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Overreactive Brain Responses to Sensory Stimuli in Youth With Autism Spectrum Disorders
Open accessAbstract
Objectives Sensory over-responsivity (SOR), defined as a negative response to or avoidance of sensory stimuli, is both highly prevalent and extremely impairing in youth with autism spectrum disorders (ASD), yet little is known about the neurological bases of SOR. This study aimed to examine the functional neural correlates of SOR by comparing brain responses to sensory stimuli in youth with and without ASD.Method A total of 25 high-functioning youth with ASD and 25 age- and IQ-equivalent typically developing (TD) youth were presented with mildly aversive auditory and visual stimuli during a functional magnetic resonance imaging (fMRI) scan. Parents provided ratings of children's SOR and anxiety symptom severity.Results Compared to TD participants, ASD participants displayed greater activation in primary sensory cortical areas as well as amygdala, hippocampus, and orbital-frontal cortex. In both groups, the level of activity in these areas was positively correlated with level of SOR severity as rated by parents, over and above behavioral ratings of anxiety.Conclusions This study demonstrates that youth with ASD show neural hyper-responsivity to sensory stimuli, and that behavioral symptoms of SOR may be related to both heightened responsivity in primary sensory regions as well as areas related to emotion processing and regulation.
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“Using simple sensory (auditory and visual) stimuli, Green et al. (2013) found increased activation in individuals with ASD in both primary sensory cortices as well as in the amygdala, hippocampus, and orbital-frontal cortex”
From Behavioral, Perceptual, and Neural Alterations in Sensory and Multisensory Function in Autism Spectrum Disorder (2015) · cites this paper as Green et al., 2013
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“Furthermore, the level of activity in these areas was positively correlated with sensory over-responsivity scores and behavioral anxiety ratings.”
From Behavioral, Perceptual, and Neural Alterations in Sensory and Multisensory Function in Autism Spectrum Disorder (2015) · cites this paper as Green et al., 2013
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“The elevation of oxidative stress in the cortex might also be involved in anxiety [28], and social recognition [26].”
Reduced intrinsic neural timescales in schizophrenia along posterior parietal and occipital areas
Uscătescu, L. C., Said‐Yürekli, S., Kronbichler, L., Stelzig-Schöler, R., Pearce, B.-G., Reich, L. A., Weber, S., Aichhorn, W., & Kronbichler, M. (2021) · Schizophrenia · doi:10.1038/s41537-021-00184-x · Cited by 33
Haigh, S. M., Gupta, A., Barb, S. M., Glass, S. A. F., Minshew, N. J., Dinstein, I., Heeger, D. J., Eack, S. M., & Behrmann, M. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.03.036 · Cited by 40
Circuit-level theories for sensory dysfunction in autism: convergence across mouse models
Monday, H. R., Wang, H. C., & Feldman, D. E. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1254297 · Cited by 31
“fMRI findings include hyperactivation by visual and auditory stimuli, which may relate to behavioral hypersensitivity (28), abnormal somatosensory maps, and decreased habituation in the somatosensory cortex to mildly aversive tactile stimuli (29).”
BackgroundMatsushima, K., Matsubayashi, J., Toichi, M., Funabiki, Y., Kato, T., Awaya, T., & Kato, T. (2016) · Research in Autism · doi:10.1016/j.rasd.2015.12.006 · Cited by 37
The neurobiological presentation of anxiety in autism spectrum disorder: A systematic review
McVey, A. J. (2019) · Autism Research · doi:10.1002/aur.2063 · Cited by 32
“behaviors may play a role in the link between anxiety and brain activity in autism [Green et al., 2015; Green et al., 2013; Yang et al., 2017].”
BackgroundResultInfluentialWilliams, Z. J., Failla, M. D., Davis, S., Heflin, B. H., Okitondo, C. D., Moore, D., & Cascio, C. J. (2019) · Scientific Reports · doi:10.1038/s41598-019-49103-2 · Cited by 35
Schwarzlose, R. F., Tillman, R., Hoyniak, C. P., Luby, J. L., & Barch, D. M. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.09.004 · Cited by 38
Yuan, H.-L., Lai, C. Y. Y., Wong, M., Kwong, T. C., Choy, Y. S., Mung, S. W. Y., & Chan, C. C. H. (2022) · Children · doi:10.3390/children9101584 · Cited by 47
“In summary, the implications of these findings on interventions for people with ASD suggest that, instead of normalizing sensory processing, the focus should be on developing coping mechanisms for managing attention and emotional responses to stimuli [136,137].”
