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Functional brain abnormalities associated with comorbid anxiety in autism spectrum disorder

Published online by Cambridge University Press:  09 November 2020

James Bartolotti
Affiliation:
Schiefelbusch Institute for Life Span Studies, University of Kansas, Lawrence, KS, USA Kansas Center for Autism Research and Training, University of Kansas Medical School, Kansas City, KS, USA
John A. Sweeney
Affiliation:
Department of Psychiatry, University of Cincinnati, Cincinnati, OH, USA
Matthew W. Mosconi*
Affiliation:
Schiefelbusch Institute for Life Span Studies, University of Kansas, Lawrence, KS, USA Kansas Center for Autism Research and Training, University of Kansas Medical School, Kansas City, KS, USA Clinical Child Psychology Program, University of Kansas, Lawrence, KS, USA
*
Author for Correspondence: Dr Matthew W. Mosconi, Life Span Institute, Kansas Center for Autism Research and Training (K-CART), Clinical Child Psychology Program, University of Kansas, 1000 Sunnyside Ave., Lawrence, KS, 66045, USA. E-mail: mosconi@ku.edu.

Abstract

Anxiety disorders are common in autism spectrum disorder (ASD) and associated with social–communication impairment and repetitive behavior symptoms. The neurobiology of anxiety in ASD is unknown, but amygdala dysfunction has been implicated in both ASD and anxiety disorders. Using resting-state functional magnetic resonance imaging, we compared amygdala–prefrontal and amygdala–striatal connections across three demographically matched groups studied in the Autism Brain Imaging Data Exchange (ABIDE): ASD with a comorbid anxiety disorder (N = 25; ASD + Anxiety), ASD without a comorbid disorder (N = 68; ASD-NoAnx), and typically developing controls (N = 139; TD). Relative to ASD-NoAnx and TD controls, ASD + Anxiety individuals had decreased connectivity between the amygdala and dorsal/rostral anterior cingulate cortex (dACC/rACC). The functional connectivity of these connections was not affected in ASD-NoAnx, and amygdala connectivity with ventral ACC/medial prefrontal cortex (mPFC) circuits was not different in ASD + Anxiety or ASD-NoAnx relative to TD. Decreased amygdala–dorsomedial prefrontal cortex (dmPFC)/rACC connectivity was associated with more severe social impairment in ASD + Anxiety; amygdala–striatal connectivity was associated with restricted, repetitive behavior (RRB) symptom severity in ASD-NoAnx individuals. These findings suggest comorbid anxiety in ASD is associated with disrupted emotion-monitoring processes supported by amygdala–dACC/mPFC pathways, whereas emotion regulation systems involving amygdala–ventromedial prefrontal cortex (vmPFC) are relatively spared. Our results highlight the importance of accounting for comorbid anxiety for parsing ASD neurobiological heterogeneity.

Type
Special Section Articles
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abbott, A. E., Linke, A. C., Nair, A., Jahedi, A., Alba, L. A., Keown, C. L., … Müller, R.-A. (2018). Repetitive behaviors in autism are linked to imbalance of corticostriatal connectivity: A functional connectivity MRI study. Social Cognitive and Affective Neuroscience, 13, 3242. https://doi.org/10.1093/scan/nsx129CrossRefGoogle ScholarPubMed
Abraham, A., Milham, M. P., Di Martino, A., Craddock, R. C., Samaras, D., Thirion, B., & Varoquaux, G. (2017). Deriving reproducible biomarkers from multi-site resting-state data: An autism-based example. NeuroImage, 147, 736745. https://doi.org/10.1016/j.neuroimage.2016.10.045CrossRefGoogle ScholarPubMed
