Physiological responses to affiliation during conversation: Comparing neurotypical males and males with Asperger syndrome

English version

Autoři: Melisa Stevanovic ^aff001; Pentti Henttonen ^aff002; Emmi Koskinen ^aff001; Anssi Peräkylä ^aff001; Taina Nieminen von-Wendt ^aff003; Elina Sihvola ^aff004; Pekka Tani ^aff004; Niklas Ravaja ^aff002; Mikko Sams ^aff005
Působiště autorů: Faculty of Social Sciences, University of Helsinki, Helsinki, Finland ^aff001; Faculty of Medicine, University of Helsinki, Helsinki, Finland ^aff002; Neuropsychiatric Rehabilitation and Medical Center, NeuroMental, Helsinki, Finland ^aff003; Helsinki University Hospital, Helsinki, Finland ^aff004; Department of Neuroscience and Biomedical Engineering, Department of Computer Science, Aalto University, Espoo, Finland ^aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222084

Souhrn

We examined the emotional and psychophysiological underpinnings of social interaction in the context of autism spectrum disorder, more specifically, involving participants diagnosed with Asperger syndrome (AS). We recorded participants’ autonomic nervous system (ANS) activation (electrodermal activity, heart rate, and heart rate variability) and facial muscle activation during conversations in two different types of male dyads: (1) ten dyads where one participant has been diagnosed with AS (AS/NT dyads) and (2) nine dyads where both participants are neurotypical (NT/NT dyads). Afterwards, three independent raters assessed continuously each participant’s affiliative and dominant behaviors during the first and last 10 minutes of the conversations. The relationship between the assessed data and ANS responses was examined. We found that, in the NT/NT dyads, a high level of affiliation displayed by the conversational partner calms down the participant when they are actively dominating the interaction. In contrast, when the participants themselves expressed affiliation, their psychophysiological responses indicated increase in arousal, which suggests that the giving of affiliation is physiologically “hard work.” The affiliation-related ANS responses were similar in those NT participants whose conversational partner had AS, while some differences in facial muscle activation did occur in comparison to NT/NT dyads. In the AS participants, in contrast, a high level of affiliation provided by the conversational partner was associated with increase in arousal, suggesting heightened alertness and stress. As for their own affiliative behavior, the AS participants exhibited similar indicators of alertness and stress as the NT participants, but only when their own level of dominance was low. Our results increase understanding of how individuals with AS experience social interaction at the physiological level, and how this experience differs from that in NT individuals. Moreover, our results confirm and further specify our earlier results, where we proposed that affiliation involves the type of “sharing of the burden” that also reverberates in the participants’ bodies.

Klíčová slova:

Biology and life sciences – Neuroscience – Cognitive science – Psychology – Social sciences – Anatomy – Medicine and health sciences – Neurology – Cognitive neurology – Cognitive neuroscience – Head – Behavior – Cardiology – Emotions – Face – Developmental neuroscience – Neuropsychological testing – Neuropsychology – Neurodevelopmental disorders – Heart rate – Developmental psychology – Pervasive developmental disorders – Autism spectrum disorder – Autism – Asperger syndrome

Zdroje

1. Frith U. Autism and Asperger syndrome. Cambridge, UK: Cambridge University Press; 1991.

2. Szatmari P. Asperger’s syndrome: diagnosis, treatment, and outcome. Ped Clin N Am, 1991;14(1),81–92.

3. Smith Myles B, Simpson RL. Asperger syndrome: an overview of characteristics. Focus on Aut and Oth Dev Dis. 2002:17(3),132–7.

4. Lindström A, Sorjonen ML. Affiliation in conversation. In: Sidnell J, Stivers T, editors. The handbook of conversation analysis. Oxford, UK: Wiley-Blackwell; 2012. pp. 350–69.

5. Stivers T. Stance, alignment, and affiliation during storytelling: when nodding is a token of affiliation. Res Lang Soc Int. 2008;41(1),31–57.

6. Jefferson G. On the sequential organization of troubles-talk in ordinary conversation. Soc Probl. 1988;35(4),418–41.

7. Selting M. Affectivity in conversational storytelling: An analysis of displays of anger or indignation in complaint stories. Pragmatics 2010;20(2), 229–277.

8. Couper-Kuhlen E. Exploring affiliation in the reception of conversational complaint stories. In: Peräkylä A, Sorjonen ML, editors. Emotion in interaction. New York, NY: Oxford University Press; 2012. pp 113–46.