BackgroundGandawijaya, J., Bamford, R. A., Burbach, J. P. H., & Oguro‐Ando, A. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.611379 · Cited by 33
Sensory Processing Patterns and Fusiform Activity During Face Processing in Autism Spectrum Disorder
Kuno‐Fujita, A., Iwabuchi, T., Wakusawa, K., Ito, H., Suzuki, K., Shigetomi, A., Kosaka, H., Tsujii, M., & Tsuchiya, K. J. (2020) · Autism Research · doi:10.1002/aur.2283 · Cited by 30
Hernandez, L. M., Green, S. A., Lawrence, K. E., Inada, M., Liu, J., Bookheimer, S. Y., & Dapretto, M. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00343 · Cited by 29
“A growing body of neuroimaging research also suggests that children with ASD who have high levels of SOR display neural hyperresponsivity to aversive visual, tactile, and auditory stimuli in primary sensory brain regions and areas important for salience detection (31, 32), suggesting that there may be an overallocatio…”
BackgroundResultYoshimura, S., Sato, W., Kochiyama, T., Uono, S., Sawada, R., Kubota, Y., & Toichi, M. (2017) · Human Brain Mapping · doi:10.1002/hbm.23822 · Cited by 24
“Several related functional MRI studies assessed the relationship between individual differences in sensory processing and brain activity and identified the involvement of early (i.e., primary and secondary) sensory regions [Green et al., 2013; Shen et al., 2016].”
BackgroundAtypical Integration of Sensory-to-Transmodal Functional Systems Mediates Symptom Severity in Autism
Park, S., Haak, K. V., Cho, H. B., Valk, S. L., Bethlehem, R. A. I., Milham, M. P., Bernhardt, B. C., Martino, A. D., & Hong, S. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.699813 · Cited by 26
A multilevel investigation of sensory sensitivity and responsivity in autistic adults
Sapey‐Triomphe, L., Dierckx, J., Vettori, S., Overwalle, J. V., & Wagemans, J. P. (2023) · Autism Research · doi:10.1002/aur.2962 · Cited by 29
“Using fMRI, Green et al. (2013) showed greater activity in primary sensory area in response to aversive visual stimuli in autistic youth than in NT, interpreted as neural over-responsivity in ASD (yet, note that the mean amplitude of the mean fMRI response to nonaversive visual stimuli was typical…”
BackgroundNeurocircuitry of impaired affective sound processing: A clinical disorders perspective
Frühholz, S., & Staib, M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.009 · Cited by 24
Nanjappa, M. S., Voyiaziakis, E., Pradhan, B., & Thippaiah, S. M. (2020) · CNS Spectrums · doi:10.1017/s109285292000214x · Cited by 24
Gigliotti, F., Giovannone, F., Belli, A., & Sogos, C. (2024) · Children · doi:10.3390/children11070875 · Cited by 29
“These findings suggest atypical features of sensory processing in ASD at both a lower level (i.e., primary or association sensory cortex) and a higher level (i.e., attentional or limbic cortices) [38].”
BackgroundCortical signatures in behaviorally clustered autistic traits subgroups: a population-based study
Mihailov, A., Philippe, C., Gloaguen, A., Grigis, A., Laidi, C., Piguet, C., Houenou, J., & Frouin, V. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00894-3 · Cited by 29
Köse, S., Türer, F., Inal-Kaleli, I., Senturk, H. N. C., Uyar, D. H. O., & Bildik, T. (2023) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-023-06190-5 · Cited by 29
“Even though hypersensitivity to stimuli seems to influence social tasks in neuroimaging studies (Green et al., 2013, 2017), the results from our study implicate a more dynamic relationship between sensory integration and the end result of social behavior as hyposensitivity to social stimuli…”
Rausch, A., Zhang, W., Beckmann, C. F., Buitelaar, J. K., Groen, W. B., & Haak, K. V. (2017) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-017-3370-3 · Cited by 21
Wagner, L., Banchik, M., Okada, N. J., McDonald, N. M., Jeste, S., Bookheimer, S. Y., Green, S. A., & Dapretto, M. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad100 · Cited by 24
Cummings, K. K., Jung, J., Zbozinek, T. D., Wilhelm, F. H., Dapretto, M., Craske, M. G., Bookheimer, S. Y., & Green, S. A. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25250 · Cited by 24
“…brain responses to sensory stimulation, but that SOR would be more strongly and uniquely correlated with brain responses to sensory stimulation in the ASD group, given prior evidence of neural hyperresponsivity in this group above and beyond the effects of anxiety (Green et al., 2013, 2015, 2019).”
