Abstract
Interoception is believed to underlie socio-cognitive functions which are often impaired in individuals with autism spectrum disorders (ASD). In this study, Experiment 1 examined in a sample of 114 neurotypical college students the associations among autistic traits, alexithymia, and interoceptive accuracy (IA), which was assessed by a novel paradigm “Eye-tracking Interoceptive Accuracy Task (EIAT). In Experiment 2, EIAT and the Autism Spectrum Quotient were administered to 52 preschool children, 50 adolescents, and 50 adults. Experiment 1 supported the association between autistic traits and alexithymia, but failed to support their association with multidimensional interoception. Experiment 2 strongly supported the association between age and IA. We conclude that cardiac IA differs between neurotypical age groups, but shows limited relationship with autistic traits.
Similar content being viewed by others
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
Baron-Cohen, S., Hoekstra, R. A., Knickmeyer, R., & Wheelwright, S. (2006). The autism-spectrum quotient (AQ)-adolescent version. Journal of Autism and Developmental Disorders, 36(3), 343–350. https://doi.org/10.1007/s10803-006-0073-6
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
Brener, J., & Ring, C. (2016). Towards a psychophysics of interoceptive processes: the measurement of heartbeat detection. Philosophical Transactions of the Royal Society B. 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. 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., 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
Ehlers, A., & Breuer, P. (1992). Increased cardiac awareness in panic disorder. Journal of Abnormal Psychology, 101(3), 371–382. https://doi.org/10.1037/0021-843x.101.3.371
Ernst, J., Northoff, G., Boeker, H., Seifritz, E., & Grimm, S. (2013). Interoceptive awareness enhances neural activity during empathy. Human Brain Mapping, 34(7), 1615–1624. https://doi.org/10.1002/hbm.22014
Failla, M. D., Bryant, L. K., Heflin, B. H., Mash, L. E., Schauder, K., Davis, S., & Cascio, 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
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
Garcia-Cordero, I., Sedeno, L., de la Fuente, L., Slachevsky, A., Forno, G., Klein, F., Lillo, P., Ferrari, J., Rodriguez, C., Bustin, J., & Feeling, T. T. (2016). Feeling, learning from and being aware of inner states: Interoceptive dimensions in neurodegeneration and stroke. Philosophical Transactions of the Royal Society B, 371(1708), 10. https://doi.org/10.1098/rstb.2016.0006
Garfinkel, S. N., Seth, A. K., Barrett, A. B., Suzuki, K., & Critchley, H. D. (2015). Knowing your own heart: Distinguishing interoceptive accuracy from interoceptive awareness. Biological Psychology, 104, 65–74. https://doi.org/10.1016/j.biopsycho.2014.11.004
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
Hill, E., Berthoz, S., & Frith, U. (2004). Brief report: Cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. Journal of Autism Developmental Disorder, 34, 229–235. https://doi.org/10.1023/B:JADD.0000022613.41399.14
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., 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
Koch, A., & Pollatos, O. (2014). Cardiac sensitivity in children: Sex differences and its relationship to parameters of emotional processing. Psychophysiology, 51(9), 932–941. https://doi.org/10.1111/psyp.12233
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
Lawson, R. P., Rees, G., & Friston, K. J. (2014). An aberrant precision account of autism. Frontiers in Human Neuroscience, 8, 302.