9. Peräkylä A, Ruusuvuori J. Facial expression and interactional regulation of emotion. In: Peräkylä A, Sorjonen ML, editors. Emotion in interaction. New York, NY: Oxford University Press; 2012. pp. 64–91.

10. Peräkylä A, Henttonen P, Voutilainen L, Kahri M, Stevanovic M, Sams M, Ravaja M. Sharing the emotional load: recipient affiliation calms down the storyteller. Soc Psych Quart. 2015;78(4):301–23.

11. Hochschild A. Emotion work, feeling rules, and social structure. Am J Sociol. 1979;85(3),551–75.

12. Hochschild A. The managed heart: Commercialization of human feeling. Berkeley: University of California Press; 1983.

13. De Jaegher H. Embodiment and sense-making in autism. Front Integr Neurosci. 2013;26.

14. Baron-Cohen S, Leslie AM, Frith U. Does the autistic child have a theory of mind? Cognition 1985;21, 37–46. 2934210

15. Senju A, Southgate V, White S, Frith U. Mindblind eyes: an absence of spontaneous theory of mind in Asperger syndrome. Science 2009;325(5942):883–5. doi: 10.1126/science.1176170 19608858

16. Pillai D, Sheppard E, Ropar D, Marsh L, Pearson A, Mitchell P. Using other minds as a window onto the world: guessing what happened from clues in behaviour. J Autism Dev Disord. 2014;44(10):2430–9. doi: 10.1007/s10803-014-2106-x 24710812

17. Cassidy S, Ropar D, Mitchell P, Chapman P. Can adults with autism spectrum disorders infer what happened to someone from their emotional response? Autism Res. 2014;7(1):112–23 doi: 10.1002/aur.1351 24307231

18. Cassidy S, Mitchell P, Chapman P, Ropar D. Processing of spontaneous emotional responses in adolescents and adults with autism spectrum disorders: effect of stimulus type. Autism Res. 2015;8(5):534–44. doi: 10.1002/aur.1468 25735657

19. Fletcher-Watson S, Leekam SR, Benson V, Frank MC, Findlay JM. Eye-movements reveal attention to social information in autism spectrum disorder. Neuropsychologia. 2009;47(1):248–57. doi: 10.1016/j.neuropsychologia.2008.07.016 18706434

20. Freeth M, Chapman P, Ropar D, Mitchell P. Do gaze cues in complex scenes capture and direct the attention of high functioning adolescents with ASD? Evidence from eye-tracking. J Autism Dev Disord. 2010;40(5):534–47. doi: 10.1007/s10803-009-0893-2 19904597

21. Doherty-Sneddon G, Whittle L, Riby DM. Gaze aversion during social style interactions in autism spectrum disorder and Williams syndrome. Res Dev Disabil. 2013;34(1):616–26. doi: 10.1016/j.ridd.2012.09.022 23123875

22. Sheppard E, Pillai D, Wong GT, Ropar D, Mitchell P. How easy is it to read the minds of people with autism spectrum disorder? J Autism Dev Disord. 2016;46(4):1247–54. doi: 10.1007/s10803-015-2662-8 26603886

23. Milton D. On the ontological status of autism: the ‘double empathy problem’, Disability & Society. 2012;27:6:883–87.

24. Karemaker JM. An introduction into autonomic nervous function. Physiol Meas. 2017;38(5),R89. doi: 10.1088/1361-6579/aa6782 28304283

25. Laborde S, Mosley E, Thayer JF. Heart rate variability and cardiac vagal tone in psychophysiological research–recommendations for experiment planning, data analysis, and data reporting. Front Psychol. 2017;8,213. doi: 10.3389/fpsyg.2017.00213 28265249

26. Saghir H, Dupuis A, Chau T, Kushki A. Atypical autonomic nervous system complexity accompanies social cognition task performance in ASD. Res Aut Spect Dis, 2017;39(Supplement C),54–62.

27. Kushki A, Drumm E, Pla Mobarak M, Tanel N, Dupuis A, Chau T, et al. Investigating the autonomic nervous system response to anxiety in children with autism spectrum disorders. PLoS ONE. 2013;8(4),e59730. doi: 10.1371/journal.pone.0059730 23577072

28. Ming X, Patel R, Kang V, Chokroverty S, Julu PO. Respiratory and autonomic dysfunction in children with autism spectrum disorders. Brain Dev. 2016;38(2),225–32. doi: 10.1016/j.braindev.2015.07.003 26235973

29. Jansen LMC, Gispen-De Wied CC, Wiegant VM, Westenberg HGM, Lahuis BE, Van Engeland H. Autonomic and neuroendocrine responses to a psychosocial stressor in adults with autistic spectrum disorder. J Aut Dev Dis. 2006;36(7),891–99.

