Abstract
Interoception, the sense of the physiological condition of our body, is impaired in individuals with autism spectrum disorders. Evidence suggests that subclinical autistic traits are mild manifestations of autistic symptoms, present in the general population. We examined the resting-state functional connectivity (rsFC) associating with interoception and autistic traits in 62 healthy young adults. Autistic traits correlated negatively with the rsFC between the lateral ventral anterior insula and anterior cingulate cortex. Interoceptive accuracy and sensibility correlated positively with the rsFC between interoceptive brain networks and the cerebellum, supplementary motor area, and visual regions. The results suggest that a negative relationship between interoception and autistic traits is largely accounted for by both self-report measures and decreased rsFC amongst the interoceptive brain network.
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Adams, R. A., Shipp, S., & Friston, K. J. (2013). Predictions not commands: Active inference in the motor system. Brain Structure & Function, 218, 611–643. https://doi.org/10.1007/s00429-012-0475-5.
APA. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). American Psychiatric Association.
Ardizzi, M., Ambrosecchia, M., Buratta, L., Ferri, F., Peciccia, M., Donnari, S., & Gallese, V. (2016). Interoception and positive symptoms in schizophrenia, Frontiers in Human Neuroscience, 10.
Bagby, R. M., Parker, J. D. A., & Taylor, G. J. (1994). The 20-item toronto alexithymia scale: Item selection and cross-validation of the factor structure. Journal of Psychosomatic Research, 38(1), 23–32. https://doi.org/10.1016/00223999(94)90005-1.
Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001). The autism-spectrum quotient (AQ): Evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31(1), 5–17. https://doi.org/10.1023/a:1005653411471.
Barrett, L. F., & Simmons, W. K. (2015). Interoceptive predictions in the brain. Nature Reviews Neuroscience, 16(7), 419–429. https://doi.org/10.1038/nrn3950.
Beer, A. L., Tina, P., Georg, M., & Greenlee, M. W. (2013). Combined diffusion-weighted and functional magnetic resonance imaging reveals a temporal-occipital network involved in auditory-visual object processing. Frontiers in Integrative Neuroscience, 7, 5. https://doi.org/10.3389/fnint.2013.00005.
Berner, L. A., Simmons, A. N., Wierenga, C. E., Bischoff-Grethe, A., Paulus, M. P., Bailer, U. F., & Kaye, W. H. (2019). Altered anticipation and processing of aversive interoceptive experience among women remitted from bulimia nervosa. Neuropsychopharmacology : Official Publication Of The American College Of Neuropsychopharmacology, 44(7), 1265–1273. https://doi.org/10.1038/s41386-019-0361-4.
Brett, M., Anton, J., Valabregue, R., & Poline, J. (2002). Region of interest analysis using an SPM toolbox. Neuroimage, 16(2), 210–217. https://doi.org/10.1016/S1053-8119(02)90013-3.
Brewer, R., Murphy, J., & Bird, G. (2021). Atypical interoception as a common risk factor for psychopathology: A review. Neuroscience and Biobehavioral Reviews, 130, 470–508. https://doi.org/10.1016/j.neubiorev.2021.07.036.
Caspi, A., Houts, R. M., Belsky, D. W., Goldman-Mellor, S. J., Harrington, H., Israel, S., Meier, M. H., Ramrakha, S., Shalev, I., Poulton, R., & Moffitt, T. E. (2014). The p factor: One General psychopathology factor in the structure of Psychiatric Disorders? Clinical Psychological Science, 2(2), 119–137. https://doi.org/10.1177/2167702613497473.
Chong, J. S. X., Ng, G. J. P., Lee, S. C., & Zhou, J. (2017). Salience network connectivity in the insula is associated with individual differences in interoceptive accuracy. Brain Structure & Function, 222(4), 1635–1644. https://doi.org/10.1007/s00429-016-1297-7.
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., Metzger, L. M., Shoushtari, C. S., Splinter, R., & Reich, W. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433. https://doi.org/10.1023/a:1025014929212.
Craig, A. D. (2002). How do you feel? Interoception: The sense of the physiological condition of the body. Nature Reviews Neuroscience, 3(8), 655–666. https://doi.org/10.1038/nrn894.
Craig, A. D. (2009). How do you feel - now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10(1), 59–70. https://doi.org/10.1038/nrn2555.
Critchley, H. D., & Garfinkel, S. N. (2015). Interactions between visceral afferent signaling and stimulus processing. Frontiers in Neuroscience, 9, https://doi.org/10.3389/fnins.2015.00286.
