Abstract
Examining brain and behaviour associations for language in autism spectrum disorder (ASD) may bring us closer to identifying neural profiles that are unique to a subgroup of individuals with ASD identified as language impaired (e.g. ASD LI+). We conducted a scoping review to examine brain regions that are associated with language performance in ASD. Further, we examined methodological differences across studies in how language ability was characterized and what neuroimaging methods were used to explore brain regions. Seventeen studies met inclusion criteria. Brain regions specific to ASD LI+ groups were found, however inconsistencies in brain and language associations were evident across study findings. Participant age, age-appropriate language scores, and neuroimaging methods likely contributed to differences in associations found.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Notes
For consistency, ASD LI + will be the acronym used to refer to individuals with ASD and co-occurring language impairment, and ASD LI- to refer to individuals with ASD and no co-occurring language impairment. The acronyms used by the original authors of included publications may differ.
References
Association, A. P. (Ed.). (2000). Diagnostic and statistical manual of mental disorders (4th ed.). American Psychiatric Association.
Association, A. P. (Ed.). (2013). Diagnostic and statistical manual of mental disorders: DSM-5 (5th ed.). American Psychiatric Association.
Anderson, J. S., Druzgal, T. J., Froehlich, A., DuBray, M. B., Lange, N., Alexander, A. L., et al. (2011). Decreased interhemispheric functional connectivity in autism. Cerebral Cortex, 21(5), 1134–1146. https://doi.org/10.1093/cercor/bhq190
Anderson, J. S., Lange, N., Froehlich, A., DuBray, M. B., Druzgal, T. J., Froimowitz, M. P., et al. (2010). Decreased left posterior insular activity during auditory language in autism. American Journal of Neuroradiology, 31(1), 131–139. https://doi.org/10.3174/ajnr.A1789
Arksey, H., & O’Malley, L. (2005). Scoping studies: Towards a methodological framework. International Journal of Social Research Methodology, 8(1), 19–32. https://doi.org/10.1080/1364557032000119616
Berman, J. I., Edgar, J. C., Blaskey, L., Kuschner, E. S., Levy, S. E., Ku, M., et al. (2016). Multimodal diffusion-MRI and MEG assessment of auditory and language system development in autism spectrum disorder. Frontiers in Neuroanatomy. https://doi.org/10.3389/fnana.2016.00030
Bigler, E. D., Mortensen, S., Neeley, E. S., Ozonoff, S., Krasny, L., Johnson, M., et al. (2007). Superior temporal gyrus, language function, and autism. Developmental Neuropsychology, 31(2), 217–238. https://doi.org/10.1080/87565640701190841
Bloom, L. (1980). Language development, language disorders, and learning disabilities: LD 3. Bulletin of the Orton Society, 30, 115–133.
Bloom, L., & Lahey, M. (1978). Language development and language disorders. Wiley.
Bretas, R. V., Taoka, M., Suzuki, H., & Iriki, A. (2020). Secondary somatosensory cortex of primates: Beyond body maps, toward conscious self-in-the-world maps. Experimental Brain Research, 238(2), 259–272. https://doi.org/10.1007/s00221-020-05727-9
Carrow-Woolfolk, E. (1995). Oral and written language scales (1st ed.). American Guidance Service.
Colquhoun, H. L., Levac, D., O’Brien, K. K., Straus, S., Tricco, A. C., Perrier, L., et al. (2014). Scoping reviews: Time for clarity in definition, methods, and reporting. Journal of Clinical Epidemiology, 67(12), 1291–1294. https://doi.org/10.1016/j.jclinepi.2014.03.013
De Fossé, L., Hodge, S. M., Makris, N., Kennedy, D. N., Caviness, V. S., McGrath, L., et al. (2004). Language-association cortex asymmetry in autism and specific language impairment. Annals of Neurology, 56(6), 757–766. https://doi.org/10.1002/ana.20275
Dollaghan, C., & Campbell, T. F. (1998). Nonword repetition and child language impairment. Journal of Speech, Language, and Hearing Research, 41(5), 1136–1146. https://doi.org/10.1044/jslhr.4105.1136
Durrleman, S., Hippolyte, L., Zufferey, S., Iglesias, K., & Hadjikhani, N. (2015). Complex syntax in autism spectrum disorders: A study of relative clauses. International Journal of Language & Communication Disorders, 50(2), 260–267. https://doi.org/10.1111/1460-6984.12130
Etchell, A., Adhikari, A., Weinberg, L. S., Choo, A. L., Garnett, E. O., Chow, H. M., & Chang, S.-E. (2018). A systematic literature review of sex differences in childhood language and brain development. Neuropsychologia, 114, 19–31. https://doi.org/10.1016/j.neuropsychologia.2018.04.011
Fletcher, P. T., Whitaker, R. T., Tao, R., DuBray, M. B., Froehlich, A., Ravichandran, C., et al. (2010). Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism. NeuroImage, 51(3), 1117–1125. https://doi.org/10.1016/j.neuroimage.2010.01.083
