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The Feeling of Me Feeling for You: Interoception, Alexithymia and Empathy in Autism

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Abstract

Following recent evidence for a link between interoception, emotion and empathy, we investigated relationships between these factors in autism spectrum disorder (ASD). 26 adults with ASD and 26 healthy participants completed tasks measuring interoception, alexithymia and empathy. ASD participants with alexithymia demonstrated lower cognitive and affective empathy than ASD participants without alexithymia. ASD participants showed reduced interoceptive sensitivity (IS), and also reduced interoceptive awareness (IA). IA was correlated with empathy and alexithymia, but IS was related to neither. Alexithymia fulfilled a mediating role between IA and empathy. Our findings are suggestive of an alexithymic subgroup in ASD, with distinct interoceptive processing abilities, and have implications for diagnosis and interventions.

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References

  • Ainley, V., Maister, L., & Tsakiris, M. (2015). Heartfelt empathy? No association between interoceptive awareness, questionnaire measures of empathy, reading the mind in the eyes task or the director task. Frontiers in Psychology, 6, 554.

    Article  PubMed  PubMed Central  Google Scholar 

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders, fifth edition (DSM-5). Arlington, VA: American Psychiatric Association.

    Book  Google Scholar 

  • Bachevalier, J., & Loveland, K. A. (2006). The orbitofrontal–amygdala circuit and self-regulation of social–emotional behavior in autism. Neuroscience & Biobehavioral Reviews, 30(1), 97–117.

    Article  Google Scholar 

  • Bagby, R. M., Parker, J. D., & Taylor, G. J. (1994). The twenty-item Toronto Alexithymia Scale—I. Item selection and cross-validation of the factor structure. Journal of Psychosomatic Research, 38(1), 23–32.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S., Leslie, A. M., & Frith, U. (1985). Does the autistic child have a “theory of mind”? Cognition, 21(1), 37–46.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S., & Wheelwright, S. (2004). The empathy quotient: An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34(2), 163–175.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Ben-Sasson, A., Hen, L., Fluss, R., Cermak, S. A., Engel-Yeger, B., & Gal, E. (2009). A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(1), 1–11.

    Article  PubMed  Google Scholar 

  • Bird, G., & Cook, R. (2013). Mixed emotions: The contribution of alexithymia to the emotional symptoms of autism. Translational Psychiatry, 3(7), e285.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bird, G., Silani, G., Brindley, R., White, S., Frith, U., & Singer, T. (2010). Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain, 133, 1515–1525.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bird, G., & Viding, E. (2014). The self to other model of empathy: Providing a new framework for understanding empathy impairments in psychopathy, autism and alexithymia. Neuroscience and Biobehavioral Reviews, 47, 520–532.

    Article  PubMed  Google Scholar 

  • Blair, R. J. R. (2005). Responding to the emotions of others: Dissociating forms of empathy through the study of typical and psychiatric populations. Consciousness and Cognition, 14(4), 698–718.

    Article  PubMed  Google Scholar 

  • Botvinick, M., Jha, A. P., Bylsma, L. M., Fabian, S. A., Solomon, P. E., & Prkachin, K. M. (2005). Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. NeuroImage, 25(1), 312–319.

    Article  PubMed  Google Scholar 

  • Brener, J., & Ring, C. (2016). Towards a psychophysics of interoceptive processes: The measurement of heartbeat detection. Philosophical Transactions of the Royal Society B, 371(1708), 20160015.

    Article  Google Scholar 

  • Brewer, R., Happe, F., Cook, R., & Bird, G. (2015). Commentary on “Autism, oxytocin and interoception”: Alexithymia, not Autism Spectrum Disorders, is the consequence of interoceptive failure. Neuroscience & Biobehavioral Reviews, 56, 348–353.

    Article  Google Scholar 

  • Cameron, O. G. (2001). Interoception: The inside story; a model for psychosomatic processes. Psychosomatic Medicine, 63, 697–710.

