Discrepancies between dimensions of interoception in autism: Implications for emotion and anxiety

Biological Psychology

Volumn 114, Issue , 2016, Pages 117-126

  Garfinkel, Sarah N ^a,b   Tiley, Claire ^a   O'Keeffe, Stephanie ^a   Harrison, Neil A ^a,b,c   Seth, Anil K ^a,b   Critchley, Hugo D ^a,b,c  

^a BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c SUSSEX PARTNERSHIP NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Alexithymia; Anxiety; Asperger syndrome; Emotion; Interoceptive

Indexed keywords

ADULT; ANXIETY; ARTICLE; AUTISM; CLINICAL ARTICLE; CONTROLLED STUDY; EMOTION; EMOTIONALITY; FEMALE; HEART BEAT; HUMAN; INTEROCEPTION; MALE; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; QUESTIONNAIRE; SELF REPORT; SYMPTOM; AROUSAL; CASE CONTROL STUDY; EMOTIONAL DISORDER; HEART RATE; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SENSATION;

ADULT; AFFECTIVE SYMPTOMS; ANXIETY; AROUSAL; AUTISTIC DISORDER; CASE-CONTROL STUDIES; EMOTIONS; FEMALE; HEART RATE; HUMANS; INTEROCEPTION; MALE; SELF REPORT; SENSATION;

EID: 84953737593     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2015.12.003     Document Type: Article

References (82)