Adam, Y., Meinlschmidt, G., Gloster, A. T., & Lieb, R. (2012). Obsessive–compulsive disorder in the community: 12-month prevalence, comorbidity and impairment. Social Psychiatry and Psychiatric Epidemiology, 47, 339349. https://doi.org/10.1007/s00127-010-0337-5CrossRefGoogle ScholarPubMed
Agam, Y., Joseph, R. M., Barton, J. J. S., & Manoach, D. S. (2010). Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders. Neuroimage, 52, 336347. https://doi.org/10.1016/j.neuroimage.2010.04.010CrossRefGoogle ScholarPubMed
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., … Zilles, K. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anatomy and Embryology, 210, 343352. https://doi.org/10.1007/s00429-005-0025-5CrossRefGoogle ScholarPubMed
Avants, B. B., Tustison, N. J., Stauffer, M., Song, G., Wu, B., & Gee, J. C. (2014). The Insight ToolKit image registration framework. Frontiers in Neuroinformatics, 8, 113. https://doi.org/10.3389/fninf.2014.00044CrossRefGoogle ScholarPubMed
Barker, H., Munro, J., Orlov, N., Morgenroth, E., Moser, J., Eysenck, M. W., & Allen, P. (2018). Worry is associated with inefficient functional activity and connectivity in prefrontal and cingulate cortices during emotional interference. Brain and Behavior, 8, e01137. https://doi.org/10.1002/brb3.1137CrossRefGoogle ScholarPubMed
Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. R. (2000). The amygdala theory of autism. Neuroscience & Biobehavioral Reviews, 24, 355364. https://doi.org/10.1016/S0149-7634(00)00011-7CrossRefGoogle ScholarPubMed
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 148. https://doi.org/10.18637/jss.v067.i01.CrossRefGoogle Scholar
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37, 90101. https://doi.org/10.1016/j.neuroimage.2007.04.042CrossRefGoogle ScholarPubMed
Blackford, J. U., & Pine, D. S. (2012). Neural substrates of childhood anxiety disorders. Child and Adolescent Psychiatric Clinics of North America, 21, 501525. https://doi.org/10.1016/j.chc.2012.05.002CrossRefGoogle ScholarPubMed
Cashin, A., & Yorke, J. (2018). The relationship between anxiety, external structure, behavioral history and becoming locked into restricted and repetitive behaviors in autism spectrum disorder. Issues in Mental Health Nursing, 39, 533537. https://doi.org/10.1080/01612840.2017.1418035CrossRefGoogle ScholarPubMed
Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012). The social motivation theory of autism. Trends in Cognitive Sciences, 16, 231239. https://doi.org/10.1016/j.tics.2012.02.007CrossRefGoogle ScholarPubMed
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162173. https://doi.org/10.1006/cbmr.1996.0014CrossRefGoogle ScholarPubMed
Craddock, R. C., James, G. A., Holtzheimer, P. E., Hu, X. P., & Mayberg, H. S. (2012). A whole brain fMRI atlas generated via spatially constrained spectral clustering. Human Brain Mapping, 33, 19141928. https://doi.org/10.1002/hbm.21333CrossRefGoogle ScholarPubMed
D'Cruz, A.-M., Mosconi, M. W., Ragozzino, M. E., Cook, E. H., & Sweeney, J. A. (2016). Alterations in the functional neural circuitry supporting flexible choice behavior in autism spectrum disorders. Translational Psychiatry, 6, e916e916. https://doi.org/10.1038/tp.2016.161CrossRefGoogle ScholarPubMed
Delmonte, S., Balsters, J. H., McGrath, J., Fitzgerald, J., Brennan, S., Fagan, A. J., & Gallagher, L. (2012). Social and monetary reward processing in autism spectrum disorders. Molecular Autism, 3, 7. https://doi.org/10.1186/2040-2392-3-7CrossRefGoogle ScholarPubMed
Delmonte, S., Gallagher, L., O'Hanlon, E., McGrath, J., & Balsters, J. H. (2013). Functional and structural connectivity of frontostriatal circuitry in autism spectrum disorder. Frontiers in Human Neuroscience, 7, 430. https://doi.org/10.3389/fnhum.2013.00430.CrossRefGoogle ScholarPubMed
Di Martino, A., O'Connor, D., Chen, B., Alaerts, K., Anderson, J. S., Assaf, M., … Milham, M. P. (2017). Enhancing studies of the connectome in autism using the Autism Brain Imaging Data Exchange II. Scientific Data, 4, 170010. https://doi.org/10.1038/sdata.2017.10CrossRefGoogle ScholarPubMed
Di Martino, A., Yan, C.-G., Li, Q., Denio, E., Castellanos, F. X., Alaerts, K., … Milham, M. P. (2014). The Autism Brain Imaging Data Exchange: Towards a large-scale evaluation of the intrinsic brain architecture in autism. Molecular Psychiatry, 19, 659667. https://doi.org/10.1038/mp.2013.78CrossRefGoogle ScholarPubMed
Duvekot, J., Ende, J., Verhulst, F. C., & Greaves-Lord, K. (2018). Examining bidirectional effects between the autism spectrum disorder (ASD) core symptom domains and anxiety in children with ASD. Journal of Child Psychology and Psychiatry, 59, 277284. https://doi.org/10.1111/jcpp.12829CrossRefGoogle ScholarPubMed
Esbensen, A. J., Seltzer, M. M., Lam, K. S. L., & Bodfish, J. W. (2009). Age-related differences in restricted repetitive behaviors in autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 5766. https://doi.org/10.1007/s10803-008-0599-xCrossRefGoogle ScholarPubMed
Etkin, A. (2009). Functional neuroanatomy of anxiety: A neural circuit perspective. In Stein, M. B. & Steckler, T. (Eds.), Behavioral neurobiology of anxiety and its treatment (Vol. 2, pp. 251277). Berlin: Springer.CrossRefGoogle Scholar
Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., & Hirsch, J. (2006). Resolving emotional conflict: A role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron, 51, 871882. https://doi.org/10.1016/j.neuron.2006.07.029CrossRefGoogle ScholarPubMed
Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D. (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Archives of General Psychiatry, 66, 1361. https://doi.org/10.1001/archgenpsychiatry.2009.104CrossRefGoogle ScholarPubMed
Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164, 14761488. https://doi.org/10.1176/appi.ajp.2007.07030504CrossRefGoogle ScholarPubMed
Faria, V., Åhs, F., Appel, L., Linnman, C., Bani, M., Bettica, P., … Furmark, T. (2014). Amygdala-frontal couplings characterizing SSRI and placebo response in social anxiety disorder. The International Journal of Neuropsychopharmacology, 17, 11491157. https://doi.org/10.1017/S1461145714000352CrossRefGoogle ScholarPubMed
Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences, 102, 96739678. https://doi.org/10.1073/pnas.0504136102CrossRefGoogle ScholarPubMed
Gelman, A. (2008). Scaling regression inputs by dividing by two standard deviations. Statistics in Medicine, 27, 28652873. https://doi.org/10.1002/sim.3107CrossRefGoogle ScholarPubMed
Goodwin, G. M. (2015). The overlap between anxiety, depression, and obsessive-compulsive disorder. Dialogues in Clinical Neuroscience, 17, 12.Google ScholarPubMed
Gotham, K., Bishop, S. L., Hus, V., Huerta, M., Lund, S., Buja, A., … Lord, C. (2013). Exploring the relationship between anxiety and insistence on sameness in autism spectrum disorders: Anxiety and insistence on sameness in ASD. Autism Research, 6, 3341. https://doi.org/10.1002/aur.1263CrossRefGoogle Scholar
Göttlich, M., Krämer, U. M., Kordon, A., Hohagen, F., & Zurowski, B. (2014). Decreased limbic and increased fronto-parietal connectivity in unmedicated patients with obsessive-compulsive disorder: Altered brain networks in OCD. Human Brain Mapping, 35, 56175632. https://doi.org/10.1002/hbm.22574CrossRefGoogle Scholar