Gage, N. M., Juranek, J., Filipek, P. A., Osann, K., Flodman, P., Isenberg, A. L., & Spence, M. A. (2009). Rightward hemispheric asymmetries in auditory language cortex in children with autistic disorder: An MRI investigation. Journal of Neurodevelopmental Disorders, 1(3), 205–214. https://doi.org/10.1007/s11689-009-9010-2
Gao, Y., Linke, A., Jao Keehn, R. J., Punyamurthula, S., Jahedi, A., Gates, K., et al. (2019). The language network in autism: Atypical functional connectivity with default mode and visual regions. Autism Research, 12(9), 1344–1355. https://doi.org/10.1002/aur.2171
Gathercole, S. E., & Baddeley, A. D. (1990). Phonological memory deficits in language disordered children: Is there a causal connection? Journal of Memory and Language, 29(3), 336–360. https://doi.org/10.1016/0749-596X(90)90004-J
Groen, W., Zwiers, M., Vandergaag, R., & Buitelaar, J. (2008). The phenotype and neural correlates of language in autism: An integrative review. Neuroscience & Biobehavioral Reviews, 32(8), 1416–1425. https://doi.org/10.1016/j.neubiorev.2008.05.008
Herbert, M. R., Harris, G. J., Adrien, K. T., Ziegler, D. A., Makris, N., Kennedy, D. N., et al. (2002). Abnormal asymmetry in language association cortex in autism. Annals of Neurology, 52(5), 588–596. https://doi.org/10.1002/ana.10349
Herringshaw, A. J., Ammons, C. J., DeRamus, T. P., & Kana, R. K. (2016). Hemispheric differences in language processing in autism spectrum disorders: A meta-analysis of neuroimaging studies. Autism Research, 9(10), 1046–1057. https://doi.org/10.1002/aur.1599
Hodge, S. M., Makris, N., Kennedy, D. N., Caviness, V. S., Howard, J., McGrath, L., et al. (2010). Cerebellum, language, and cognition in autism and specific language impairment. Journal of Autism and Developmental Disorders, 40(3), 300–316. https://doi.org/10.1007/s10803-009-0872-7
Jao Keehn, R. J., Sanchez, S. S., Stewart, C. R., Zhao, W., Grenesko-Stevens, E. L., Keehn, B., & Müller, R.-A. (2017). Impaired downregulation of visual cortex during auditory processing is associated with autism symptomatology in children and adolescents with autism spectrum disorder. Autism Research, 10(1), 130–143. https://doi.org/10.1002/aur.1636
Joseph, R. M., Fricker, Z., Fenoglio, A., Lindgren, K. A., Knaus, T. A., & Tager-Flusberg, H. (2014). Structural asymmetries of language-related gray and white matter and their relationship to language function in young children with ASD. Brain Imaging and Behavior, 8(1), 60–72. https://doi.org/10.1007/s11682-013-9245-0
Kana, R. K., Keller, T. A., Cherkassky, V. L., Minshew, N. J., & Just, M. A. (2006). Sentence comprehension in autism: Thinking in pictures with decreased functional connectivity. Brain, 129(9), 2484–2493. https://doi.org/10.1093/brain/awl164
Kana, R. K., Sartin, E. B., Stevens, C., Deshpande, H. D., Klein, C., Klinger, M. R., & Klinger, L. G. (2017). Neural networks underlying language and social cognition during self-other processing in autism spectrum disorders. Neuropsychologia, 102, 116–123. https://doi.org/10.1016/j.neuropsychologia.2017.06.008
Kazak, S., Collis, G. M., & Lewis, V. (1997). Can young people with autism refer to knowledge states? Evidence from their understanding of “know” and “guess.” Journal of Child Psychology and Psychiatry, 38(8), 1001–1009. https://doi.org/10.1111/j.1469-7610.1997.tb01617.x
Kelley, E., Paul, J. J., Fein, D., & Naigles, L. R. (2006). Residual language deficits in optimal outcome children with a history of autism. Journal of Autism and Developmental Disorders, 36(6), 807. https://doi.org/10.1007/s10803-006-0111-4
Kjelgaard, M. M., & Tager-Flusberg, H. (2001). An investigation of language impairment in autism: Implications for genetic subgroups. Language and Cognitive Processes, 16(2–3), 287–308. https://doi.org/10.1080/01690960042000058
Knaus, T. A., Burns, C., Kamps, J., & Foundas, A. L. (2017). Atypical activation of action-semantic network in adolescents with autism spectrum disorder. Brain and Cognition, 117, 57–64. https://doi.org/10.1016/j.bandc.2017.06.004
Knaus, T. A., Silver, A. M., Dominick, K. C., Schuring, M. D., Shaffer, N., Lindgren, K. A., et al. (2009). Age-related changes in the anatomy of language regions in autism spectrum disorder. Brain Imaging and Behavior, 3(1), 51–63. https://doi.org/10.1007/s11682-008-9048-x
Knaus, T. A., Silver, A. M., Lindgren, K. A., Hadjikhani, N., & Tager-Flusberg, H. (2008). fMRI activation during a language task in adolescents with ASD. Journal of the International Neuropsychological Society, 14(6), 967–979. https://doi.org/10.1017/S1355617708081216
Knopf, A. (2020). Autism prevalence increases from 1 in 60 to 1 in 54: CDC. The Brown University Child & Adolescent Psychopharmacology Update, 22(6), 6–7. https://doi.org/10.1002/cpu.30499
Kort, W., Schittekatte, M., & Compaan, E. (2008). CELF-4-NL: Clinical evaluation of language fundamentals. Pearson Assessment and Information B.V.
Lange, N., Dubray, M. B., Lee, J. E., Froimowitz, M. P., Froehlich, A., Adluru, N., et al. (2010). Atypical diffusion tensor hemispheric asymmetry in autism. Autism Research: Official Journal of the International Society for Autism Research, 3(6), 350–358. https://doi.org/10.1002/aur.162
Leonard, L. B. (1998). Children with specific language impairment. The MIT Press.
Leonard, L. B., Ellis Weismer, S., Miller, C. A., Francis, D. J., Tomblin, J. B., & Kail, R. V. (2007). Speed of processing, working memory, and language impairment in children. Journal of Speech, Language, and Hearing Research, 50(2), 408–428. https://doi.org/10.1044/1092-4388(2007/029)
Levinson, S., Eisenhower, A., Bush, H. H., Carter, A. S., & Blacher, J. (2020). Brief report: Predicting social skills from semantic, syntactic, and pragmatic language among young children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 50(11), 4165–4175. https://doi.org/10.1007/s10803-020-04445-z
Lindell, A. K., & Hudry, K. (2013). Atypicalities in cortical structure, handedness, and functional lateralization for language in autism spectrum disorders. Neuropsychology Review, 23(3), 257–270. https://doi.org/10.1007/s11065-013-9234-5
Lombardo, M. V., Pierce, K., Eyler, L. T., Carter Barnes, C., Ahrens-Barbeau, C., Solso, S., et al. (2015). Different functional neural substrates for good and poor language outcome in autism. Neuron, 86(2), 567–577. https://doi.org/10.1016/j.neuron.2015.03.023
Mody, M., & Belliveau, J. W. (2012). Speech and language impairments in autism: Insights from behavior and neuroimaging. North American Journal of Medicine & Science, 5(3), 157. https://doi.org/10.7156/v5i3p157
Modyanova, N., Perovic, A., & Wexler, K. (2017). Grammar is differentially impaired in subgroups of autism spectrum disorders: Evidence from an investigation of tense marking and morphosyntax. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2017.00320
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group, T. P. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. PLOS Medicine, 6(7), e1000097. https://doi.org/10.1371/journal.pmed.1000097
Nagae, L. M., Zarnow, D. M., Blaskey, L., Dell, J., Khan, S. Y., Qasmieh, S., et al. (2012). Elevated mean diffusivity in the left hemisphere superior longitudinal fasciculus in autism spectrum disorders increases with more profound language impairment. American Journal of Neuroradiology, 33(9), 1720–1725. https://doi.org/10.3174/ajnr.A3037
Perovic, A., Modyanova, N., & Wexler, K. (2013). Comprehension of reflexive and personal pronouns in children with autism: A syntactic or pragmatic deficit? Applied Psycholinguistics, 34(4), 813–835. https://doi.org/10.1017/S0142716412000033
Ribeiro de Oliveira, L., Brian, J., Kelley, E., Beal, D., Nicolson, R., Georgiades, S., et al. (2020). Exploring the use of the verbal intelligence quotient as a proxy for language ability in autism spectrum disorder. Research in Autism Spectrum Disorders, 73, 101548. https://doi.org/10.1016/j.rasd.2020.101548
Riches, N. G., Loucas, T., Baird, G., Charman, T., & Simonoff, E. (2010). Sentence repetition in adolescents with specific language impairments and autism: an investigation of complex syntax. International Journal of Language & Communication Disorders, 45(1), 47–60. https://doi.org/10.3109/13682820802647676
Roberts, J. A., Rice, M. L., & Tager-Flusberg, H. (2004). Tense marking in children with autism. Applied Psycholinguistics, 25(3), 429–448. https://doi.org/10.1017/S0142716404001201
Roberts, T. P. L., Heiken, K., Zarnow, D., Dell, J., Nagae, L., Blaskey, L., et al. (2014). Left hemisphere diffusivity of the arcuate fasciculus: Influences of autism spectrum disorder and language impairment. American Journal of Neuroradiology, 35(3), 587–592. https://doi.org/10.3174/ajnr.A3754
Semel, E. M., Wiig, E. H., & Secord, W. (2003). Clinical evaluation of language fundamentals (CELF-4) (4th ed.). Psychological Corporation.
Semel, E. M., Wiig, E. H., & Secord, W. A. (1995). Clinical evaluation of language fundamentals (CELF-3) (3rd ed.). Psychological Corporation.
Sharda, M., Foster, N. E. V., Tryfon, A., Doyle-Thomas, K. A. R., Ouimet, T., Anagnostou, E., et al. (2017). Language ability predicts cortical structure and covariance in boys with autism spectrum disorder. Cerebral Cortex, 27(3), 1849–1862. https://doi.org/10.1093/cercor/bhw024
Soares, J. M., Marques, P., Alves, V., & Sousa, N. (2013). A hitchhiker’s guide to diffusion tensor imaging. Frontiers in Neuroscience. https://doi.org/10.3389/fnins.2013.00031
Tager-Flusberg, H. (2006). Defining language phenotypes in autism. Clinical Neuroscience Research, 6(3–4), 219–224. https://doi.org/10.1016/j.cnr.2006.06.007
Tomblin, J. B., & Zhang, X. (1999). Language patterns and etiology in children with specific language impairment. In H. Tager-Flusberg (Ed.), Neurodevelopmental disorders (pp. 361–382). The MIT Press.
Tryfon, A., Foster, N. E. V., Sharda, M., & Hyde, K. L. (2018). Speech perception in autism spectrum disorder: An activation likelihood estimation meta-analysis. Behavioural Brain Research, 338, 118–127. https://doi.org/10.1016/j.bbr.2017.10.025
Verhoeven, J. S., Rommel, N., Prodi, E., Leemans, A., Zink, I., Vandewalle, E., et al. (2012). Is there a common neuroanatomical substrate of language deficit between autism spectrum disorder and specific language impairment? Cerebral Cortex, 22(10), 2263–2271. https://doi.org/10.1093/cercor/bhr292
Veritas Health Innovation. (n.d.). Covidence systematic review software. Melbourne, VIC, Australia. covidence.org
Verly, M., Verhoeven, J., Zink, I., Mantini, D., Peeters, R., Deprez, S., et al. (2014). Altered functional connectivity of the language network in ASD: Role of classical language areas and cerebellum. NeuroImage: Clinical, 4, 374–382. https://doi.org/10.1016/j.nicl.2014.01.008
Verly, M., Verhoeven, J., Zink, I., Mantini, D., Van Oudenhove, L., Lagae, L., et al. (2014). Structural and functional underconnectivity as a negative predictor for language in autism. Human Brain Mapping, 35(8), 3602–3615. https://doi.org/10.1002/hbm.22424
Volden, J., Coolican, J., Garon, N., White, J., & Bryson, S. (2009). Brief report: Pragmatic language in autism spectrum disorder: Relationships to measures of ability and disability. Journal of Autism and Developmental Disorders, 39(2), 388–393. https://doi.org/10.1007/s10803-008-0618-y
Whyatt, C. P., & Torres, E. B. (2018). Autism research: An objective quantitative review of progress and focus between 1994 and 2015. Frontiers in Psychology, 9, 1526. https://doi.org/10.3389/fpsyg.2018.01526
Acknowledgments
We thank Erica Lenton for her assistance with the literature search.
Funding
The authors did not receive support from any organization for the submitted work.
Author information
Authors and Affiliations
Contributions
CC completed article screening (R1), wrote the paper and approved the final draft. SA completed article screening (R2) and assisted with revisions. LRO assisted with initial project conceptualization. DB, JB and EA conceptualized the project, provided critical review of the manuscript, and approved the final draft. AT assisted with revisions. TS resolved reviewer conflicts (R3) and contributed to multiple revisions of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cermak, C.A., Arshinoff, S., Ribeiro de Oliveira, L. et al. Brain and Language Associations in Autism Spectrum Disorder: A Scoping Review. J Autism Dev Disord 52, 725–737 (2022). https://doi.org/10.1007/s10803-021-04975-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-021-04975-0