Critchley, H. D., & Harrison, N. A. (2013). Visceral influences on Brain and Behavior. Neuron, 77(4), 624–638. https://doi.org/10.1016/j.neuron.2013.02.008.
Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7(2), 189–195. https://doi.org/10.1038/nn1176.
Critchley, H., Eccles, J., van Praag, C. G., Watson, D., & Garfinkel, S. (2018). Interoceptive gating of anxiety and fear, a novel target for anxiety treatment. Biological Psychiatry, 83(9), S13–S13. https://doi.org/10.1016/j.biopsych.2018.02.049.
Di Martino, A., Shehzad, Z., Kelly, C., Roy, A. K., Gee, D. G., Uddin, L. Q., & Milham, M. P. (2009). Relationship between Cingulo-Insular Functional Connectivity and autistic traits in neurotypical adults. American Journal of Psychiatry, 166(8), 891–899. https://doi.org/10.1176/appi.ajp.2009.08121894.
Ebisch, S. J. H., Gallese, V., Willems, R. M., Mantini, D., Groen, W. B., Romani, G. L., Buitelaar, J. K., & Bekkering, H. (2011). Altered intrinsic functional connectivity of anterior and posterior insula regions in high-functioning participants with autism spectrum disorder. Human Brain Mapping, 32(7), 1013–1028. https://doi.org/10.1002/hbm.21085.
Failla, M. D., Bryant, L. K., Heflin, B. H., Mash, L. E., Schauder, K., Davis, S., Gerdes, Madison, B., Weitlauf, A., Rogers, B. P., & Cascio, C. J. (2020). Neural correlates of cardiac interoceptive focus across development: Implications for social symptoms in autism spectrum disorder. Autism Research, 13(6), 908–920. https://doi.org/10.1002/aur.2289.
Flasinski, T., Dierolf, A. M., Rost, S., Lutz, A. P., Voderholzer, U., Koch, S., & Mertens, V. C. (2020). Altered interoceptive awareness in high habitual symptom reporters and patients with somatoform disorders. Frontiers in Psychology, 11, 1–12. https://doi.org/10.3389/fpsyg.2020.01859.
Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Review Neuroscience, 8(9), 700–711. https://doi.org/10.1038/nrn2201.
Francis, S. M., Camchong, J., Brickman, L., Goelkel-Garcia, L., Mueller, B. A., Tseng, A., Lim, K. O., & Jacob, S. (2019). Hypoconnectivity of insular resting-state networks in adolescents with autism spectrum disorder. Psychiatry Research-Neuroimaging, 283, 104–112. https://doi.org/10.1016/j.pscychresns.2018.12.003.
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. P., Frith, C. D., & Frackowiak, R. S. (1994). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2(4), 189–210. https://doi.org/10.1002/hbm.460020402.
Garfinkel, S. N., Barrett, A. B., Minati, L., Dolan, R. J., Seth, A. K., & Critchley, H. D. (2013). What the heart forgets: Cardiac timing influences memory for words and is modulated by metacognition and interoceptive sensitivity. Psychophysiology, 50(6), 505–512. https://doi.org/10.1111/psyp.12039.
Garfinkel, S. N., Tiley, C., O’Keeffe, S., Harrison, N. A., Seth, A. K., & Critchley, H. D. (2016). Discrepancies between dimensions of interoception in autism: Implications for emotion and anxiety. Biological Psychology, 114, 117–126. https://doi.org/10.1016/j.biopsycho.2015.12.003.
Grahn, J. A., & Watson, S. L. (2013). Perspectives on rhythm processing in motor regions of the brain. Music Therapy Perspectives, 31(1), 25–30. https://doi.org/10.1093/mtp/31.1.25.
Harshaw, C. (2015). Interoceptive dysfunction: Toward an Integrated Framework for understanding somatic and affective disturbance in Depression. Psychological Bulletin, 141(2), 311–363. https://doi.org/10.1037/a0038101.
Herman, A. M., Critchley, H. D., & Duka, T. (2018). Risk-Taking and Impulsivity: The Role of Mood States and Interoception. Frontiers in Psychology, 9. https://doi.org/10.3389/fpsyg.2018.01625.
Jakobson, L. S., & Rigby, S. N. (2021). Alexithymia and sensory Processing sensitivity: Areas of overlap and links to sensory Processing Styles. Frontiers in Psychology, 12, https://doi.org/10.3389/fpsyg.2021.583786.