Iidaka, T., Kogata, T., Mano, Y., & Komeda, H. (2019). Thalamocortical hyperconnectivity and amygdala-cortical hypoconnectivity in male patients with autism spectrum disorder. Frontiers in Psychiatry, 10, 252. https://doi.org/10.3389/fpsyt.2019.00252CrossRefGoogle ScholarPubMed
Indovina, I., Robbins, T. W., Núñez-Elizalde, A. O., Dunn, B. D., & Bishop, S. J. (2011). Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron, 69, 563571. https://doi.org/10.1016/j.neuron.2010.12.034CrossRefGoogle ScholarPubMed
Jalbrzikowski, M., Larsen, B., Hallquist, M. N., Foran, W., Calabro, F., & Luna, B. (2017). Development of white matter microstructure and intrinsic functional connectivity between the amygdala and ventromedial prefrontal cortex: Associations with anxiety and depression. Biological Psychiatry, 82, 511521. https://doi.org/10.1016/j.biopsych.2017.01.008CrossRefGoogle ScholarPubMed
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62, 782790. https://doi.org/10.1016/j.neuroimage.2011.09.015CrossRefGoogle ScholarPubMed
Kerns, C. M., Renno, P., Kendall, P. C., Wood, J. J., & Storch, E. A. (2017). Anxiety disorders interview schedule–autism addendum: Reliability and validity in children with autism spectrum disorder. Journal of Clinical Child & Adolescent Psychology, 46, 88100. https://doi.org/10.1080/15374416.2016.1233501CrossRefGoogle ScholarPubMed
Kessler, K., Seymour, R. A., & Rippon, G. (2016). Brain oscillations and connectivity in autism spectrum disorders (ASD): New approaches to methodology, measurement and modelling. Neuroscience & Biobehavioral Reviews, 71, 601620. https://doi.org/10.1016/j.neubiorev.2016.10.002CrossRefGoogle ScholarPubMed
Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011). The structural and functional connectivity of the amygdala: From normal emotion to pathological anxiety. Behavioural Brain Research, 223, 403410. https://doi.org/10.1016/j.bbr.2011.04.025CrossRefGoogle ScholarPubMed
Kim, M. J., & Whalen, P. J. (2009). The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. Journal of Neuroscience, 29, 1161411618. https://doi.org/10.1523/jneurosci.2335-09.2009CrossRefGoogle ScholarPubMed
King, B. H., Hollander, E., Sikich, L., McCracken, J. T., Scahill, L., Bregman, J. D., … Ritz, L. (2009). Lack of efficacy of citalopram in children with autism spectrum disorders and high levels of repetitive behavior: Citalopram ineffective in children with autism. Archives of General Psychiatry, 66, 583. https://doi.org/10.1001/archgenpsychiatry.2009.30CrossRefGoogle ScholarPubMed
King, J. B., Prigge, M. B. D., King, C. K., Morgan, J., Weathersby, F., Fox, J. C., … Anderson, J. S. (2019). Generalizability and reproducibility of functional connectivity in autism. Molecular Autism, 10, 123. https://doi.org/10.1186/s13229-019-0273-5CrossRefGoogle ScholarPubMed
Kleinhans, N. M., Reiter, M. A., Neuhaus, E., Pauley, G., Martin, N., Dager, S., & Estes, A. (2016). Subregional differences in intrinsic amygdala hyperconnectivity and hypoconnectivity in autism spectrum disorder: Subregional amygdala connectivity in autism. Autism Research, 9, 760772. https://doi.org/10.1002/aur.1589CrossRefGoogle ScholarPubMed
Lago, T., Davis, A., Grillon, C., & Ernst, M. (2017). Striatum on the anxiety map: Small detours into adolescence. Brain Research, 1654, 177184. https://doi.org/10.1016/j.brainres.2016.06.006CrossRefGoogle ScholarPubMed
Lai, M.-C., Kassee, C., Besney, R., Bonato, S., Hull, L., Mandy, W., … Ameis, S. H. (2019). Prevalence of co-occurring mental health diagnoses in the autism population: A systematic review and meta-analysis. The Lancet Psychiatry, 6, 819829. https://doi.org/10.1016/S2215-0366(19)30289-5CrossRefGoogle ScholarPubMed
