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Action viewing and language in adolescents with autism spectrum disorder

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Abstract

The mirror neuron system consists of fronto-parietal regions and responds to both goal-directed action execution and observation. The broader action observation network is specifically involved in observation of actions and is thought to play a role in understanding the goals of the motor act, the intention of others, empathy, and language. Many, but not all, studies have found mirror neuron system or action observation network dysfunction in autism spectrum disorder. The objective of this study was to use observation of a goal-directed action fMRI paradigm to examine the action observation network in autism spectrum disorder and to determine whether fronto-parietal activation is associated with language ability. Adolescents with autism spectrum disorder (n = 23) were compared to typically developing adolescents (n = 20), 11–17 years. Overall, there were no group differences in activation, however, the autism spectrum group with impaired expressive language (n = 13) had significantly reduced inferior frontal and inferior parietal activation during action viewing. In controls, right supramarginal gyrus activation was associated with higher expressive language; bilateral supramarginal and left pars opercularis activation was associated with better verbal-gesture integration. Results suggest that action-observation network dysfunction may characterize a subgroup of individuals with autism spectrum disorder with expressive language deficits. Therefore, interventions that target this dysfunctional network may improve expressive language in this autism spectrum subgroup. Future treatment studies should individualize therapeutic approaches based on brain-behavior relationships.

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Availability of data and material

The data that support the findings of this study are not publicly available due to them containing information that could compromise research participant privacy and consent.

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References

  • Almli CR (unpublished) Handedness Test (Preschool Version)

  • Almli CR, Rivkin MJ, McKinstry RC (2007) The NIH MRI study of normal brain development (Objective-2): Newborns infants toddlers and preschoolers. NeuroImage 35(1):308–325. https://doi.org/10.1016/j.neuroimage.2006.08.058

  • American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association Press, Washington, DC

    Google Scholar 

  • American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Association Press, Washington, DC

    Book  Google Scholar 

  • Arnstein D, Cui F, Keysers C, Maurits NM, Gazzola V (2011) mu-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices. J Neurosci 31(40):14243–14249. https://doi.org/10.1523/JNEUROSCI.0963-11.2011

    Article  CAS  Google Scholar 

  • Bernier R, Dawson G, Webb S, Murias M (2007) EEG mu rhythm and imitation impairments in individuals with autism spectrum disorder. Brain Cogn 64:228–237

    Article  CAS  Google Scholar 

  • Bonini L, Rotunno C, Arcuri E, Gallese V (2022) Mirror neurons 30 years later: implications and applications. Trends Cogn Sci 26(9):767–781. https://doi.org/10.1016/j.tics.2022.06.003

    Article  Google Scholar 

  • Buffington DM, Krantz PJ, McClannahan LE, Poulson CL (1998) Procedures for teaching appropriate gestural communication skills to children with autism. J Autism Dev Disord 28(6):535–545

    Article  CAS  Google Scholar 

  • Calvo-Merino B, Glaser DE, Grèzes J, Passingham RE, Haggard P (2005) Action observation and acquired motor skills: an fMRI study with expert dancers. Cereb Cortex 15(8):1243–1249

    Article  CAS  Google Scholar 

  • Capobianco M, Pizzuto EA, Devescovi A (2017) Gesture-speech combinations and early verbal abilities. Interact Stud 18:54–75. https://doi.org/10.1075/is.18.1.03cap

    Article  Google Scholar 

  • Carrow-Woolfolk E (1995) Oral and written language scales. American Guidance Services Inc, Circle Pines, MN

    Google Scholar 

  • Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50(3):1148–1167. https://doi.org/10.1016/j.neuroimage.2009.12.112

    Article  Google Scholar 

  • Catmur C, Walsh V, Hayes C (2007) Sensorimotor learning configures the human mirror system. Curr Biol 17:1527–1531

    Article  CAS  Google Scholar 

  • Cross ES, Hamilton AF, Grafton ST (2006) Building a motor simulation de novo: observation of dance by dancers. Neuroimage 31(3):1257–1267. https://doi.org/10.1016/j.neuroimage.2006.01.033

    Article  Google Scholar 

  • Dapretto M, Davies MS, Pfeifer JH, Scott AA, Sigman M, Bookheimer SY, Iacoboni M (2006) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9(1):28–30