    Article  PubMed  Google Scholar 

  • Cook, R., Brewer, R., Shah, P., & Bird, G. (2013). Alexithymia, not autism, predicts poor recognition of emotional facial expressions. Psychological Science, 24(5), 723–732.

    Article  PubMed  Google Scholar 

  • Craig, A. (2008). Interoception and emotion: A neuroanatomical perspective. In Handbook of emotions (3rd ed., pp. 272–292). New York: Guildford Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Crane, L., Goddard, L., & Pring, L. (2009). Sensory processing in adults with autism spectrum disorders. Autism, 13(3), 215–228.

    Article  PubMed  Google Scholar 

  • Critchley, H. D. (2005). Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology, 493, 154–166.

    Article  PubMed  Google Scholar 

  • Damasio, A. (2000). The feeling of what happens: Body and emotion in the making of consciousness. San Diego: Harvest Books.

    Google Scholar 

  • Demurie, E., De Corel, M., & Roeyers, H. (2011). Empathic accuracy in adolescents with autism spectrum disorders and adolescents with attention-deficit/hyperactivity disorder. Research in Autism Spectrum Disorders, 5(1), 126–134.

    Article  Google Scholar 

  • DuBois, D., Ameis, S. H., Lai, M., Casanova, M. F., & Desarkar, P. (2016). Interoception in autism spectrum disorder: A review. International Journal of Developmental Neuroscience, 52, 104–111.

    Article  PubMed  Google Scholar 

  • Dunn, B. D., Stefanovitch, I., Evans, D., Oliver, C., Hawkins, A., & Dalgleish, T. (2010). Can you feel the beat? Interoceptive awareness is an interactive function of anxiety-and depression-specific symptom dimensions. Behaviour Research and Therapy, 48(11), 1133–1138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dziobek, I., Rogers, K., Fleck, S., Bahnemann, M., Heekeren, H. R., Wolf, O. T., & Convit, A. (2008). Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the multifaceted empathy test. Journal of Autism and Developmental Disorders, 38, 464–473.

    Article  PubMed  Google Scholar 

  • Eisenberg, N. (2000). Emotion, regulation and moral development. Annual Review of Psychology, 51, 665–697.

    Article  PubMed  Google Scholar 

  • Elwin, M., Ek, L., Kjellin, L., & Schröder, A. (2013). Too much or too little: Hyper-and hypo-reactivity in high-functioning autism spectrum conditions. Journal of Intellectual and Developmental Disability, 38(3), 232–241.

    Article  PubMed  Google Scholar 

  • Ernst, J., Northoff, G., Bäker, H., Seifritz, E., & Grimm, S. (2012). Interoceptive awareness enhances neural activity during empathy. Human Brain Mapping, 34, 1615–1624.

    Article  PubMed  Google Scholar 

  • Fan, Y. T., Chen, C., Chen, S. C., Decety, J., & Cheng, Y. (2014). Empathic arousal and social understanding in individuals with autism: Evidence from fMRI and ERP measurements. Social Cognitive and Affective Neuroscience, 9(8), 1203–1213.

    Article  PubMed  Google Scholar 

  • Fiene, L., & Brownlow, C. (2015). Investigating interoception and body awareness in adults with and without autism spectrum disorder. Autism Research, 8, 709–716.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 emotions and anxiety. Biological Psychology, 114, 117–126.

    Article  PubMed  Google Scholar 

  • Gillberg, C. L. (1992). The Emanuel Miller memorial lecture 1991. Journal of Child Psychology and Psychiatry, 33(5), 813–842.

    Article  PubMed  Google Scholar 

  • Golan, O., & Baron-Cohen, S. (2006). Systemizing empathy: Teaching adults with Asperger syndrome or high-functioning autism to recognize complex emotions using interactive multimedia. Development and Psychopathology, 18(02), 591–617.