1. Antony M.M., Brown T.A., Craske M.G., Barlow D.H., Mitchell W.B., Meadows E.A. Accuracy of heartbeat perception in panic disorder, social phobia, and nonanxious subjects. Journal of Anxiety Disorders 1995, 9(5):355-371. 10.1016/0887-6185(95) 00017-I.
2. Baron-Cohen S., Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders 2004, 34(2):163-175.
3. Barsky A.J., Cleary P.D., Sarnie M.K., Ruskin J.N. Panic disorder, palpitations, and the awareness of cardiac activity. Journal of Nervous and Mental Disease 1994, 182(2):63-71. 10.1097/00005053-199402000-00001.
4. Bernhardt B.C., Singer T. The neural basis of empathy. Annual Review of Neuroscience 2012, 35(35):1-23. 10.1146/annurev-neuro-062111-150536.
5. Berthoz S., Artiges E., Van de Moortele P.F., Poline J.B., Rouquette S., Consoli S.M., Martinot J.L. Effect of impaired recognition and expression of emotions on frontocingulate cortices: an fMRI study of men with alexithymia. American Journal of Psychiatry 2002, 159(6):961-967. 10.1176/appi.ajp.159.6.961.
6. Bird G., Silani G., Brindley R., White S., Frith U., Singer T. Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain 2010, 133(Pt. 5):1515-1525. awq060 [pii]. 10.1093/brain/awq060.
7. Brener J., Kluvitse C. Heartbeat detection-judgments of the simultaneity of external stimuli and heartbeats. Psychophysiology 1988, 25(5):554-561. 10.1111/j.1469-8986.1988.tb01891.x.
8. Brener J., Liu X.Q., Ring C. A method of constant stimuli for examining heartbeat detection-comparison with the Brener-Kluvitse and Whitehead methods. Psychophysiology 1993, 30(6):657-665. 10.1111/j.1469-8986.1993.tb02091.x.
9. Cameron O.G. Visceral sensory neuroscience: interoception 2001, Oxford University Press, USA, New York.
10. Canales-Johnson A., Silva C., Huepe D., Rivera-Rei A., Noreika V., Garcia Mdel C., et al. Auditory feedback differentially modulates behavioral and neural markers of objective and subjective performance when tapping to your heartbeat. Cerebral Cortex 2015, 25:4490-4503. 10.1093/cercor/bhv076.
11. Ceunen E., Van Diest I., Vlaeyen J.W.S. Accuracy and awareness of perception: related, yet distinct (commentary on Herbert et al., 2012). Biological Psychology 2013, 92(2):426-427.
12. Chauhan B., Mathias C.J., Critchley H.D. Autonomic contributions to empathy: evidence from patients with primary autonomic failure. Autonomic Neuroscience-Basic & Clinical 2008, 140(1-2):96-100. 10.1016/j.autneu.2008.03.005.
13. Chien Y.L., Gau S.S.F., Chiu Y.N., Tsai W.C., Shang C.Y., Wu Y.Y. Impaired sustained attention, focused attention, and vigilance in youths with autistic disorder and Asperger's disorder. Research in Autism Spectrum Disorders 2014, 8(7):881-889. 10.1016/j.rasd.2014.04.006.
14. Clark A. Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behavioral and Brain Sciences 2013, 36(3):181-204. 10.1017/S0140525x12000477.
15. Cobos P., Sanchez M., Garcia C., Vera M.N., Vila J. Revisiting the James versus Cannon debate on emotion: startle and autonomic modulation in patients with spinal cord injuries. Biological Psychology 2002, 61(3):251-269. Pii S0301-0511(02) 00061-3. 10.1016/s0301-0511(02) 00061-3.
16. Cohen J. Statistical Power Analysis for the Behavioral Sciences 1988, Lawrence Erlbaum Associates, Hillsdale, NJ. 2nd ed.
17. Cohen J. A power primer. Psychological Bulletin 1992, 112(1):155-159. 10.1037/0033-2909.112.1.155.
18. Craig A.D. How do you feel?: an interoceptive moment with your neurobiological self 2015, Princeton University Press, New Jersey.
19. Critchley H.D., Corfield D.R., Chandler M.P., Mathias C.J., Dolan R.J. Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. Journal of Physiology-London 2000, 523(1):259-270. 10.1111/j.1469-7793.2000.t01-1-00259.x.
20. Critchley H.D., Rotshtein P., Nagai Y., O'Doherty J., Mathias C.J., Dolan R.J. Activity in the human brain predicting differential heart rate responses to emotional facial expressions. Neuroimage 2005, 24(3):751-762. 10.1016/j.neuroimage.2004.10.013.
21. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nature Neuroscience 2004, 7(2):189-195. 10.1038/nn1176.
22. Depascalis V., Alberti M.L., Pandolfo R. Anxiety, perce ption, and control of heart-rate. Perceptual and Motor Skills 1984, 59(1):203-211.
23. Duerden E.G., Taylor M.J., Soorya L.V., Wang T., Fan J., Anagnostou E. Neural correlates of inhibition of socially relevant stimuli in adults with autism spectrum disorder. Brain Research 2013, 1533:80-90. 10.1016/j.brainres.2013.08.021.
24. Dunn B.D., Stefanovitch I., Evans D., Oliver C., Hawkins A., Dalgleish T. Can you feel the beat? Interoceptive awareness is an interactive function of anxiety- and depression-specific symptom dimensions. Behaviour Research and Therapy 2010, 48(11):1133-1138. 10.1016/j.brat.2010.07.006.
25. Ebisch S.J.H., Gallese V., Willems R.M., Mantini D., Groen W.B., Romani G.L., Buitelaar J.K., Bekkering H. Altered intrinsic functional connectivity of anterior and posterior insula regions in high-functioning participants with autism spectrum disorder. Human Brain Mapping 2011, 32(7):1013-1028. 10.1002/hbm.21085.
26. Ehlers A., Breuer P. Increased cardiac awareness in panic disorder. Journal of Abnormal Psychology 1992, 101(3):371-382. 10.1037//0021-843x.101.3.371.
27. Ehlers A., Margraf J., Roth W.T., Taylor C.B., Birbaumer N. Anxiety induced by false heart-rate feedback in patients with panic disorder. Behaviour Research and Therapy 1988, 26(1):1-11. 10.1016/0005-7967(88) 90028-9.
28. Ernst J., Boker H., Hattenschwiler J., Schupbach D., Northoff G., Seifritz E., Grimm S. The association of interoceptive awareness and alexithymia with neurotransmitter concentrations in insula and anterior cingulate. Social Cognitive and Affective Neuroscience 2014, 9(6):857-863. 10.1093/scan/nst058.
29. Frewen P.A., Dozois D.J.A., Neufeld R.W.J., Lanius R.A. Meta-analysis of alexithymia in posttraumatic stress disorder. Journal of Traumatic Stress 2008, 21(2):243-246. 10.1002/jts.20320.
30. Frith U. Autism-are we any closer to explaining the enigma?. Psychologist 2014, 27(10):744-745.
31. Garfinkel S.N., Critchley H.D. Interoception, emotion and brain: new insights link internal physiology to social behaviour. Social Cognitive and Affective Neuroscience 2013, 8(3):231-234. 10.1093/scan/nss140.
32. Garfinkel S.N., Seth A.K., Barrett A.B., Suzuki K., Critchley H.D. Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biological Psychology 2015, 104:65-74. S0301-0511(14) 00229-4 [pii]. 10.1016/j.biopsycho.2014.11.004.
33. Green D.M., Swets J.A. Signal detection theory and psychophysics 1966, Wiley, New York.
34. Gu X., Eilam-Stock T., Zhou T., Anagnostou E., Kolevzon A., Soorya L., Friston K.J., Fan J. Autonomic and brain responses associated with empathy deficits in autism spectrum disorder. Human Brain Mapping 2015, 36(9):3323-3338. 10.1002/hbm.22840.
35. Hadjikhani N., Joseph R.M., Manoach D.S., Naik P., Snyder J., Dominick K., Van den Stock J., Gelder B. Body expressions of emotion do not trigger fear contagion in autism spectrum disorder. Social Cognitive and Affective Neuroscience 2009, 4(1):70-78. 10.1093/scan/nsn038.
36. Hart N., McGowan J., Minati L., Critchley H.D. Emotional regulation and bodily sensation: interoceptive awareness is intact in borderline personality disorder. Journal of Personality Disorders 2013, 27(4):506-518.
37. Hill E., Berthoz S., Frith U. Brief report: cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. Journal of Autism and Developmental Disorders 2004, 34(2):229-235. 10.1023/b:jadd.0000022613.41399.14.
38. Karlsson H., Naatanen P., Stenman H. Cortical activation in alexithymia as a response to emotional stimuli. British Journal of Psychiatry 2008, 192(1):32-38. 10.1192/bjp.bp.106.034728.
39. Katkin E.S., Reed S.D., Deroo C. A methodological analysis of 3 techniques for the assessment of individual-differences in heartbeat detection. Psychophysiology 1983, 20(4):452.