30. Smeekens I, Didden R, Verhoeven EWM. Exploring the relationship of autonomic and endocrine activity with social functioning in adults with autism spectrum disorders. J Aut Dev Dis, 2015;45(2),495–505.

31. Porges SW, Macellaio M, Stanfill SD, McCue K, Lewis GF, Harden ER, et al. Respiratory sinus arrhythmia and auditory processing in autism: modifiable deficits of an integrated social engagement system? Int J Psychophy. 2013;88(3),261–70.

32. Neuhaus E, Bernier R, Beauchaine TP. Brief report: social skills, internalizing and externalizing symptoms, and respiratory sinus arrhythmia in autism. J Aut Dev Dis. 2014;44(3),730–7.

33. Harder R., Malow BA, Goodpaster RL, Iqbal F, Halbower A, Goldman SE, et al. Heart rate variability during sleep in children with autism spectrum disorder. Clin Auton Res. 2016;26(6):423–32. doi: 10.1007/s10286-016-0375-5 27491489

34. Mathersul D, McDonald S, Rushby JA. Automatic facial responses to affective stimuli in high-functioning adults with autism spectrum disorder. Physiol Beh, 2013a;109,14–22.

35. Mathersul D, McDonald S, Rushby JA. Psychophysiological correlates of social judgement in high-functioning adults with autism spectrum disorder. Int J Psychophy, 2013b;87(1),88–94.

36. Hubert BE, Wicker B, Monfardini E, Deruelle C. Electrodermal reactivity to emotion processing in adults with autistic spectrum disorders. Aut. 2009;13(1),9–19.

37. Kylliäinen A. Hietanen JK. Skin conductance responses to another person’s gaze in children with autism. J Aut Dev Dis. 2006;36(4),517–25.

38. Kaartinen M, Puura K, Mäkelä T, Rannisto M, Lemponen R, Helminen M, et al. Autonomic arousal to direct gaze correlates with social impairments among children with ASD. J Aut Dev Dis. 2012;42(9),1917–27.

39. O’Haire M, Mckenzie S, Beck A, Slaughter V. Animals may act as social buffers: skin conductance arousal in children with autism spectrum disorder in a social context. Dev Psychol. 2015;57(5),584–95.

40. Sullivan HS. The interpersonal theory of psychiatry. New York: Norton; 1953.

41. Leary T. Interpersonal diagnosis of personality. New York: Ronald Press; 1957.

42. Carson RC. Interaction concepts of personality. Chicago, IL: Aldine; 1969.

43. Kiesler DJ. The 1982 Interpersonal Circle: a taxonomy for complementarity in human transactions. Psychol Rev. 1983;90(3),185–214.

44. Kiesler DJ. Contemporary interpersonal theory and research: Personality, psychopathology, and psychotherapy. New York, NY: Wiley; 1996.

45. Wiggins JS. Circumplex models of interpersonal behavior in clinical psychology. In: Kendall PC, Butcher JN, editors. Handbook of research methods in clinical psychology. New York: Wiley; 1982. pp. 183–221.

46. Widiger TA. Personality, interpersonal circumplex, and DSM-5: a commentary on five studies. J Pers Assess. 2010;92,528–32. doi: 10.1080/00223891.2010.513707 20954054

47. Yaughn E, Nowicki S. Close relationships and complementary interpersonal styles among men and women. J Soc Psychol. 1999;139,473–8.

48. Gurtman MB. Interpersonal complementarity: Integrating interpersonal measurement with interpersonal models. J Coun Psychol. 2001;48(1):97–110.

49. Smith JL, Ruiz JM. Interpersonal orientation in context: correlates and effects of interpersonal complementarity on subjective and cardiovascular experiences. J Pers, 2007;75,679–708. doi: 10.1111/j.1467-6494.2007.00453.x 17576355

50. Sadler P, Ethier N, Gunn GR, Duong D, Woody E. Are we on the same wavelength? Complementarity as shared cyclical patterns within an interaction. J Pers Soc Psychol. 2009;97,1005–20. doi: 10.1037/a0016232 19968416

51. Lizdek I, Sadler P, Woody E, Ethier N, & Malet G. Capturing the stream of behavior: a computer-joystick method for coding interpersonal behavior continuously over time. Soc Sci Comp Rev. 2012;30,513–21.