    Article  CAS  Google Scholar 

  • di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91(1):176–180. https://doi.org/10.1007/BF00230027

    Article  Google Scholar 

  • Errante A, Fogassi L (2021) Functional lateralization of the mirror neuron system in monkey and humans. Symmetry 13:77. https://doi.org/10.3390/sym13010077

    Article  Google Scholar 

  • Fan Y-T, Decety J, Yang C-Y, Liu J-L, Cheng Y (2010) Unbroken mirror neurons in autism spectrum disorders. J Child Psychol Psychiatry 51(9):981–988

    Article  Google Scholar 

  • Fecteau S, Carmant L, Tremblay C, Robert M, Bouthillier A, Théoret H (2004) A motor resonance mechanism in children? Evidence from subdural electrodes in a 36-month-old child. NeuroReport 15:2625–2627

    Article  CAS  Google Scholar 

  • Gallese VLF, Fadiga L, Rizzolatti G (2002) Action represntation and the inferior parietal lobule. In: Prinz W, Hommel B (eds) Common mechanisms in perception and action: attention and performance, vol XIX. Oxford University Press, New York

    Google Scholar 

  • Hamilton AF (2013) Reflecting on the mirror neuron system in autism: a systematic review of current theories. Dev Cogn Neurosci 3:91–105. https://doi.org/10.1016/j.dcn.2012.09.008

    Article  Google Scholar 

  • Hardwick RM, Caspers S, Eickhoff SB, Swinnen SP (2018) Neural correlates of action: Comparing meta-analyses of imagery, observation, and execution. Neurosci Biobehav Rev 94:31–44. https://doi.org/10.1016/j.neubiorev.2018.08.003

    Article  Google Scholar 

  • Haslinger B, Erhard P, Altenmüller E, Schroeder U, Boecker H, Ceballos-Baumann AO (2005) Transmodal sensorimotor networks during action observation in professional pianists. J Cogn Neurosci 17(2):282–293

    Article  CAS  Google Scholar 

  • Heyes C (2010) Where do mirror neurons come from? Neurosci Biobehav Rev 34:575–583

    Article  Google Scholar 

  • Hobson HM, Bishop DVM (2016) Mu suppression–a good measure of the human mirror neuron system? Cortex 82:290–310. https://doi.org/10.1016/j.cortex.2016.03.019

    Article  Google Scholar 

  • Hobson HM, Bishop DV (2017) The interpretation of mu suppression as an index of mirror neuron activity: past, present and future. R Soc Open Sci 4(3):160662. https://doi.org/10.1098/rsos.160662

    Article  Google Scholar 

  • Iacoboni M, Dapretto M (2006) The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7(12):942–951

    Article  CAS  Google Scholar 

  • Ingersoll B, Lewis E, Kroman E (2007) Teaching the imitation and spontaneous use of descriptive gestures in young children with autism using a naturalistic behavioral intervention. J Autism Dev Disord 37:1446–1456

    Article  Google Scholar 

  • Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5(2):143–156

    Article  CAS  Google Scholar 

  • Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17(2):825–841

    Article  Google Scholar 

  • Kiefer M, Pulvermuller F (2012) Conceptual representations in mind and brain: theoretical developments, current evidence and future directions. Cortex 48(7):805–825. https://doi.org/10.1016/j.cortex.2011.04.006

    Article  Google Scholar 

  • Kilroy E, Cermak SA, Aziz-Zadeh L (2019) A review of functional and structural neurobiology of the action observation network in autism spectrum disorder and developmental coordination disorder. Brain Sci. https://doi.org/10.3390/brainsci9040075

    Article  Google Scholar 

  • Knaus TA, Silver AM, Kennedy M, Lindgren KA, Dominick KC, Siegel J, Tager-Flusberg H (2010) Language laterality in autism spectrum disorder and typical controls: a functional, volumetric, and diffusion tensor MRI study. Brain Lang 112:113–120

    Article  Google Scholar 

  • Lepage JF, Théoret H (2006) EEG evidence for the presence of an action observation-execution matching system in children. Eur J Neurosci 23:2505–2510