Langen, M., Bos, D., Noordermeer, S. D. S., Nederveen, H., van Engeland, H., & Durston, S. (2014). Changes in the development of striatum are involved in repetitive behavior in autism. Biological Psychiatry, 76, 405411. https://doi.org/10.1016/j.biopsych.2013.08.013CrossRefGoogle ScholarPubMed
Lenth, R., Signmann, H., Love, J., Buerkner, P., & Herve, M. (2019). Emmeans (1.4.1, R package). https://CRAN.R-project.org/package=emmeansGoogle Scholar
Linke, A. C., Olson, L., Gao, Y., Fishman, I., & Müller, R.-A. (2017). Psychotropic medication use in autism spectrum disorders may affect functional brain connectivity. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2, 518527. https://doi.org/10.1016/j.bpsc.2017.06.008Google ScholarPubMed
Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview—Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659685. doi:10.1007/BF02172145CrossRefGoogle ScholarPubMed
Lüdecke, D. (2019). sjPlot: Data visualization for statistics in social science. https://doi.org/10.5281/zenodo.1308157CrossRefGoogle Scholar
Makovac, E., Meeten, F., Watson, D. R., Herman, A., Garfinkel, S. N., Critchley, H. D., & Ottaviani, C. (2016). Alterations in amygdala-prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biological Psychiatry, 80, 786795. https://doi.org/10.1016/j.biopsych.2015.10.013CrossRefGoogle ScholarPubMed
Mosconi, M. W., Cody-Hazlett, H., Poe, M. D., Gerig, G., Gimpel-Smith, R., & Piven, J. (2009a). Longitudinal study of amygdala volume and joint attention in 2- to 4-year-old children with autism. Archives of General Psychiatry, 66, 509. https://doi.org/10.1001/archgenpsychiatry.2009.19CrossRefGoogle Scholar
Mosconi, M. W., Kay, M., D'Cruz, A.-M., Seidenfeld, A., Guter, S., Stanford, L. D., & Sweeney, J. A. (2009b). Impaired inhibitory control is associated with higher-order repetitive behaviors in autism spectrum disorders. Psychological Medicine, 39, 1559. https://doi.org/10.1017/S0033291708004984CrossRefGoogle Scholar
Motzkin, J. C., Philippi, C. L., Wolf, R. C., Baskaya, M. K., & Koenigs, M. (2015). Ventromedial prefrontal cortex is critical for the regulation of amygdala activity in humans. Biological Psychiatry, 77, 276284. https://doi.org/10.1016/j.biopsych.2014.02.014CrossRefGoogle ScholarPubMed
Müller, R.-A. (2007). The study of autism as a distributed disorder. Mental Retardation and Developmental Disabilities Research Reviews, 13, 8595. https://doi.org/10.1002/mrdd.20141CrossRefGoogle Scholar
Müller, R.-A., Shih, P., Keehn, B., Deyoe, J. R., Leyden, K. M., & Shukla, D. K. (2011). Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. Cerebral Cortex, 21, 22332243. https://doi.org/10.1093/cercor/bhq296CrossRefGoogle ScholarPubMed
Murphy, E. R., Foss-Feig, J., Kenworthy, L., Gaillard, W. D., & Vaidya, C. J. (2012). Atypical functional connectivity of the amygdala in childhood autism spectrum disorders during spontaneous attention to eye-gaze. Autism Research and Treatment, 2012, 112. https://doi.org/10.1155/2012/652408CrossRefGoogle ScholarPubMed
Murphy, K., & Fox, M. D. (2017). Towards a consensus regarding global signal regression for resting state functional connectivity MRI. NeuroImage, 154, 169173. https://doi.org/10.1016/j.neuroimage.2016.11.052CrossRefGoogle ScholarPubMed
Nair, A., Keown, C. L., Datko, M., Shih, P., Keehn, B., & Müller, R.-A. (2014). Impact of methodological variables on functional connectivity findings in autism spectrum disorders: FcMRI methods in autism. Human Brain Mapping, 35, 40354048. https://doi.org/10.1002/hbm.22456CrossRefGoogle ScholarPubMed
Nordahl, C. W. (2012). Increased rate of amygdala growth in children aged 2 to 4 years with autism spectrum disorders: A longitudinal study. Archives of General Psychiatry, 69, 53. https://doi.org/10.1001/archgenpsychiatry.2011.145CrossRefGoogle ScholarPubMed