    Article  PubMed  Google Scholar 

  • Greimel, E., Schulte-Rüther, M., Kircher, T., Kamp-Becker, I., Remschmidt, H., Fink, G. R., … Konrad, K. (2010). Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. NeuroImage, 49(1), 1055–1065.

    Article  PubMed  Google Scholar 

  • Grynberg, D., Chang, B., Corneille, O., Maurage, P., Vermeulen, N., Berthoz, S., & Luminet, O. (2012). Alexithymia and the processing of emotional facial expressions (EFEs): Systematic review, unanswered questions and further perspectives. PLoS ONE, 7, e42429.

    Article  PubMed  PubMed Central  Google Scholar 

  • Grynberg, D., Luminet, O., Corneille, O., Grèzes, J., & Berthoz, S. (2010). Alexithymia in the interpersonal domain: A general deficit of empathy? Personality and Individual Differences, 49, 845–850.

    Article  Google Scholar 

  • Grynberg, D., & Pollatos, O. (2015). Perceiving one’s body shapes empathy. Physiology & Behavior, 140, 54–60.

    Article  Google Scholar 

  • Guttman, H., & Laporte, L. (2002). Alexithymia, empathy, and psychological symptoms in a family context. Comprehensive Psychiatry, 43(6), 448–455.

    Article  PubMed  Google Scholar 

  • Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.

    Google Scholar 

  • Herbert, B. M., Herbert, C., & Pollatos, O. (2011). On the relationship between interoceptive awareness and alexithymia: Is interoceptive awareness related to emotional awareness? Journal of Personality, 79, 1149–1175.

    Article  PubMed  Google Scholar 

  • Herbert, B. M., Pollatos, O., & Schandry, R. (2007). Interoceptive sensitivity and emotion processing: An EEG study. International Journal of Psychophysiology, 65, 214–227.

    Article  PubMed  Google Scholar 

  • 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 and Developmental Disorders, 34(2), 229–235.

    Article  PubMed  Google Scholar 

  • Jabbi, M., Bastiaansen, J., & Keysers, C. (2008). A common anterior insula representation of disgust observation, experience and imagination shows divergent functional connectivity pathways. PLoS ONE, 3(8), e2939.

    Article  PubMed  PubMed Central  Google Scholar 

  • James, W. (1894). Discussion: The physical basis of emotion. Psychological Review, 1, 516–529.

    Article  Google Scholar 

  • Kandasamy, N., Garfinkel, S. N., Page, L., Hardy, B., Critchley, H. D., Gurnell, M., & Coates, J. M. (2016). Interoceptive ability predicts survival on a London trading floor. Scientific Reports, 6, 32986.

    Article  PubMed  PubMed Central  Google Scholar 

  • Keysers, C., & Gazzola, V. (2009). Expanding the mirror: Vicarious activity for actions, emotions, and sensations. Current Opinion in Neurobiology, 19(6), 666–671.

    Article  PubMed  Google Scholar 

  • Khalsa, S. S., & Lapidus, R. C. (2016). Can interoception improve the pragmatic search for biomarkers in psychiatry? Frontiers in Psychiatry, 7, 121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khalsa, S. S., Rudrauf, D., Damasio, A. R., Davidson, R. J., Lutz, A., & Tranel, D. (2008). Interoceptive awareness in experienced meditators. Psychophysiology, 45(4), 671–677.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Knoll, J. F., & Hodapp, V. (1992). A comparison between two methods for assessing heartbeat perception. Psychophysiology, 29(2), 218–222.

    Article  PubMed  Google Scholar 

  • Linden, W., Wen, F., & Paulhus, D. (1995). Measuring alexithymia: Reliability, validity, and prevalence. Advances in Personality Assessment, 10, 51–95.

    Google Scholar 

  • Livingston, L. A., & Livingston, L. M. (2016). Commentary: Alexithymia, not autism, is associated with impaired interoception. Frontiers in Psychology, 7, 1103.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H. Jr., Leventhal, B. L., DiLavore, P. C., … Rutter, M. (2000). The autism diagnostic observation schedule—Generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.