InfluentialSolders, S. K., Carper, R. A., & Müller, R. (2017) · Autism Research · doi:10.1002/aur.1807 · Cited by 21
“…and auditory stimuli [Barbas & De Olmos, 1990; Ghashghaei & Barbas, 2002; Schmahmann & Pandya, 2006; Von Der Heide, Skipper, Klobusicky, & Olson, 2013; Oishi et al., 2015], which may be impaired in ASD [Green et al., 2013; Blasi et al., 2015; Kana, Patriquin, Black, Channell, & Wicker, 2016].”
Neural Correlates of Sensory Abnormalities Across Developmental Disabilities
Cardon, G. J. (2018) · International review of research in developmental disabilities · doi:10.1016/bs.irrdd.2018.08.001 · Cited by 20
“For example, Dougherty found DTI similarities between those with ASD and ADHD.”
BackgroundResultInfluentialIsaiah, S., Loots, D. T., Solomons, R., van der Kuip, M., van Furth, A. M., & Mason, S. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00296 · Cited by 20
Alhowikan, A. M. (2016) · Medical Principles and Practice · doi:10.1159/000445351 · Cited by 19
Zhao, Y., Du, M., Gao, X., Xiao, Y., Shah, C., Sun, H., Chen, F., Yang, L., Yan, Z., Fu, Y., et al. (2016) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2016.10.013 · Cited by 17
Anxiety in autistic preschool children: Phenomenology and a network analysis of correlates
Vasa, R. A., Kerns, C. M., Singh, V., McDonald, R. G., Jang, Y. S., & Keefer, A. J. (2023) · Autism Research · doi:10.1002/aur.2968 · Cited by 16
“, amygdalabased circuits) overlap with those mediating uncertainty and sensory responses (Green et al., 2013; Tanovic et al., 2018).”
BackgroundFard, Y. A., Sadeghi, E. N., Pajoohesh, Z., Gharehdaghi, Z., Khatibi, D. M., Khosravifar, S., Pishkari, Y., Nozari, S., Hijazi, A., Pakmehr, S., et al. (2024) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32986 · Cited by 16
“…hold clinical significance, as heightened activity in primary sensory areas, alongside regions involved in emotion processing and regulation like the amygdala and orbital-frontal cortex, correlates positively with the severity of sensory over-responsivity (SOR) symptoms in ASD (Green et al., 2013).”
Dong, Y., Batallé, D., & Deprez, M. (2025) · Human Brain Mapping · doi:10.1002/hbm.70190 · Cited by 21
Wei, S., Wu, C., Yu, B., Ma, M., Qin, F., & Yuan, J. (2020) · Translational Andrology and Urology · doi:10.21037/tau.2019.12.08 · Cited by 15
“Also, it was reported that anxiety affects patient’s ejaculation, as well as their perception sensitivity (58,59).”
BackgroundMcCormack, L., Wong, S. W., & Campbell, L. E. (2023) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-022-05644-6 · Cited by 15
Metadata
- Authors
- Green, S. A., Rudie, J. D., Colich, N. L., Wood, J. J., Shirinyan, D., Hernandez, L., Tottenham, N., Dapretto, M., & Bookheimer, S. Y.
- Affiliations
- University of California, Los Angeles (US)
- Stanford University (US)
- Santa Monica College (US)
- Corresponding author
- Green, Shulamite A.
- ORCID
- Venue
- Journal of the American Academy of Child & Adolescent Psychiatry
- Publisher
- Elsevier BV
- Published
- 2013-11
- Volume
- 52
- Issue
- 11
- Pages
- 1158-1172
- ISSN
- 0890-8567 (ISSN-L)
- PMC
- PMC3820504
- OpenAlex
- W2091176864
- Cited by
- 207
- References
- 51
- Citations by year
- 2026: 15 · 2025: 11 · 2024: 19 · 2023: 17 · 2022: 13 · 2021: 19 · 2020: 19 · 2019: 18 · 2018: 8 · 2017: 25 · 2016: 17 · 2015: 14 · 2014: 9
- FWCI
- 7.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of the American Academy of Child & Adolescent Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (F31MH093999, HD055784)
- National Institute of General Medical Sciences (T32GM008042)
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50HD055784, R01HD065280)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Health Sciences › Medicine › Psychiatry and Mental health › Child Nutrition and Feeding Issues
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- sensory hypersensitivity, autism spectrum disorder, sensory processing, amygdala, hippocampus, orbitofrontal cortex, primary sensory cortex, anxiety, emotion regulation
- MeSH terms
- Adolescent, Amygdala, Anxiety, Cerebral Cortex, Child, Child Development Disorders, Pervasive, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Perceptual Disorders, Psychiatric Status Rating Scales, Sensation Disorders, Severity of Illness Index, Prefrontal Cortex, Functional Neuroimaging
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