52. Voutilainen L, Henttonen P, Kahri M, Kivioja M, Ravaja N, Sams M et al. Affective stance, ambivalence, and psychophysiological responses during conversational storytelling. Journal of Pragmatics. 2012;68:1–24.

53. Attwood T. Asperger’s syndrome: A guide for parents and professionals. London: Kingsley; 1998.

54. World Health Organization. ICD-10, the ICD-10 classification of mental and behavioural disorders: Diagnostic criteria for research. Geneva: World Health Organization; 1993.

55. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Aut Dev Dis. 2001;31(1):5–17.

56. Baron-Cohen S, Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Aut Dev Dis. 2004;34(2):163–75.

57. Baron-Cohen S, Richler J, Bisarya D, Gurunathan N, Wheelwright S. The systemizing quotient: an investigation of adults with Asperger syndrome or high–functioning autism, and normal sex differences. Phil Trans R Soc Lond B Biol Sci. 2003;358(1430):361–74.

58. Wechsler D. Wechsler Adult Intelligence Scale–Revised (WAIS-R). New York: The Psychological Corporation; 1981. Finnish translation. Translated and adapted by permission. Helsinki: Psykologien Kustannus Oy; 1992.

59. Berntson GG, Quigley KS, Lozano D. Cardiovascular psychophysiology. In: Cacioppo JT, Tassinary LG, Berntson GG, editors. Handbook of psychophysiology. 3rd ed. Cambridge: Cambridge University Press; 2007. pp. 182–210.

60. Malik M. Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur. Heart J. 1996;17:354–81. 8737210

61. Sadler P, Woody E McDonald K, Lizdek I, Little J. A lot can happen in a few minutes: examining dynamic patterns within an interaction to illuminate the interpersonal nature of personality disorders. J Pers Dis. 2015;29(4),526–46.

62. Stevanovic M, Henttonen P, Koski S, Kahri M, Voutilainen L, Koskinen E, et al. On the Asperger experience of interaction: interpersonal dynamics in dyadic conversations. J Aut. 2017;4(2). http://dx.doi.org/10.7243/2054-992X-4-2

63. Brainard DH, Vision S. The psychophysics toolbox. Spat Vis. 1997;10(4):433–6. 9176952

64. Pelli DG. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis. 1997;10(4),437–42. 9176953

65. Kleiner M, Brainard D, Pelli D, Ingling A, Murray R, Broussard C. What’s new in psychtoolbox-3. Perception. 2007;36(14):1–16.

66. Cronbach LJ. Coefficient alpha and the internal structure of tests. Psychometrika. 1951;16(3):297–334.

67. Nunnally JC, Bernstein I. Psychometric theory. 3rd ed. New York, NY: McGraw-Hill; 1994.

68. George D, Mallery P. SPSS for Windows step by step: A simple guide and reference. 11.0 update. 4th ed. Boston: Allyn & Bacon; 2003.

69. De Carvalho JL, Da Rocha AF, de Oliveira Nascimento FA, Neto JS, Junqueira LF. Development of a Matlab software for analysis of heart rate variability. In: Proceedings of the 6th IEEE International conference on signal processing, 2002; Beijing, China. pp. 1488–91.

70. Kenny DA, Kashy DA, Cook WL, Simpson JA. Dyadic data analysis. Methodology in the social sciences. New York, NY: Guilford; 2006.

71. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57(1):289–300.

72. Hatfield E, Cacioppo JT, Rapson RL. Emotional contagion. Cambridge, UK:CUP; 1994.

73. Hobson RP, Lee A. Hello and goodbye: a study of social engagement in autism. J Aut Dev Dis. 1998;28(2),117–27.

74. Hobson RP. The cradle of thought. London: Macmillan; 2002.

75. Gutstein SE. Autism/Aspergers: Solving the Relationship Puzzle. Arlington, TX: Future Horizons; 2001.

76. Ke F, Whalon K, Yun J. Social skill interventions for youth and adults with autism spectrum disorder: a systematic review. Rev Ed Res. 2018;88(1),3–42.

Physiological responses to affiliation during conversation: Comparing neurotypical males and males with Asperger syndrome

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz