BIBTEX
Bhat AN, Landa RJ, Galloway JC (2011) Current perspectives on motor functioning in infants, children, and adults with autism spectrum disorders. Phys Ther 91:1116–1129. https://doi.org/10.2522/ptj.20100294
Bo J, Langan J, Seidler RD (2008) Cognitive Neuroscience of Skill Acquisition. Elsevier
Bo J, Lee C-M, Colbert A, Shen B (2016) Do children with autism spectrum disorders have motor learning difficulties? Res Autism Spectr Disord 23:50–62. https://doi.org/10.1016/j.rasd.2015.12.001
Boutros NN, Korzyukov O, Jansen B et al (2004) Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 126:203–215. https://doi.org/10.1016/j.psychres.2004.01.007
Classen J, Gerloff C, Honda M, Hallett M (1998) Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. J Neurophysiol 79:1567–1573. https://doi.org/10.1152/JN.1998.79.3.1567/ASSET/IMAGES/LARGE/JNP.MR03F4.JPEG
Cochin S, Barthelemy C, Lejeune B et al (1998) Perception of motion and qEEG activity in human adults. Electroencephalogr Clin Neurophysiol 107:287–295. https://doi.org/10.1016/S0013-4694(98)00071-6
Cochin S, Barthelemy C, Roux S, Martineau J (2001) Electroencephalographic activity during perception of motion in childhood. Eur J Neurosci 13:1791–1796. https://doi.org/10.1046/j.0953-816x.2001.01544.x
Cossu G, Boria S, Copioli C et al (2012) Motor representation of actions in children with autism. PLoS One 7:e44779. https://doi.org/10.1371/journal.pone.0044779
Cunnington R, Iansek R, Bradshaw JL, Phillips JG (1995) Movement-related potentials in parkinson’s disease: Presence and predictability of temporal and spatial cues. Brain 118:935–950. https://doi.org/10.1093/brain/118.4.935
Damasio AR, Maurer RG (1978) A Neurological Model for Childhood Autism. Arch Neurol 35:777–786. https://doi.org/10.1001/archneur.1978.00500360001001
Deecke L, Kornhuber HH (1978) An electrical sign of participation of the mesial “supplementary” motor cortex in human voluntary finger movement. Brain Res 159:473–476. https://doi.org/10.1016/0006-8993(78)90561-9
Deecke L, Lang W (1996) Generation of movement-related potentials and fields in the supplementary sensorimotor area and the primary motor area. Adv Neurol 70:127–146
Dinstein I, Thomas C, Humphreys K et al (2010) Normal movement selectivity in autism. Neuron 66:461–469. https://doi.org/10.1016/j.neuron.2010.03.034
Downey R, Rapport MJK (2012) Motor activity in children with autism: a review of current literature. Pediatr Phys Ther 24:2–20. https://doi.org/10.1097/PEP.0b013e31823db95f
Dziuk MA, Larson JCG, Apostu A et al (2007) Dyspraxia in autism: association with motor, social, and communicative deficits. Dev Med Child Neurol 49:734–739. https://doi.org/10.1111/j.1469-8749.2007.00734.x
Edwards LA (2014) A meta-analysis of imitation abilities in individuals with autism spectrum disorders. Autism Res 7:363–380. https://doi.org/10.1002/aur.1379
Enticott PG, Bradshaw JL, Iansek R et al (2009) Electrophysiological signs of supplementary-motor-area deficits in high-functioning autism but not Asperger syndrome: an examination of internally cued movement-related potentials. Dev Med Child Neurol 51:787–791. https://doi.org/10.1111/j.1469-8749.2009.03270.x
Esposito G, Venuti P (2008) Analysis of toddlers’ gait after six months of independent walking to identify autism: a preliminary study. Percept Mot Skills 106:259–269. https://doi.org/10.2466/pms.106.1.259-269
Ewen JB, Lakshmanan BM, Hallett M et al (2015) Dynamics of functional and effective connectivity within human cortical motor control networks. Clin Neurophysiol 126:987. https://doi.org/10.1016/J.CLINPH.2014.09.006
Ewen JB, Lakshmanan BM, Pillai AS et al (2016) Decreased modulation of EEG oscillations in high-functioning autism during a motor control task. Front Hum Neurosci 10:1–11. https://doi.org/10.3389/fnhum.2016.00198
Fan YT, Decety J, Yang CY et al (2010) Unbroken mirror neurons in autism spectrum disorders. J Child Psychol Psychiatry 51:981–988. https://doi.org/10.1111/j.1469-7610.2010.02269.x