    Article  Google Scholar 

  • Liew S-L, Aziz-Zadeh L (2013) The human mirror neuron system, social control, and language. In: Franks DD, Turner JH (eds) Handbook of Neurosociology. Springer, New York

    Google Scholar 

  • Lord C, Luyster RJ, Gotham K, Guthrie W (2012) Autism diagnostic observation schedule, second edition (ADOS-2) manual (Part II) : toddler module. Western Psychological Services, Torrance, CA

    Google Scholar 

  • Molenberghs P, Cunnington R, Mattingley JB (2012) Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev 36:341–349

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Perkins T, Stokes M, McGillivray J, Bittar R (2010) Mirror neuron dysfunction in autism spectrum disorders. J Clin Neurosci 17:1239–1243

    Article  Google Scholar 

  • Perry A, Bentin S (2009) Mirror activity in the human brain while observing hand movements: a comparison between EEG desynchronization in the mu-range and previous fMRI results. Brain Res 1282:126–132. https://doi.org/10.1016/j.brainres.2009.05.059

    Article  CAS  Google Scholar 

  • Pokorny JJ, Hatt NV, Colombi C, Vivanti G, Rogers SJ, Rivera SM (2015) The action observation system when observing hand actions in autism and typical development. Autism Res 8(3):284–296. https://doi.org/10.1002/aur.1445

    Article  Google Scholar 

  • Ramachandran VS, Oberman LM (2006) Broken mirrors: a theory of autism. Sci Am 295(5):62–69

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21(5):188–194

    Article  CAS  Google Scholar 

  • Rizzolatti G, Fabbri-Destro M (2010) Mirror neurons: from discovery to autism. Exp Brain Res 200:223–237

    Article  Google Scholar 

  • Rizzolatti G, Fabbri-Destro M, Cattaneo L (2009) Mirror neurons and their clinical relevance. Nat Clin Pract Neurol 5(1):24–34

    Article  Google Scholar 

  • Rutter M, Bailey A, Lord C (2003a) Social communication questionnaire. Western Psychological Services, Los Angeles

    Google Scholar 

  • Rutter M, Le Couteur A, Lord C (2003b) Autism diagnostic interview–revised. Western Psychological Services, Los Angeles

    Google Scholar 

  • Ruysschaert L, Warreyn P, Wiersema JR, Oostra A, Roeyers H (2014) Exploring the role of neural mirroring in children with autism spectrum disorder. Autism Res 7(2):197–206. https://doi.org/10.1002/aur.1339

    Article  Google Scholar 

  • Schulte-Ruther M, Otte E, Adiguzel K, Firk C, Herpertz-Dahlmann B, Koch I, Konrad K (2017) Intact mirror mechanisms for automatic facial emotions in children and adolescents with autism spectrum disorder. Autism Res 10(2):298–310. https://doi.org/10.1002/aur.1654

    Article  Google Scholar 

  • Shimada S, Hiraki K (2006) Infant’s brain responses to live and televised action. Neuroimage 32:930–939

    Article  Google Scholar 

  • Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, De Stefano N (2002) Accurate, robust and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17(1):479–489

    Article  Google Scholar 

  • Southgate V, Begus K (2013) Motor activation during the prediction of nonexecutable actions in infants. Psychol Sci 24(6):828–835. https://doi.org/10.1177/0956797612459766

    Article  Google Scholar 

  • Southgate V, Johnson MH, Osborne T, Csibra G (2009) Predictive motor activation during action observation in human infants. Biol Lett 5(6):769–772. https://doi.org/10.1098/rsbl.2009.0474

    Article  Google Scholar 

  • Wadsworth HM, Maximo JO, Lemelman AR, Clayton K, Sivaraman S, Deshpande HD, Ver Hoef L, Kana RK (2017) The Action Imitation network and motor imitation in children and adolescents with autism. Neuroscience 343:147–156. https://doi.org/10.1016/j.neuroscience.2016.12.001

    Article  CAS  Google Scholar 

  • Wechsler D (1997) Wechsler adult intelligence scale. Harcourt Assessment, San Antonio

    Google Scholar 

  • Wechsler D (1999) Wechsler abbreviated scale of intelligence. Harcourt Association, New York