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
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., Brewer, R., Catmur, C., & Bird, G. (2017). Interoception and psychopathology: A developmental neuroscience perspective. Developmental Cognitive Neuroscience, 23, 45–56. https://doi.org/10.1016/j.dcn.2016.12.006
Murphy, J., Brewer, R., Hobson, H., Catmur, C., & Bird, G. (2018c). Is alexithymia characterised by impaired interoception? Further evidence, the importance of control variables, and the problems with the heartbeat counting task. Biological Psychology, 136, 189–197. https://doi.org/10.1016/j.biopsycho.2018.05.010
Murphy, J., Catmur, C., & Bird, G. (2018a). 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
Murphy, J., Geary, H., Millgate, E., Catmur, C., & Bird, G. (2018b). Direct and indirect effects of age on interoceptive accuracy and awareness across the adult lifespan. Psychonomic Bulletin & Review, 25(3), 1193–1202. https://doi.org/10.3758/s13423-017-1339-z
Nicholson, T., Williams, D., Carpenter, K., & Kallitsounaki, A. (2019). Interoception is impaired in children, but not adults, with autism spectrum disorder. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-019-04079-w
Noel, J., 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
O’Brien, W. H., Reid, G. J., & Jones, K. R. (1998). Differences in heartbeat awareness among males with higher and lower levels of systolic blood pressure. International Journal of Psychophysiology, 29(1), 53–63. https://doi.org/10.1016/s0167-8760(98)00004-x
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. https://doi.org/10.1371/journal.pone.0203212
Pollatos, O., Schandry, R., Auer, D. P., & Kaufmann, C. (2007). Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Research, 1141, 178–187. https://doi.org/10.1016/j.brainres.2007.01.026
Porges, S. (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
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., 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
Robins, D. L., Fein, D., Barton, M. L., & Green, J. A. (2001). The Modified checklist for autism in toddlers: An initial study investigating the early detection of autism and pervasive developmental disorders. Journal of Autism and Developmental Disorders, 31(2), 131–144.
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
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.
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
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., & Lepine, J. P. (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
Si, T. M., Liang, S. H. U., 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. 503.
Siebes, R., Muntjewerff, J. W., & Staal, W. (2018). Differences of symptom distribution across adult age in high functioning individuals on the autism spectrum using subscales of the autism spectrum quotient. Journal of Autism and Developmental Disorders, 48(11), 3939–3944. https://doi.org/10.1007/s10803-018-3657-z
Trevisan, D. A., Mehling, W. E., & McPartland, J. C. (2021). 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
Tsakiris, M., & Critchley, H. (2016). Interoception beyond homeostasis: affect, cognition and mental health. Philosophical Transactions of the Royal Society B. 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. https://doi.org/10.1098/rstb.2016.0005
Wallace, G. L., Dudley, K., Anthony, L., Pugliese, C. E., Orionzi, B., Clasen, L., Lee, N. R., Giedd, J. N., Martin, A., Raznahan, A., & Kenworthy, L. (2017). Divergence of age-related differences in social-communication: improvements for typically developing youth but declines for youth with autism spectrum disorder. Journal of Autism and Developmental Disorders, 47(2), 472–479. https://doi.org/10.1007/s10803-016-2972-5
West, R., Murphy, K. J., Armilio, M. L., Craik, F. I., & Stuss, D. T. (2002). Lapses of intention and performance variability reveal age-related increases in fluctuations of executive control. Brain and Cognition, 49, 402–419.
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
Zhou, Q., Hofer, C., Eisenberg, N., Reiser, M., Spinrad, T. L., & Fabes, R. A. (2007). The developmental trajectories of attention focusing, attentional and behavioral persistence, and externalizing problems during school-age years. Developmental Psychology, 43(2), 369–385. https://doi.org/10.1037/0012-1649.43.2.369
Zhu, X., Yi, J., Yao, S., Ryder, A. G., Taylor, G. J., & Michael Bagby, R. (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.
Acknowledgments
This study was supported by a grant form National Science Foundation China (31970997) and the CAS Key Laboratory of Mental Health, Institute of Psychology. No conflict of interest to be declared.
Author information
Authors and Affiliations
Contributions
Author Raymond C. K. Chan designed the study and wrote the protocol. Authors Han-xue Yang, Han-yu Zhou, Zhen Wei, and Guo-bin Wan managed the data collection. Author Han-xue Yang undertook the statistical analysis and wrote the first draft of the manuscript. Authors Raymond C. K. Chan, Yi Wang, Tian-xiao Yang, and Simon S. Y. Lui edited the manuscript and gave critical comments. All authors contributed to and have approved the final 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
Yang, Hx., Zhou, Hy., Wei, Z. et al. Multidimensional Interoception and Autistic Traits Across life Stages: Evidence From a Novel Eye-tracking Task. J Autism Dev Disord 52, 2644–2655 (2022). https://doi.org/10.1007/s10803-021-05155-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-021-05155-w