Abstract
Interoceptive accuracy has been widely measured using the Heartbeat Tracking Test (HTT). We devised the novel paradigm of Interoception-Exteroception Synchronicity Judgement (IESJ) task to assess participants’ interoceptive accuracy, exteroceptive accuracy, and the balancing score which reflected the ability to allocate attentions between interoceptive and exteroceptive signals. This study administered the behavioural paradigms of the HTT and the IESJ as well as other self-report scales to 119 typically-developing youths. Individuals with lower autistic traits (n = 30) showed comparable interoceptive accuracy, exteroceptive accuracy, and balancing scores as their higher autistic traits counterparts (n = 33). Taken together, the high autistic traits subgroup exhibited higher levels of alexithymia but not empathy or interoception than the low autistic traits subgroup.
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References
APA. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). American Psychiatric Association.
Bagby, R. M., Parker, J. D. A., & Taylor, G. J. (1994). The 20-item toronto- alexithymia scale. 1. Item selection and cross-validation of the factor structure. Journal of Psychosomatic Research, 38(1), 23–32. https://doi.org/10.1016/0022-3999(94)90005-1
Baio, J. B. (2018). Centre for disease control and prevention. Prevalence of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network United States. MMWR Surveillance Summaries, 67, 1–23.
Baron-Cohen, S. (2002). The extreme male brain theory of autism. Trends in Cognitive Sciences, 6(6), 248–254. https://doi.org/10.1016/s1364-6613(02)01904-6
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., Quigley, K. S., & Hamilton, P. (2016). An active inference theory of allostasis and interoception in depression. Philosophical Transactions of the Royal Society B Biological Sciences, 371(1708), 2016001. https://doi.org/10.1098/rstb.2016.0011
Barttfeld, P., Wicker, B., Cukier, S., Navarta, S., Lew, S., Leiguarda, R., & Sigman, M. (2012). State-dependent changes of connectivity patterns and functional brain network topology in autism spectrum disorder. Neuropsychologia, 50(14), 3653–3662. https://doi.org/10.1016/j.neuropsychologia.2012.09.047
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993). Cardiac psychophysiology and autonomic space in humans: Empirical perspectives and conceptual implications. Psychological Bulletin, 114, 296–322. https://doi.org/10.1037/0033-2909.114.2.296
Brener, J., & Ring, C. (2016). Towards a psychophysics of interoceptive processes: The measurement of heartbeat detection. Philosophical Transactions of the Royal Society B-Biological Sciences, 371(1708), 20160015. https://doi.org/10.1098/rstb.2016.0015
Brewer, R., Cook, R., & Bird, G. (2016). Alexithymia: A general deficit of interoception. Royal Society Open Science, 3(10), 150664. https://doi.org/10.1098/rsos.150664
Chua, E. F., & Bliss-Moreau, E. (2016). Knowing your heart and your mind: The relationships between metamemory and interoception. Consciousness and Cognition, 45, 146–158. https://doi.org/10.1016/j.concog.2016.08.015
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., et al. (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
DeWitt, S. J., Ketcherside, A., McQueeny, T. M., Dunlop, J. P., & Filbey, F. M. (2015). The hyper-sentient addict: An exteroception model of addiction. American Journal of Drug and Alcohol Abuse, 41(5), 374–381. https://doi.org/10.3109/00952990.2015.1049701
Dunn, B. D., Galton, H. C., Morgan, R., Evans, D., Oliver, C., Meyer, M., et al. (2010). Listening to your heart: How interoception shapes emotion experience and intuitive decision making. Psychological Science, 21(12), 1835–1844. https://doi.org/10.1177/0956797610389191
Ebisch, S. J. H., Mantini, D., Northoff, G., Salone, A., De Berardis, D., Ferri, F., et al. (2014). Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia. Schizophrenia Bulletin, 40(5), 1072–1082. https://doi.org/10.1093/schbul/sbt153
Failla, M. D., Bryant, L. K., Heflin, B. H., Mash, L. E., Schauder, K., Davis, S., et al. (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
Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39, 175–191. https://doi.org/10.3758/BF03193146
Francis, S. M., Camchong, J., Brickman, L., Goelkel-Garcia, L., Mueller, B. A., Tseng, A., et al. (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
Fuestoes, J., Gramann, K., Herbert, B. M., & Pollatos, O. (2013). On the embodiment of emotion regulation: Interoceptive awareness facilitates reappraisal. Social Cognitive and Affective Neuroscience, 8(8), 911–917. https://doi.org/10.1093/scan/nss089
Fukushima, H., Terasawa, Y., & Umeda, S. (2011). Association between interoception and empathy: Evidence from heartbeat-evoked brain potential. International Journal of Psychophysiology, 79(2), 259–265. https://doi.org/10.1016/j.ijpsycho.2010.10.015
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
Grinter, E. J., Beek, P. L. V., Maybery, M. T., & Badcock, D. R. (2009). Brief report: Visuospatial analysis and self-rated autistic-like traits. Journal of Autism and Developmental Disorders, 39(4), 670–677. https://doi.org/10.1007/s10803-008-0658-3
Iarocci, G., & McDonald, J. (2006). Sensory integration and the perceptual experience of persons with autism. Journal of Autism and Developmental Disorders, 36(1), 77–90. https://doi.org/10.1007/s10803-005-0044-3
Katkin, E. S., Reed, S. D., & Deroo, C. (1983). A methodological analysis of 3techniques for the assessment of individual-differences in heartbeat detection. Psychophysiology, 20(4), 452.
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. https://doi.org/10.3389/fpsyt.2018.00444
Khalsa, S. S., Rudrauf, D., & Tranel, D. (2009). Interoceptive awareness declines with age. Psychophysiology, 46(6), 1130–1136. https://doi.org/10.1111/j.1469-8986.2009.00859.x
Knapp-Kline, K., & Kline, J. P. (2005). Heart rate, heart rate variability, and heartbeat detection with the method of constant stimuli: Slow and steady wins the race. Biological Psychology, 69(3), 387–396. https://doi.org/10.1016/j.biopsycho.2004.09.002
Kutscheidt, K., Dresler, T., Hudak, J., Barth, B., Blume, F., Ethofer, T., et al. (2019). Interoceptive awareness in patients with attention-deficit/hyperactivity disorder (ADHD). Attention Deficit and Hyperactivity Disorders. https://doi.org/10.1007/s12402-019-00299-3
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
Liang, Y. S., Yang, H. X., Ma, Y. T., Lui, S. S. Y., Cheung, E. F. C., Wang, Y., & Chan, R. C. K. (2019). Validation and extension of the questionnaire of cognitive and affective empathy in the Chinese setting. PsyCh Journal, 8(4), 439–448. https://doi.org/10.1002/pchj.281
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
Maister, L., Tang, T., & Tsakiris, M. (2017). Neurobehavioral evidence of interoceptive sensitivity in early infancy. eLife. https://doi.org/10.7554/eLife.25318
McDonnell, C. G., Valentino, K., & Diehl, J. J. (2017). A developmental psychopathology perspective on autobiographical memory in autism spectrum disorder. Developmental Review, 44, 59–81. https://doi.org/10.1016/j.dr.2017.01.001
McFadden, K. L., Tregellas, J. R., Shott, M. E., & Frank, G. K. W. (2014). Reduced salience and default mode network activity in women with anorexia nervosa. Journal of Psychiatry & Neuroscience, 39(3), 178–188. https://doi.org/10.1503/jpn.130046
Mehling, W. E., Acree, M., Stewart, A., Silas, J., & Jones, A. (2018). The multidimensional assessment of interoceptive awareness, version 2 (MAIA-2). PLoS ONE, 13(12), e0208034. https://doi.org/10.1371/journal.pone.0208034
Mul, C.-L., Stagg, S. D., Herbelin, B., & Aspell, J. E. (2018). The feeling of me feeling for you: Interoception, alexithymia and empathy in autism. Journal of Autism and Developmental Disorders, 48(9), 2953–2967. https://doi.org/10.1007/s10803-018-3564-3
Murphy, J., Catmur, C., & Bird, G. (2018). Alexithymia is associated with a multidomain, multidimensional failure of interoception: Evidence from novel tests. Journal of Experimental Psychology-General, 147(3), 398–408. https://doi.org/10.1037/xge0000366
Noel, J.-P., Lytle, M., Cascio, C., & Wallace, M. T. (2018). Disrupted integration of exteroceptive and interoceptive signaling in autism spectrum disorder. Autism Research, 11(1), 194–205. https://doi.org/10.1002/aur.1880