Faw B (2003) Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: A tutorial review. Conscious Cogn 12:83–139
Floris DL, Lai MC, Auer T et al (2016) Atypically rightward cerebral asymmetry in male adults with autism stratifies individuals with and without language delay. Hum Brain Mapp 37:230–253. https://doi.org/10.1002/HBM.23023
Floris DL, Howells H (2018) Atypical structural and functional motor networks in autism. In: Progress in Brain Research. Elsevier B.V., pp 207–248
Fournier KA, Hass CJ, Naik SK et al (2010) Motor coordination in autism spectrum disorders: A synthesis and meta-analysis. J Autism Dev Disord 40:1227–1240. https://doi.org/10.1007/s10803-010-0981-3
Freitag CM, Kleser C, Schneider M, von Gontard A (2007) Quantitative assessment of neuromotor function in adolescents with high functioning autism and Asperger syndrome. J Autism Dev Disord 37:948–959. https://doi.org/10.1007/s10803-006-0235-6
Gastaut HJ (1951) The Electrical Activity of the Brain. Annu Rev Physiol 13:297–326. https://doi.org/10.1146/annurev.ph.13.030151.001501
Ghanbari Y, Bloy L, Christopher Edgar J et al (2015) Joint analysis of band-specific functional connectivity and signal complexity in autism. J Autism Dev Disord 45:444–460. https://doi.org/10.1007/s10803-013-1915-7
Gowen E, Hamilton A (2013) Motor abilities in autism: A review using a computational context. J Autism Dev Disord 43:323–344
Gurau O, Bosl WJ, Newton CR (2017) How useful is electroencephalography in the diagnosis of autism spectrum disorders and the delineation of subtypes: A systematic review. Front Psychiatry 8:121
Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H (2006) Anatomical differences in the mirror neuron system and social cognition network in autism. Cereb Cortex 16:1276–1282. https://doi.org/10.1093/cercor/bhj069
Hill EL, Frith U (2003) Understanding autism: insights from mind and brain. Philos Trans R Soc Lond B Biol Sci 358:281–289. https://doi.org/10.1098/rstb.2002.1209
Hollander E, Wang AT, Braun A, Marsh L (2009) Neurological considerations: Autism and Parkinson’s disease. Psychiatry Res 170:43–51. https://doi.org/10.1016/j.psychres.2008.07.014
Hoshiyama M, Kakigi R, Berg P et al (1997) Identification of motor and sensory brain activities during unilateral finger movement: Spatiotemporal source analysis of movement associated magnetic fields. Exp Brain Res 115:6–14. https://doi.org/10.1007/PL00005685
Kana RK, Wadsworth HM, Travers BG (2011) A systems level analysis of the mirror neuron hypothesis and imitation impairments in autism spectrum disorders. Neurosci Biobehav Rev 35:894–902
Kennedy DP, Redcay E, Courchesne E (2006) Failing to deactivate: Resting functional abnormalities in autism. Proc Natl Acad Sci U S A 103:8275–8280. https://doi.org/10.1073/pnas.0600674103
Kitzbichler MG, Khan S, Ganesan S et al (2015) Altered development and multifaceted band-specific abnormalities of resting state networks in autism. Biol Psychiatry 77:794–804. https://doi.org/10.1016/j.biopsych.2014.05.012
Kumar JS, Bhuvaneswari P (2012) Analysis of electroencephalography (EEG) signals and its categorization - A study. In: Procedia Engineering. Elsevier Ltd, pp. 2525–2536
Larson JCG, Bastian ÃAJ, Donchin O et al (2008) Acquisition of internal models of motor tasks in children with autism. Brain 131:2894–2903. https://doi.org/10.1093/brain/awn226
Lee CM, Bo J (2021) Visuomotor adaptation and its relationship with motor ability in children with and without autism spectrum disorder. Hum Mov Sci. https://doi.org/10.1016/j.humov.2021.102826
Luck SJ (2014) An Introduction to the Event-Related Potential Technique, Second Edition | The MIT Press. MIT Press, Cambridge, MA
Lukito S, Norman L, Carlisi C et al (2020) Comparative meta-analyses of brain structural and functional abnormalities during cognitive control in attention-deficit/hyperactivity disorder and autism spectrum disorder. Psychol Med 50:894–919