40. Kleckner I.R., Wormwood J.B., Simmons W.K., Barrett L.F., Quigley K.S. Methodological recommendations for a heartbeat detection-based measure of interoceptive sensitivity. Psychophysiology 2015, 10.1111/psyp.12503.
41. Knoll J.F., Hodapp V. A comparison between 2 methods for assessing heartbeat perception. Psychophysiology 1992, 29(2):218-222. 10.1111/j.1469-8986.1992.tb01689.x.
42. Kootz J.P., Marinelli B., Cohen D.J. Modulation of response to environmental stimulation in autistic-children. Journal of Autism and Developmental Disorders 1982, 12(2):185-193. 10.1007/Bf01531308.
43. Lange C.G., James W. The Emotions 1967, Hafner Publishing Co., New York; London, reprinted. K. Dunlap (Ed.).
44. Lawrence E.J., Shaw P., Baker D., Baron-Cohen S., David A.S. Measuring empathy: reliability and validity of the empathy quotient. Psychological Medicine 2004, 34(5):911-919. 10.1017/s0033291703001624.
45. Ludwickrosenthal R., Neufeld R.W.J. Heart beat interoception-a study of individual-differences. International Journal of Psychophysiology 1985, 3(1):57-65. 10.1016/0167-8760(85) 90020-0.
46. MacNeil B.M., Lopes V.A., Minnes P.M. Anxiety in children and adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders 2009, 3(1):1-21. 10.1016/j.rasd.2008.06.001.
47. Naring G.W.B., Vanderstaak C.P.F. Perception of heart-rate and blood-pressure-the role of alexithymia and anxiety. Psychotherapy and Psychosomatics 1995, 63(3-4):193-200.
48. Nicotra A., Critchley H.D., Mathias C.J., Dolan R.J. Emotional and autonomic consequences of spinal cord injury explored using functional brain imaging. Brain 2006, 129:718-728. 10.1093/brain/awh699.
49. Nummenmaa L., Glerean E., Hari R., Hietanen J.K. Bodily maps of emotions. Proceedings of the National Academy of Sciences of the United States of America 2014, 111(2):646-651. 10.1073/pnas.1321664111.
50. Palkovitz R.J., Wiesenfeld A.R. Differential autonomic responses of autistic and normal children. Journal of Autism and Developmental Disorders 1980, 10(3):347-360.
51. Paulus M.P., Stein M.B. An insular view of anxiety. Biological Psychiatry 2006, 60(4):383-387. 10.1016/j.biopsych.2006.03.042.
52. Paulus M.P., Stein M.B. Interoception in anxiety and depression. Brain Structure & Function 2010, 214(5-6):451-463. 10.1007/s00429-010-0258-9.
53. Payne R.A., Symeonides C.N., Webb D.J., Maxwell S.R.J. Pulse transit time measured from the ECG: an unreliable marker of beat-to-beat blood pressure. Journal of Applied Physiology 2006, 100(1):136-141. 10.1152/japplphysiol.00657.2005.
54. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002, 16(2):331-348. 10.1006/nimg.2002.1087.
55. Phillips G.C., Jones G.E., Rieger E.J., Snell J.B. Effects of the presentation of false heart-rate feedback on the performance of two common heartbeat-detection tasks. Psychophysiology 1999, 36(4):504-510. 10.1017/s0048577299980071.
56. Pollatos O., Traut-Mattausch E., Schroeder H., Schandry R. Interoceptive awareness mediates the relationship between anxiety and the intensity of unpleasant feelings. Journal of Anxiety Disorders 2007, 21(7):931-943. S0887-6185(06) 00232-5 [pii]. 10.1016/j.janxdis.2006.12.004.
57. Porges S. Body perception questionnaire: laboratory of development assessment 1993, University of Maryland.
58. Porges S.W. Peripheral and neurochemical parallels of psychopathology: a psychophysiological model relating autonomic imbalance to hyperactivity, psychopathy and autism. Advances in Child Development and Behavior 1976, 11:35-65.
59. Quattrocki E., Friston K. Autism, oxytocin and interoception. Neuroscience and Biobehavioral Reviews 2014, 47:410-430. 10.1016/j.neubiorev.2014.09.012.
60. Ring C., Brener J. The temporal locations of heartbeat sensations. Psychophysiology 1992, 29(5):535-545. 10.1111/j.1469-8986.1992.tb02027.x.
61. Ring C., Brener J. Influence of beliefs about heart rate and actual heart rate on heartbeat counting. Psychophysiology 1996, 33(5):541-546. 10.1111/j.1469-8986.1996.tb02430.x.
62. Ring C., Brener J., Knapp K., Mailloux J. Effects of heartbeat feedback on beliefs about heart rate and heartbeat counting: a cautionary tale about interoceptive awareness. Biological Psychology 2015, 104:193-198.