    Google Scholar 

  • Wechsler D (2003) Wechsler intelligence scale for children. The Psychological Corporation, Toronto, ON

    Google Scholar 

  • Williams JHG (2008) Self-other relations in social development and autism: multiple roles for mirror neurons and other brain bases. Autism Res 1:73–90

    Article  Google Scholar 

  • Woolrich MW, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14(6):1370–1386. https://doi.org/10.1006/nimg.2001.0931

    Article  CAS  Google Scholar 

  • Worsley KJ, Liao CH, Aston J, Petre V, Duncan GH, Morales F, Evans AC (2002) A general statistical analysis for fMRI data. Neuroimage 15:1–15

    Article  CAS  Google Scholar 

  • Yamazaki Y, Yokochi H, Tanaka M, Okanoya K, Iriki A (2010) Potential role of monkey inferior parietal neurons coding action semantic equivalences as precursors of parts of speech. Soc Neurosci 5(1):105–117. https://doi.org/10.1080/17470910802625306

    Article  Google Scholar 

  • Zarr N, Ferguson R, Glenberg AM (2013) Language comprehension warps the mirror neuron system. Front Hum Neurosci 7:870. https://doi.org/10.3389/fnhum.2013.00870

    Article  Google Scholar 

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Acknowledgements

We extend our sincere gratitude to the children and families who participated in this study. This work was supported by the Louisiana Board of Regents—Research Competitiveness Subprogram [grant number LEQSF(2012-15)-RD-A-13].

Author information

Author notes

  1. Tracey A. Knaus

    Present address: Department of Psychology, University of New Orleans, New Orleans, LA, USA

  2. Anne L. Foundas

    Present address: The Brain Institute of Louisiana, New Orleans, USA

  3. Claire O. Burns

    Present address: Michael R. Boh Center for Child Development, Ochsner Hospital, New Orleans, LA, USA

Authors and Affiliations

  1. Brain and Behavior Program at Children’s Hospital, Department of Neurology, Louisiana State University Health Sciences Center—New Orleans, New Orleans, USA

    Tracey A. Knaus, Claire O. Burns & Anne L. Foundas

  2. Department of Psychology, Children’s Hospital and Department of Pediatrics, Louisiana State Univeristy Health Sciences Center, New Orleans, USA

    Jodi Kamps

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Contributions

Author contributions included conception and study design (TAK), subject recruitment (COB, TAK, and JK), clinical impression (JK), data collection or acquisition (TAK and COB), data processing and statistical analysis (TAK and COB), interpretation of results (TAK and ALF), drafting the manuscript work or revising it critically for important intellectual content (TAK, ALF, and JK) and approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (All authors).

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Correspondence to Tracey A. Knaus.

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The authors have no conflict of interest.

Ethical approval

This study was reviewed and approved by the Louisiana State University Health Sciences Center Institutional Review Board and the Children’s Hospital Institutional Review Board. All data collected were collected in compliance with these boards and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Parents and participants were informed of the procedures and parents gave written informed consent prior to the child’s participation in the study. Participants 13 years and older also provided written assent.

Consent to participate

Parents and participants were informed of all procedures. Parents provided written informed consent prior to the child’s participation in the study. All children 13 years and older also provided written assent.

Additional information

Communicated by Melvyn A. Goodale.

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Appendix

Appendix

Action viewing task stimuli used in fMRI

Action clip

Writing name

Putting coin in bank

Cutting pie with knife

Removing lid of box

Erasing dry-erase board

Watering plant

Salting food

Putting puzzle piece in

Stirring drink with spoon

Painting on paper

Stacking cups

Putting lid on box

Squeezing lemon in cup

Stapling papers

Pouring drink from teapot

Drawing with a marker

Shaking bottle

Pushing calculator buttons

Stacking blocks

Wiping table with cloth

Mixing in bowl

Cracking peanuts

Pushing toy car

Turning page of book

Squeezing ball

Hammering peg

Dialing phone

Moving checkers game pieces

Opening soft drink can

Dipping chip

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Knaus, T.A., Burns, C.O., Kamps, J. et al. Action viewing and language in adolescents with autism spectrum disorder. Exp Brain Res 241, 559–570 (2023). https://doi.org/10.1007/s00221-022-06540-2

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