    Article  PubMed  Google Scholar 

  • Marchesi, C., Brusamonti, E., & Maggini, C. (2000). Are alexithymia, depression, and anxiety distinct constructs in affective disorders? Journal of Psychosomatic Research, 49, 43–49.

    Article  PubMed  Google Scholar 

  • Mehling, W. (2016). Differentiating attention styles and regulatory aspects of self-reported interoceptive sensibility. Philosophical Transactions of the Royal Society B, 371(1708), 20160013.

    Article  Google Scholar 

  • 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, e48230.

    Article  PubMed  PubMed Central  Google Scholar 

  • Meissner, K., & Wittmann, M. (2011). Body signals, cardiac awareness, and the perception of time. Biological Psychology, 86, 289–297.

    Article  PubMed  Google Scholar 

  • Murphy, J., Brewer, R., Catmur, C., & Bird, G. (2017). Interoception and psychopathology: A developmental neuroscience perspective. Developmental Cognitive Neuroscience, 23, 45–56.

    Article  PubMed  Google Scholar 

  • Nemiah, J., Freyberger, H., & Sifneos, P. (1976). Alexithymia: A view of the psychosomatic process. Modern Trends in Psychosomatic Medicine, 3, 430–439.

    Google Scholar 

  • Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain—A meta-analysis of imaging studies on the self. NeuroImage, 31(1), 440–457.

    Article  PubMed  Google Scholar 

  • Ochsner, K. N., Zaki, J., Hanelin, J., Ludlow, D. H., Knierim, K., Ramachandran, T., … Mackey, S. C. (2008). Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other. Social Cognitive and Affective Neuroscience, 3(2), 144–160.

    Article  PubMed  PubMed Central  Google Scholar 

  • Parker, J. D., Taylor, G. J., & Bagby, R. M. (2003). The 20-item Toronto Alexithymia Scale: III. Reliability and factorial validity in a community population. Journal of Psychosomatic Research, 55(3), 269–275.

    Article  PubMed  Google Scholar 

  • Paulus, M. P., & Stein, M. B. (2010). Interoception in anxiety and depression. Brain Structure and Function, 214(5–6), 451–463.

    Article  PubMed  Google Scholar 

  • Phillips, G. C., Jones, G. E., Rieger, E. J., & Snell, J. B. (1999). Effects of the presentation of false heart-rate feedback on the performance of two common heartbeat-detection tasks. Psychophysiology, 36(4), 504–510.

    Article  PubMed  Google Scholar 

  • Porges, S. (1993). Body perception questionnaire. College Park: Laboratory of Developmental Assessment, University of Maryland.

    Google Scholar 

  • Quattrocki, E., & Friston, K. (2014). Autism, oxytocin and interoception. Neuroscience & Biobehavioral Reviews, 47, 410–430.

    Article  Google Scholar 

  • Reniers, R. L., Corcoran, R., Drake, R., Shryane, N. M., & Völlm, B. A. (2011). The QCAE: A questionnaire of cognitive and affective empathy. Journal of Personality Assessment, 93, 84–95.

    Article  PubMed  Google Scholar 

  • Rogers, K., Dziobek, I., Hassenstab, J., Wolf, O. T., & Convit, A. (2007). Who cares? Revisiting empathy in Asperger syndrome. Journal of Autism and Developmental Disorders, 37, 709–715.

    Article  PubMed  Google Scholar 

  • Rueda, P., Fernández-Berrocal, P., & Baron-Cohen, S. (2015). Dissociation between cognitive and affective empathy in youth with Asperger syndrome. European Journal of Developmental Psychology, 12, 85–98.

    Article  Google Scholar 

  • Samson, A. C., Huber, O., & Gross, J. J. (2012). Emotion regulation in Asperger’s syndrome and high-functioning autism. Emotion, 12(4), 659–666.