63. Schaefer M., Egloff B., Gerlach A.L., Witthoft M. Improving heartbeat perception in patients with medically unexplained symptoms reduces symptom distress. Biological Psychology 2014, 101:69-76. S0301-0511(14) 00154-9 [pii]. 10.1016/j.biopsycho.2014.05.012.
64. Schandry R. Heart beat perception and emotional experience. Psychophysiology 1981, 18(4):483-488. 10.1111/j.1469-8986.1981.tb02486.x.
65. Schauder K.B., Mash L.E., Bryant L.K., Cascio C.J. Interoceptive ability and body awareness in autism spectrum disorder. Journal of Experimental Child Psychology 2014, 205-207. S0022-0965(14) 00205-7 [pii]. 10.1016/j.jecp.2014.11.002.
66. Scheuren R., Sutterlin S., Anton F. Rumination and interoceptive accuracy predict the occurrence of the thermal grill illusion of pain. BMC Psychology 2014, 2:22.
67. Schulz A., Lass-Hennemann J., Sutterlin S., Schachinger H., Vogele C. Cold pressor stress induces opposite effects on cardioceptive accuracy dependent on assessment paradigm. Biological Psychology 2013, 93(1):167-174. 10.1016/j.biopsycho.2013.01.007.
68. Serpa J.G., Taylor S.L., Tillisch K. Mindfulness-based stress reduction (MBSR) reduces anxiety, depression, and suicidal ideation in veterans. Medical Care 2014, 52(12 Suppl. 5):S19-S24. 00005650-201412001-00007 [pii]. 10.1097/mlr.0000000000000202.
69. Seth A.K. Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences 2013, 17(11):565-573.
70. Sherrington C.S. The integrative action of the nervous system 1948, Cambridge University Press, Cambridge, UK.
71. Simonoff E., Pickles A., Charman T., Chandler S., Loucas T., Baird G. Psychiatric disorders in children with autism spectrum disorders: prevalence, comorbidity, and associated factors in a population-derived sample. Journal of the American Academy of Child and Adolescent Psychiatry 2008, 47(8):921-929. 10.1097/Chi.0b013e318179964f.
72. Singer T., Lamm C. The social neuroscience of empathy. Year in Cognitive Neuroscience 2009 2009, 1156:81-96. 10.1111/j.1749-6632.2009.04418.x.
73. Spielberger C.D., Gorsuch R.L., Lushene R., Vagg P.R., Jacobs G.A. Manual for the state-trait anxiety inventory 1983, Consulting Psychologists Press, Palo Alto, CA.
74. Sze J.A., Gyurak A., Yuan J.W., Levenson R.W. Coherence between emotional experience and physiology: does body awareness training have an impact?. Emotion 2010, 10(6):803-814.
75. Terasawa Y., Shibata M., Moriguchi Y., Umeda S. Anterior insular cortex mediates bodily sensibility and social anxiety. Social Cognitive and Affective Neuroscience 2013, 8(3):259-266. 10.1093/scan/nss108.
76. Watanabe T., Yahata N., Abe O., Kuwabara H., Inoue H., Takano Y., Aoki Y., Yamasue H. Diminished medial prefrontal activity behind autistic social judgments of incongruent information. Public Library Of Science 2012, 7(6):e39561. ARTN. 10.1371/journal.pone.0039561.
77. White S.W., Oswald D., Ollendick T., Scahill L. Anxiety in children and adolescents with autism spectrum disorders. Clinical Psychology Review 2009, 29(3):216-229. 10.1016/j.cpr.2009.01.003.
78. Whitehead W.E., Drescher V.M., Heiman P., Blackwell B. Relation of heart-rate control to heartbeat perception. Biofeedback and Self-Regulation 1977, 2(4):371-392. 10.1007/Bf00998623.
79. Wiens S., Mezzacappa E.S., Katkin E.S. Heartbeat detection and the experience of emotions. Cognition and Emotion 2000, 14(3):417-427.
80. Wiens S., Palmer S.N. Quadratic trend analysis and heartbeat detection. Biological Psychology 2001, 58(2):159-175. 10.1016/s0301-0511(01) 00110-7.
81. Zahn T.P., Rumsey J.M., Van Kammen D.P. Autonomic nervous system activity in autistic, schizophrenic, and normal men: effects of stimulus significance. Journal of Abnormal Psychology 1987, 96(2):135-144.
82. Zaki J., Davis J.I., Ochsner K.N. Overlapping activity in anterior insula during interoception and emotional experience. Neuroimage 2012, 62(1):493-499. 10.1016/j.neuroimage.2012.05.012.