Jarrahi, B., Mantini, D., Balsters, J. H., Michels, L., Kessler, T. M., Mehnert, U., & Kollias, S. S. (2015). Differential functional brain network connectivity during visceral interoception as revealed by independent component analysis of fMRI time-series. Human Brain Mapping, 36(11), 4438–4468. https://doi.org/10.1002/hbm.22929.
Jonas, S. (1981). The supplementary motor region and speech emission. Journal of Communication Disorders, 14(5), 349–373. https://doi.org/10.1016/00219924(81)90019-8.
Khalsa, S. S., Hassanpour, M. S., Strober, M., Craske, M. G., Arevian, A. C., & Feusner, J. D. (2018). Interoceptive anxiety and body representation in Anorexia Nervosa. Frontiers in Psychiatry, 9. https://doi.org/10.3389/fpsyt.2018.00444.
Kleckner, I. R., Zhang, J., Touroutoglou, A., Chanes, L., Xia, C., Simmons, W. K., Quigley, K. S., Dickerson, B. C., & Barrett, L. F. (2017). Evidence for a large-scale brain system supporting allostasis and interoception in humans. Nature Human Behaviour, 1(5), https://doi.org/10.1038/s41562-017-0069.
Krautwurst, S., Gerlach, A. L., Gomille, L., Hiller, W., & Witthoeft, M. (2014). Health anxiety - an indicator of higher interoceptive sensitivity? Journal of Behavior Therapy and Experimental Psychiatry, 45(2), 303–309. https://doi.org/10.1016/j.jbtep.2014.02.001.
Lau, W. Y. P., Gau, S. S. F., Chiu, Y. N., Wu, Y. Y., Chou, W. J., Liu, S. K., & Chou, M. C. (2013). Psychometric properties of the chinese version of the Autism Spectrum Quotient (AQ). Research in Developmental Disabilities, 34(1), 294–305. https://doi.org/10.1016/j.ridd.2012.08.005.
Leising, D., Grande, T., & Faber, R. (2009). The Toronto Alexithymia Scale (TAS-20): A measure of general psychological distress. Journal of Research in Personality, 43(4), 707–710. https://doi.org/10.1016/j.jrp.2009.03.009.
Lin, F. L., Hsu, C. C., Mehling, W., & Yeh, M. L. (2017). Translation and psychometric testing of the chinese version of the multidimensional assessment of interoceptive awareness. Journal of Nursing Research, 25(1), 76–83. https://doi.org/10.1097/jnr.0000000000000182.
Martínez, K., Martínez-García, M., Marcos-Vidal, L., Janssen, J., & Carmona, S. (2019). Sensory-to-cognitive systems integration is associated with clinical severity in autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 59(3), https://doi.org/10.1016/j.jaac.2019.05.033.
Mehling, W. E., Price, C., Daubenmier, J. J., Acree, M., Bartmess, E., & Stewart, A. (2012). The Multidimensional Assessment of Interoceptive Awareness (MAIA). Plos One, 7(11), https://doi.org/10.1371/journal.pone.0048230.
Mufson, E. J., Mesulam, M. M., & Pandya, D. N. (1981). Insular interconnections with the amygdala in rhesus monkey. Neuroscience, 6, 1231–1248. https://doi.org/10.1016/0306-4522(81)90184-6.
O’Reilly, J. X., Beckmann, C. F., Tomassini, V., Ramnani, N., & Johansen-Berg, H. (2010). Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cerebral Cortex, 20(4), 953–965. https://doi.org/10.1093/cercor/bhp157.
Palser, E. R., Fotopoulou, A., Pellicano, E., & Kilner, J. M. (2018). The link between interoceptive processing and anxiety in children diagnosed with autism spectrum disorder: Extending adult findings into a developmental sample. Biological Psychology, 136, 13–21. https://doi.org/10.1016/j.biopsycho.2018.05.003.
Porges, S. W. (1993). Body perception questionnaire. Laboratory of Developmental. Assessment, University of Maryland.
Quattrocki, E., & Friston, K. (2014). Autism, oxytocin and interoception. Neuroscience and Biobehavioral Reviews, 47, 410–430. https://doi.org/10.1016/j.neubiorev.2014.09.012.
Riva-Posse, P., Inman, C. S., Choi, K. S., Crowell, A. L., Gross, R. E., Hamann, S., & Mayberg, H. S. (2019). Autonomic arousal elicited by subcallosal cingulate stimulation is explained by white matter connectivity. Brain Stimulation, 12(3), 743–751. https://doi.org/10.1016/j.brs.2019.01.015.