    Article  PubMed  Google Scholar 

  • Schaefer, M., Egloff, B., & Witthüft, M. (2012). Is interoceptive awareness really altered in somatoform disorders? Testing competing theories with two paradigms of heartbeat perception. Journal of Abnormal Psychology, 121, 719–724.

    Article  PubMed  Google Scholar 

  • Schandry, R. (1981). Heartbeat perception and emotional experience. Psychophysiology, 18, 483–488.

    Article  PubMed  Google Scholar 

  • Schauder, K. B., Mash, L. E., Bryant, L. K., & Cascio, C. J. (2015). Interoceptive ability and body awareness in ASD. Journal of Experimental Child Psychology, 131, 193–200.

    Article  PubMed  Google Scholar 

  • Schulz, A., Lass-Hennemann, J., Sütterlin, S., Schächinger, H., & Vögele, C. (2013). Cold pressor stress induces opposite effects on cardioceptive accuracy dependent on assessment paradigm. Biological Psychology, 93(1), 167–174.

    Article  PubMed  Google Scholar 

  • 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, 3193–3194.

    Article  Google Scholar 

  • Shah, P., Catmur, C., & Bird, G. (2016a). Emotional decision-making in autism spectrum disorder: The roles of interoception and alexithymia. Molecular Autism, 7, 43–52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shah, P., Hall, R., Catmur, C., & Bird, G. (2016b). Alexithymia, not autism, is associated with impaired interoception. Cortex, 81, 215–220.

    Article  PubMed  PubMed Central  Google Scholar 

  • Silani, G., Bird, G., Brindley, R., Singer, T., Frith, C., & Frith, U. (2008). Levels of emotional awareness and autism: An fMRI study. Social Neuroscience, 3(2), 97–112.

    Article  PubMed  Google Scholar 

  • Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences, 13, 334–340.

    Article  PubMed  Google Scholar 

  • Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303, 1157–1162.

    Article  PubMed  Google Scholar 

  • Skokauskas, N., & Gallagher, L. (2010). Psychosis, affective disorders and anxiety in autistic spectrum disorder: Prevalence and nosological considerations. Psychopathology, 43, 8–16.

    Article  PubMed  Google Scholar 

  • Terasawa, Y., Moriguchi, Y., Tochizawa, S., & Umeda, S. (2014). Interoceptive sensitivity predicts sensitivity to the emotions of others. Cognition & Emotion, 28, 1435–1448.

    Article  Google Scholar 

  • Wechsler, D. (2011). Wechsler abbreviated scale of intelligence—second edition (WASI-II). San Antonio, TX: NCS Pearson.

    Google Scholar 

  • Whitehead, W. E., Drescher, V. M., Heiman, P., & Blackwell, B. (1977). Relation of heart rate control to heartbeat perception. Biofeedback and Self-Regulation, 2(4), 371–392.

    Article  Google Scholar 

  • Wicker, B., Keysers, C., Plailly, J., Royet, J., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron, 40(3), 655–664.

    Article  PubMed  Google Scholar 

  • Wiens, S., Mezzacappa, E. S., & Katkin, E. S. (2000). Heartbeat detection and the experience of emotions. Cognition & Emotion, 14(3), 417–427.

    Article  Google Scholar 

  • Zaki, J., Davis, J. I., & Ochsner, K. N. (2012). Overlapping activity in anterior insula during interoception and emotional experience. NeuroImage, 62(1), 493–499.

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was funded by Anglia Ruskin University, Cambridge, UK, as part of the doctoral study of Cari-lène Mul.

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CM and JA designed the experiment. SS conducted the diagnostic interviews. BH created experimental software. CM recruited participants, collected the data, and analysed the data. All authors discussed the results and contributed to the final manuscript.

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Correspondence to Cari-lène Mul.

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Mul, Cl., Stagg, S.D., Herbelin, B. et al. The Feeling of Me Feeling for You: Interoception, Alexithymia and Empathy in Autism. J Autism Dev Disord 48, 2953–2967 (2018). https://doi.org/10.1007/s10803-018-3564-3

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