Martineau J, Cochin S, Magne R, Barthelemy C (2008) Impaired cortical activation in autistic children: Is the mirror neuron system involved? Int J Psychophysiol 68:35–40. https://doi.org/10.1016/j.ijpsycho.2008.01.002
Martineau J, Cochin S (2003) Visual perception in children: Human, animal and virtual movement activates different cortical areas. In: International Journal of Psychophysiology. Elsevier, pp 37–44
Michel CM, Brunet D (2019) EEG source imaging: A practical review of the analysis steps. Front Neurol 10:325. https://doi.org/10.3389/FNEUR.2019.00325/XML/NLM
Michel CM, He B (2019) EEG source localization. Handb Clin Neurol 160:85–101. https://doi.org/10.1016/B978-0-444-64032-1.00006-0
Moher D, Shamseer L, Clarke M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 4:1. https://doi.org/10.1186/2046-4053-4-1
Montirosso R, Piazza C, Giusti L et al (2019) exploring the EEG mu rhythm associated with observation and execution of a goal-directed action in 14-month-old preterm infants. Sci Rep 9:8975. https://doi.org/10.1038/s41598-019-45495-3
Mosconi MW, Sweeney JA (2015) Sensorimotor dysfunctions as primary features of autism spectrum disorders. Sci China Life Sci 58:1016–1023
Mostofsky SH, Burgess MP, Gidley Larson JC (2007) Increased motor cortex white matter volume predicts motor impairment in autism. Brain 130:2117–2122. https://doi.org/10.1093/brain/awm129
Mostofsky SH, Powell SK, Simmonds DJ et al (2009) Decreased connectivity and cerebellar activity in autism during motor task performance. Brain 132:2413–2425. https://doi.org/10.1093/brain/awp088
Müller RA, Pierce K, Ambrose JB et al (2001) Atypical patterns of cerebral motor activation in autism: a functional magnetic resonance study. Biol Psychiatry 49:665–676. https://doi.org/10.1016/S0006-3223(00)01004-0
Muñoz-Gutiérrez PA, Giraldo E, Bueno-López M, Molinas M (2018) Localization of active brain sources from EEG signals using empirical mode decomposition: a comparative study. Front Integr Neurosci 12:55. https://doi.org/10.3389/FNINT.2018.00055/XML/NLM
Nebel MB, Joel SE, Muschelli J et al (2014) Disruption of functional organization within the primary motor cortex in children with autism. Hum Brain Mapp 35:567–580. https://doi.org/10.1002/hbm.22188
Oberman LM, Hubbard EM, McCleery JP et al (2005) EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cogn Brain Res 24:190–198. https://doi.org/10.1016/j.cogbrainres.2005.01.014
Oberman LM, Ramachandran VS, Pineda JA (2008) Modulation of mu suppression in children with autism spectrum disorders in response to familiar or unfamiliar stimuli: The mirror neuron hypothesis. Neuropsychologia 46:1558–1565. https://doi.org/10.1016/j.neuropsychologia.2008.01.010
Oberman LM, McCleery JP, Hubbard EM et al (2013) Developmental changes in mu suppression to observed and executed actions in autism spectrum disorders. Soc Cogn Affect Neurosci 8:300–304. https://doi.org/10.1093/scan/nsr097
Oztop E, Arbib MA (2002) Schema design and implementation of the grasp-related mirror neuron system. Biol Cybern 87:116–140. https://doi.org/10.1007/s00422-002-0318-1
Pillai AS, McAuliffe D, Lakshmanan BM et al (2018) Altered task-related modulation of long-range connectivity in children with autism. Autism Res 11:245–257. https://doi.org/10.1002/aur.1858
Pokorny JJ, HattColombi NVC et al (2015) The Action Observation System when Observing Hand Actions in Autism and Typical Development. Autism Res 8:284–296. https://doi.org/10.1002/aur.1445
Provost B, Lopez BR, Heimerl S (2007) A comparison of motor delays in young children: Autism spectrum disorder, developmental delay, and developmental concerns. J Autism Dev Disord 37:321–328. https://doi.org/10.1007/s10803-006-0170-6
Qiu A, Adler M, Crocetti D, et al (2010) Basal Ganglia Shapes Predict Social, Communication, and Motor Dysfunctions in Boys With Autism Spectrum Disorder. J Am Acad Child Adolesc Psychiatry 49