Palser, E. R., Palmer, C. E., Galvez-Pol, A., Hannah, R., Fotopoulou, A., & Kilner, J. M. (2018). Alexithymia mediates the relationship between interoceptive sensibility and anxiety. PLoS ONE, 13(9), e0203212. https://doi.org/10.1371/journal.pone.0203212
Paulus, M. P., & Stein, M. B. (2010). Interoception in anxiety and depression. Brain Structure & Function, 214(5–6), 451–463. https://doi.org/10.1007/s00429-010-0258-9
Pollatos, O., Traut-Mattausch, E., & Schandry, R. (2009). Differential effexts of anxiety and depression on interoceptive accuracy. Depression and Anxiety, 26(2), 167–173. https://doi.org/10.1002/da.20504
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
Reniers, R. L. E. P., Corcoran, R., Drake, R., Shryane, N. M., & Voellm, B. A. (2011). The QCAE: A questionnaire of cognitive and affective empathy. Journal of Personality Assessment, 93(1), 84–95. https://doi.org/10.1080/00223891.2010.528484
Ring, C., & Brener, J. (2018). Heartbeat counting is unrelated to heartbeat detection: A comparison of methods to quantify interoception. Psychophysiology, 55(9), e13084. https://doi.org/10.1111/psyp.13084
Ring, C., Brener, J., Knapp, K., & Mailloux, J. (2015). Effects of heartbeat feedback on beliefs about heart rate and heartbeat counting: A cautionary tale about interoceptive awareness. Biological Psychology, 104, 193–198. https://doi.org/10.1016/j.biopsycho.2014.12.010
Rouse, C., Jones, G., & Jones, K. (1988). The effect of body composition and gender on cardiac awareness. Psychophysiology, 25(4), 400–407. https://doi.org/10.1111/j.1469-8986.1988.tb01876.x
Santos, M., Uppal, N., Butti, C., Wicinski, B., Schmeidler, J., Giannakopoulos, P., et al. (2011). von Economo neurons in autism: A stereologic study of the frontoinsular cortex in children. Brain Research, 1380, 206–217. https://doi.org/10.1016/j.brainres.2010.08.067
Schaan, L., Schulz, A., Nuraydin, S., Bergert, C., Hilger, A., Rach, H., & Hechler, T. (2019). Interoceptive accuracy, emotion recognition, and emotion regulation in preschool children. International Journal of Psychophysiology, 138, 47–56. https://doi.org/10.1016/j.ijpsycho.2019.02.001
Schandry, R. (1981). Heart beat perception and emotional experience. Psychophysiology, 18(4), 483–488. https://doi.org/10.1111/j.1469-8986.1981.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
Schneider, T. R., Ring, C., & Katkin, E. S. (1998). A test of the validity of the method of constant stimuli as an index of heartbeat detection. Psychophysiology, 35, 86–89. https://doi.org/10.1111/1469-8986.3510086
Seth, A. K. (2013). Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences, 17(11), 565–573. https://doi.org/10.1016/j.tics.2013.09.007
Seth, A. K., & Tsakiris, M. (2018). Being a beast machine: The somatic basis of selfhood. Trends in Cognitive Sciences, 22(11), 969–981. https://doi.org/10.1016/j.tics.2018.08.008
Shah, P. (2016). Interoception: The eighth sensory system: practical solutions for improving self-regulation, self-awareness and social understanding of individuals with autism spectrum and related disorders. Journal of Autism and Developmental Disorders, 46(9), 3193–3194. https://doi.org/10.1007/s10803-016-2848-8
Sheehan, D. V., Janavs, J., Baker, R., Harnett-Sheehan, K., Knapp, E., Sheehan, M., et al. (1998). MINI—mini international neuropsychiatric interview—english version 5.0.0—DSM-IV. Journal of Clinical Psychiatry, 59, 34–57. https://doi.org/10.4088/JCP.09m05305whi
Soosalu, G., Henwood, S., & Deo, A. (2019). Head, heart, and gut in decision making: Development of a multiple brain preference questionnaire. SAGE Open. https://doi.org/10.1177/2158244019837439
Sun, X., Allison, C., Wei, L., Matthews, F. E., Auyeung, B., Wu, Y. Y., et al. (2019). Autism prevalence in China is comparable to Western prevalence. Molecular Autism. https://doi.org/10.1186/s13229-018-0246-0
Tian-Mei, S., Liang, S., Wei-Min, D., Yun-Ai, S. E., Jing-Xu, C., Wen-Tian, D., & Wei-Hua, Z. (2009). Evaluation of the reliability and validity of Chinese version of the mini-international neuropsychiatric interview in patients with mental disorders. Chinese Mental Health Journal, 23(7), 493–497.