Odriozola, P., Dajani, D. R., Burrows, C. A., Gabard-Durnam, L. J., Goodman, E., Baez, A. C., … Gee, D. G. (2019). Atypical frontoamygdala functional connectivity in youth with autism. Developmental Cognitive Neuroscience, 37, 100603. https://doi.org/10.1016/j.dcn.2018.12.001CrossRefGoogle ScholarPubMed
Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004). Extinction learning in humans: Role of the amygdala and vmPFC. Neuron, 43, 897905. https://doi.org/10.1016/j.neuron.2004.08.042CrossRefGoogle ScholarPubMed
Picci, G., Gotts, S. J., & Scherf, K. S. (2016). A theoretical rut: Revisiting and critically evaluating the generalized under/over-connectivity hypothesis of autism. Developmental Science, 19, 524549. https://doi.org/10.1111/desc.12467CrossRefGoogle ScholarPubMed
Plitt, M., Barnes, K. A., Wallace, G. L., Kenworthy, L., & Martin, A. (2015). Resting-state functional connectivity predicts longitudinal change in autistic traits and adaptive functioning in autism. Proceedings of the National Academy of Sciences, 112, E6699E6706. https://doi.org/10.1073/pnas.1510098112CrossRefGoogle ScholarPubMed
Polanczyk, G. V., Salum, G. A., Sugaya, L. S., Caye, A., & Rohde, L. A. (2015). Annual research review: A meta-analysis of the worldwide prevalence of mental disorders in children and adolescents. Journal of Child Psychology and Psychiatry, 56, 345365. https://doi.org/10.1111/jcpp.12381CrossRefGoogle ScholarPubMed
Qin, S., Young, C. B., Duan, X., Chen, T., Supekar, K., & Menon, V. (2014). Amygdala subregional structure and intrinsic functional connectivity predicts individual differences in anxiety during early childhood. Biological Psychiatry, 75, 892900. https://doi.org/10.1016/j.biopsych.2013.10.006CrossRefGoogle ScholarPubMed
Rausch, A., Zhang, W., Beckmann, C. F., Buitelaar, J. K., Groen, W. B., & Haak, K. V. (2018). Connectivity-based parcellation of the amygdala predicts social skills in adolescents with autism spectrum disorder. Journal of Autism and Developmental Disorders, 48, 572582. https://doi.org/10.1007/s10803-017-3370-3CrossRefGoogle ScholarPubMed
Rausch, A., Zhang, W., Haak, K. V., Mennes, M., Hermans, E. J., van Oort, E., … Groen, W. B. (2016). Altered functional connectivity of the amygdaloid input nuclei in adolescents and young adults with autism spectrum disorder: A resting state fMRI study. Molecular Autism, 7. https://doi.org/10.1186/s13229-015-0060-xCrossRefGoogle Scholar
R Core Team. (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.orgGoogle Scholar
Rodgers, J., Glod, M., Connolly, B., & McConachie, H. (2012). The relationship between anxiety and repetitive behaviours in autism spectrum disorder. Journal of Autism and Developmental Disorders, 42, 24042409. https://doi.org/10.1007/s10803-012-1531-yCrossRefGoogle ScholarPubMed
Rodgers, J., Wigham, S., McConachie, H., Freeston, M., Honey, E., & Parr, J. R. (2016). Development of the anxiety scale for children with autism spectrum disorder (ASC-ASD): Measuring anxiety in ASD. Autism Research, 9, 12051215. https://doi.org/10.1002/aur.1603CrossRefGoogle Scholar
Roy, A. K., Fudge, J. L., Kelly, C., Perry, J. S. A., Daniele, T., Carlisi, C., … Ernst, M. (2013). Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 290299.e2. https://doi.org/10.1016/j.jaac.2012.12.010CrossRefGoogle ScholarPubMed
Scahill, L., Lecavalier, L., Schultz, R. T., Evans, A. N., Maddox, B., Pritchett, J., … Edwards, M. C. (2019). Development of the parent-rated anxiety scale for youth with autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 58(9), 887896. https://doi.org/10.1016/j.jaac.2018.10.016.CrossRefGoogle ScholarPubMed
Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. Journal of Neuroscience, 26, 76747679. https://doi.org/10.1523/JNEUROSCI.1285-06.2006CrossRefGoogle ScholarPubMed
Selles, R. R., Arnold, E. B., Phares, V., Lewin, A. B., Murphy, T. K., & Storch, E. A. (2015). Cognitive-behavioral therapy for anxiety in youth with an autism spectrum disorder: A follow-up study. Autism, 19, 613621. https://doi.org/10.1177/1362361314537912CrossRefGoogle ScholarPubMed
Shen, M. D., Li, D. D., Keown, C. L., Lee, A., Johnson, R. T., Angkustsiri, K., … Nordahl, C. W. (2016). Functional connectivity of the amygdala is disrupted in preschool-aged children with autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 55, 817824. https://doi.org/10.1016/j.jaac.2016.05.020CrossRefGoogle ScholarPubMed
Simmons, A., Matthews, S. C., Feinstein, J. S., Hitchcock, C., Paulus, M. P., & Stein, M. B. (2008). Anxiety vulnerability is associated with altered anterior cingulate response to an affective appraisal task. Neuroreport, 19, 10331037. https://doi.org/10.1097/WNR.0b013e328305b722CrossRefGoogle Scholar
Swartz, J. R., Carrasco, M., Wiggins, J. L., Thomason, M. E., & Monk, C. S. (2014). Age-related changes in the structure and function of prefrontal cortex–amygdala circuitry in children and adolescents: A multi-modal imaging approach. NeuroImage, 86, 212220. https://doi.org/10.1016/j.neuroimage.2013.08.018CrossRefGoogle ScholarPubMed
Thakkar, K. N., Polli, F. E., Joseph, R. M., Tuch, D. S., Hadjikhani, N., Barton, J. J. S., & Manoach, D. S. (2008). Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD). Brain, 131, 24642478. https://doi.org/10.1093/brain/awn099CrossRefGoogle Scholar
Uddin, L. Q., Supekar, K., & Menon, V. (2013). Reconceptualizing functional brain connectivity in autism from a developmental perspective. Frontiers in Human Neuroscience, 7, 458. https://doi.org/10.3389/fnhum.2013.00458.CrossRefGoogle ScholarPubMed
Unruh, K., Martin, L. E., Magnon, G., Vaillancourt, D. E., Sweeney, J. A., & Mosconi, M. W. (2019). Cortical and subcortical alterations associated with precision visuomotor behavior in individuals with autism spectrum disorder. Journal of Neurophysiology, 122, 13301341. https://doi.org/10.1152/jn.00286.2019CrossRefGoogle ScholarPubMed
Van Dijk, K. R. A., Hedden, T., Venkataraman, A., Evans, K. C., Lazar, S. W., & Buckner, R. L. (2010). Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization. Journal of Neurophysiology, 103, 297321. https://doi.org/10.1152/jn.00783.2009CrossRefGoogle Scholar
Voorhies, W., Dajani, D. R., Vij, S. G., Shankar, S., Turan, T. O., & Uddin, L. Q. (2018). Aberrant functional connectivity of inhibitory control networks in children with autism spectrum disorder: Inhibitory control networks in autism. Autism Research, 11, 14681478. https://doi.org/10.1002/aur.2014CrossRefGoogle ScholarPubMed
Whalen, P. J., Johnstone, T., Somerville, L. H., Nitschke, J. B., Polis, S., Alexander, A. L., … Kalin, N. H. (2008). A functional magnetic resonance imaging predictor of treatment response to venlafaxine in generalized anxiety disorder. Biological Psychiatry, 63, 858863. https://doi.org/10.1016/j.biopsych.2007.08.019CrossRefGoogle ScholarPubMed
Yan, C.-G., Craddock, R. C., Zuo, X.-N., Zang, Y.-F., & Milham, M. P. (2013). Standardizing the intrinsic brain: Towards robust measurement of inter-individual variation in 1000 functional connectomes. NeuroImage, 80, 246262. https://doi.org/10.1016/j.neuroimage.2013.04.081CrossRefGoogle ScholarPubMed
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