Raymaekers R, Wiersema JR, Roeyers H (2009) EEG study of the mirror neuron system in children with high functioning autism. Brain Res 1304:113–121. https://doi.org/10.1016/j.brainres.2009.09.068
Rinehart NJ, Tonge BJ, Bradshaw JL et al (2006a) Gait function in high-functioning autism and Asperger’s disorder : evidence for basal-ganglia and cerebellar involvement? Eur Child Adolesc Psychiatry 15:256–264. https://doi.org/10.1007/s00787-006-0530-y
Rinehart NJ, Tonge BJ, Bradshaw JL et al (2006b) Movement-related potentials in high-functioning autism and Asperger’s disorder. Dev Med Child Neurol 48:272–277. https://doi.org/10.1017/S0012162206000594
Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661–670. https://doi.org/10.1038/35090060
Rogers SJ (1999) An examination of the imitation deficit in autism. Cambridge University Press, Cambridge
Schipul SE, Keller TA, Just MA (2011) Inter-Regional Brain Communication and Its Disturbance in Autism. Front Syst Neurosci 5:1–11. https://doi.org/10.3389/FNSYS.2011.00010
Shallice T, Burgess PW (1991) Deficits in strategy application following frontral lobe damage in man. Brain 114:727–741. https://doi.org/10.1093/brain/114.2.727
Sokhadze EM, Tasman A, Sokhadze GE et al (2016) Behavioral, Cognitive, and Motor Preparation Deficits in a Visual Cued Spatial Attention Task in Autism Spectrum Disorder. Appl Psychophysiol Biofeedback 41:81–92. https://doi.org/10.1007/s10484-015-9313-x
Swatzyna RJ, Boutros NN, Genovese AC et al (2019) Electroencephalogram (EEG) for children with autism spectrum disorder: evidential considerations for routine screening. Eur Child Adolesc Psychiatry 28:615–624. https://doi.org/10.1007/s00787-018-1225-x
Taylor JA, Krakauer JW, Ivry RB (2014) Explicit and Implicit Contributions to Learning in a Sensorimotor Adaptation Task. J Neurosci 34:3023–3032. https://doi.org/10.1523/JNEUROSCI.3619-13.2014
Teplan M (2002) Fundamentals of EEG measurement. Measurement Science Review 2:1–11
Unruh KE, Martin LE, Magnon G et al (2019) Cortical and subcortical alterations associated with precision visuomotor behavior in individuals with autism spectrum disorder. J Neurophysiol 122:1330–1341. https://doi.org/10.1152/jn.00286.2019
Vasa RA, Mostofsky SH, Ewen JB (2016) The disrupted connectivity hypothesis of autism spectrum disorders: time for the next phase in research. Biol Psychiatry Cogn Neurosci Neuroimaging 1:245–252
Vivanti G, Barbaro J, Hudry K et al (2013) Intellectual development in autism spectrum disorders: new insights from longitudinal studies. Front Hum Neurosci 7:354. https://doi.org/10.3389/fnhum.2013.00354
Wass S (2011) Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn 75:18–28. https://doi.org/10.1016/j.bandc.2010.10.005
Wheaton LA, Nolte G, Bohlhalter S et al (2005a) Synchronization of parietal and premotor areas during preparation and execution of praxis hand movements. Clin Neurophysiol 116:1382–1390. https://doi.org/10.1016/J.CLINPH.2005.01.008
Wheaton LA, Shibasaki H, Hallett M (2005b) Temporal activation pattern of parietal and premotor areas related to praxis movements. Clin Neurophysiol 116:1201–1212. https://doi.org/10.1016/j.clinph.2005.01.001
Williams JHG, Whiten A, Suddendorf T, Perrett DI (2001) Imitation, mirror neurons and autism. Neurosci Biobehav Rev 25:287–295
Yang J, Hofmann J (2016) Action observation and imitation in autism spectrum disorders: an ALE meta-analysis of fMRI studies. Brain Imaging Behav 10:960–969. https://doi.org/10.1007/s11682-015-9456-7
Ye AX, Leung RC, Schäfer CB et al (2014) Atypical resting synchrony in autism spectrum disorder. Hum Brain Mapp 35:6049–6066. https://doi.org/10.1002/hbm.22604
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Bo, J., Acluche, F., Lasutschinkow, P.C. et al. Motor networks in children with autism spectrum disorder: a systematic review on EEG studies. Exp Brain Res 240, 3073–3087 (2022). https://doi.org/10.1007/s00221-022-06483-8
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DOI: https://doi.org/10.1007/s00221-022-06483-8