Torregrossa, L., Snodgress, M., Amedy, A., Nummenmaa, L., & Park, S. (2019). Interoception, internal noise and minimal self-disturbances in schizophrenia. Schizophrenia Bulletin, 45, S106–S106. https://doi.org/10.1093/schbul/sbz022.044
Tsakiris, M., & Critchley, H. (2016). Interoception beyond homeostasis: Affect, cognition and mental health. Philosophical Transactions of the Royal Society B-Biological Sciences, 371(1708), 20160002. https://doi.org/10.1098/rstb.2016.0002
Umeda, S., Tochizawa, S., Shibata, M., & Terasawa, Y. (2016). Prospective memory mediated by interoceptive accuracy: A psychophysiological approach. Philosophical Transactions of the Royal Society B-Biological Sciences, 371(1708), 20160005. https://doi.org/10.1098/rstb.2016.0005
van Borkulo, C., van Bork, R., Boschloo, L., Kossakowski, J., Tio, P., Schoevers, R., Borsboom, D., Waldorp, L. (2017) Comparing network structures on three aspects: A permutation test. https://doi.org/10.13140/RG.2.2.29455.38569
Whitehead, W. E., Drescher, V. M., Heiman, P., & Blackwell, B. (1977). Relation of heartrate control to heartbeat perception. Biofeedback and Self-Regulation, 2(4), 371–392. https://doi.org/10.1007/bf00998623
Wittmann, M. (2015). Modulations of the experience of self and time. Consciousness and Cognition, 38, 172–181. https://doi.org/10.1016/j.concog.2015.06.008
Yao, S., Becker, B., Zhao, W., Zhao, Z., Kou, J., Ma, X., et al. (2018). Oxytocin modulates attention switching between interoceptive signals and external social cues. Neuropsychopharmacology, 43(2), 294–301. https://doi.org/10.1038/npp.2017.189
Zhou, H. Y., Cai, X. L., Weigl, M., Bang, P., Cheung, E. F. C., & Chan, R. C. K. (2018). Multisensory temporal binding window in autism spectrum disorders and schizophrenia spectrum disorders: A systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews, 86, 66–76. https://doi.org/10.1016/j.neubiorev.2017.12.013
Zhu, X. Z., Yi, J. Y., & Yao, S. Q. (2004). Developing a Chinese version of observer alexithymia scale and Toronto alexithymia scale. International Journal of Psychology, 39(5–6), 392–392.
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This study was supported by a grant from the National Natural Science Foundation of China (31970997) and the CAS Key Laboratory of Mental Health, Institute of Psychology.
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Author Raymond C. K. Chan designed the study and wrote the protocol. Author Han-xue Yang, Han-yu Zhou, Yan-yu Wang and Hong Zheng managed the data collection. Authors Han-xue Yang undertook the statistical analysis and wrote the first draft of the manuscript. Author Raymond C. K. Chan, Simon S. Y. Lui and Yi Wang edited the manuscript. All authors contributed to and have approved the final manuscript.
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Yang, HX., Zhou, HY., Zheng, H. et al. Individuals with Autistic Traits Exhibit Heightened Alexithymia But Intact Interoceptive-Exteroceptive Sensory Integration. J Autism Dev Disord 52, 3142–3152 (2022). https://doi.org/10.1007/s10803-021-05199-y
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DOI: https://doi.org/10.1007/s10803-021-05199-y