Schandry, R. (1981). Heartbeat perception and emotional experience. Psychophysiology, 18(4), 483–488. https://doi.org/10.1111/j.14698986.1981.tb02486.x.
Schauder, K. B., Mash, L. E., Bryant, L. K., & Cascio, C. J. (2015). Interoceptive ability and body awareness in autism spectrum disorder. Journal of Experimental Child Psychology, 131, 193–200. https://doi.org/10.1016/j.jecp.2014.11.002.
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., & Dunbar, G. C. (1998). The mini-international neuropsychiatric interview (MINI): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59, 22–33. https://doi.org/10.4088/JCP.09m05305whi.
Smith, S. D., Nadeau, C., Sorokopud-Jones, M., & Kornelsen, J. (2021). The relationship between functional connectivity and interoceptive sensibility. Brain connectivity. https://doi.org/10.1089/brain.2020.0777.
Sridharan, D., Levitin, D. J., & Menon, V. (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences of the United States of America, 105(34), 12569–12574. https://doi.org/10.1073/pnas.0800005105.
Terasawa, Y., Fukushima, H., & Umeda, S. (2013). How does interoceptive awareness interact with the subjective experience of emotion? An fMRI study. Human Brain Mapping, 34(3), 598–612. https://doi.org/10.1002/hbm.21458.
Tremblay, P., & Gracco, V. L. (2006). Contribution of the frontal lobe to externally and internally specified verbal responses: fmri evidence. NeuroImage, 33(3), 947–957. https://doi.org/10.1016/j.neuroimage.2006.07.041.
Trevisan, D. A., Mehling, W. E., & McPartland, J. C. (2021a). Adaptive and maladaptive bodily awareness: Distinguishing interoceptive sensibility and interoceptive attention from anxiety-induced somatization in autism and alexithymia. Autism Research, 14(2), 240–247. https://doi.org/10.1002/aur.2458.
Trevisan, D. A., Parker, T., & McPartland, J. C. (2021b). First-hand accounts of interoceptive difficulties in autistic adults. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-020-04811-x.
Uddin, L. Q., & Menon, V. (2009). The anterior insula in autism: Under-connected and under-examined. Neuroscience and Biobehavioral Reviews, 33(8), 1198–1203. https://doi.org/10.1016/j.neubiorev.2009.06.002.
Ueno, D., Matsuoka, T., Kato, Y., Ayani, N., Maeda, S., Takeda, M., & Narumoto, J. (2020). Individual differences in interoceptive accuracy are correlated with salience network connectivity in older adults. Frontiers in Aging Neuroscience, 12, https://doi.org/10.3389/fnagi.2020.592002.
Wang, X., Tan, Y., Van den Bergh, O., von Leupoldt, A., & Qiu, J. (2020). Intrinsic functional brain connectivity patterns underlying enhanced interoceptive sensibility. Journal of Affective Disorders, 276, 804–814. https://doi.org/10.1016/j.jad.2020.07.032.
Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016). DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics 14, 339–351. https://doi.org/10.1007/s12021-016-9299-4.
Zhu, X. Z., Yi, J. Y., Yao, S. Q., Ryder, A. G., Taylor, G. J., & Bagby, M. (2007). Cross-cultural validation of a chinese translation of the 20-item toronto alexithymia scale. Comprehensive Psychiatry, 48(5), 489–496. https://doi.org/10.1016/j.comppsych.2007.04.007.
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This study was supported by a grant form National Science Foundation China (31970997), the Scientific Foundation of Institute of Psychology, Chinese Academy of Sciences (E2CX3415CX), and the Philip K. H. Wong Foundation. No conflict of interest to be declared.
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Conceptualization: R. C. K. Chan; Methodology: H. X. Yang, Y. Wang; Formal Analysis: H. X. Yang and Y. J. Zhang; Investigation: H. X. Hu, L. L. Wang, and Y. J. Yan; Writing – Original Draft Preparation: H. X. Yang; Writing – Review & Editing: R. C. K. Chan, and Simon S. Y. Lui; Supervision: R. C. K. Chan. All authors commented and approved the final version for submission.
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Yang, Hx., Zhang, Yj., Hu, Hx. et al. Relationship Between Interoception and Autistic Traits: A Resting-State Functional Connectivity Study. J Autism Dev Disord (2023). https://doi.org/10.1007/s10803-023-06050-2
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DOI: https://doi.org/10.1007/s10803-023-06050-2