Influences of heart rate feedback and autistic traits on affective mindreading.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 08 2024
13 08 2024
Historique:
received:
31
05
2023
accepted:
30
07
2024
medline:
14
8
2024
pubmed:
14
8
2024
entrez:
13
8
2024
Statut:
epublish
Résumé
Although mindreading is an important prerequisite for successful social interactions, the underlying mechanisms are still matter of debate. It is unclear, for example, if inferring others' and own mental states are distinct processes or are based on a common mechanism. Using an affect-induction experimental set-up with an acoustic heart rate feedback that addresses affective mindreading in self and others, we investigated if non-autistic study participants relied on similar information for self- and other-directed mindreading. We assumed that due to altered mindreading capacities in autism, mainly individuals with low autistic traits would focus on additional sensory cues, such as heart rate, to infer their own and their gambling partner's affective states. Our analyses showed that the interpretation of a heart rate signal differed in self- and other-directed mindreading trials. This effect was modulated by autistic traits suggesting that individuals with higher autistic traits might not have interpreted the heart rate feedback for gambling partner ratings and differentiated less between self- and other-directed mindreading trials. We discuss these results in the context of a common mechanism underlying self- and other-directed mindreading and hypothesize that the weighting of internal and external sensory information might contribute to how we make sense of our and others' mental states.
Identifiants
pubmed: 39138278
doi: 10.1038/s41598-024-69038-7
pii: 10.1038/s41598-024-69038-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
18783Subventions
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : 337619223/RTG2386
Informations de copyright
© 2024. The Author(s).
Références
Baron-Cohen, S., Leslie, A. M. & Frith, U. Does the autistic child have a "theory of mind" ?. Cognition 21, 37–46 (1985).
pubmed: 2934210
doi: 10.1016/0010-0277(85)90022-8
Schurz, M. et al. Toward a hierarchical model of social cognition: A neuroimaging meta-analysis and integrative review of empathy and theory of mind. Psychological Bulletin, 147(3), 293–327. https://doi.org/10.1037/bul0000303 (2021).
doi: 10.1037/bul0000303
pubmed: 33151703
Kalbe, E. et al. Dissociating cognitive from affective theory of mind: A TMS study. Cortex 46, 769–780 (2010).
pubmed: 19709653
doi: 10.1016/j.cortex.2009.07.010
Carruthers, P. The Opacity of Mind: An Integrative Theory of Self-Knowledge. (Oxford University Press, 2011). https://doi.org/10.1093/acprof:oso/9780199596195.001.0001
Carruthers, P. Mindreading the self. in Understanding Other Minds: Perspectives from Developmental Social Neuroscience (ed. Baron-Cohen, S.) 467–486 (Oxford University Press, 2013).
Wells, G. L. & Petty, R. E. The effects of overt head movements on persuasion: Compatibility and incompatibility of responses. Basic Appl. Soc. Psych. 1, 219–230 (1980).
doi: 10.1207/s15324834basp0103_2
Gu, J., Zhong, C. B. & Page-Gould, E. Listen to your heart: When false somatic feedback shapes moral behavior. J. Exp. Psychol. Gen. 142, 307–312 (2013).
pubmed: 22889162
doi: 10.1037/a0029549
Jouffre, S. Power modulates over-reliance on false cardiac arousal when judging target attractiveness: The powerful are more centered on their own false arousal than the powerless. Personal. Soc. Psychol. Bull. 41, 116–126 (2015).
doi: 10.1177/0146167214559718
Nishimura, N., Ishi, A., Sato, M., Fukushima, S. & Kajimoto, H. Facilitation of affection by tactile feedback of false heratbeat. 2321–2326 (2012). https://doi.org/10.1145/2212776.2223796
World Health Organization (WHO). The ICD-10 Classification of Mental and Behavioural Disorders. (1993).
Zeidan, J. et al. Global prevalence of autism: A systematic review update. Autism Res. 15, 778–790 (2022).
pubmed: 35238171
pmcid: 9310578
doi: 10.1002/aur.2696
Maenner, M.et al. Prevalence and characteristics of autism spectrum disorder among children aged 8 years—Autism and developmental disabilities monitoring network, 11 sites, United States, 2020. MMWR Surveill. Summ. 72, 1–14 (2023).
pubmed: 36952289
pmcid: 10042614
doi: 10.15585/mmwr.ss7202a1
Brewer, N., Young, R. L. & Barnett, E. Measuring theory of mind in adults with autism spectrum disorder. J. Autism Dev. Disord. 47, 1927–1941 (2017).
pubmed: 28275927
pmcid: 5487761
doi: 10.1007/s10803-017-3080-x
Grainger, C., Williams, D. M. & Lind, S. E. Metacognition, metamemory, and mindreading in high-functioning adults with autism spectrum disorder. J. Abnorm. Psychol. 123, 650–659 (2014).
pubmed: 24955572
doi: 10.1037/a0036531
Rosenblau, G., Kliemann, D., Heekeren, H. R. & Dziobek, I. Approximating implicit and explicit mentalizing with two naturalistic video-based tasks in typical development and autism spectrum disorder. J. Autism Dev. Disord. 45, 953–965 (2015).
pubmed: 25267068
doi: 10.1007/s10803-014-2249-9
Rueda, P., Fernández-Berrocal, P. & Baron-Cohen, S. Dissociation between cognitive and affective empathy in youth with Asperger syndrome. Eur. J. Dev. Psychol. 12, 85–98 (2015).
doi: 10.1080/17405629.2014.950221
Schuwerk, T., Vuori, M. & Sodian, B. Implicit and explicit Theory of Mind reasoning in autism spectrum disorders: The impact of experience. Autism 19, 459–468 (2015).
pubmed: 24627427
doi: 10.1177/1362361314526004
Tomchek, S. D. & Dunn, W. Sensory processing in children with and without autism: A comparative study using the short sensory profile. Am. J. Occup. Ther. 61, 190–200 (2007).
pubmed: 17436841
doi: 10.5014/ajot.61.2.190
Crane, L., Goddard, L. & Pring, L. Sensory processing in adults with autism spectrum disorders. Autism 13, 215–228 (2009).
pubmed: 19369385
doi: 10.1177/1362361309103794
Williams, D. & Happé, F. Representing intentions in self and other: Studies of autism and typical development. Dev. Sci. 13, 307–319 (2010).
pubmed: 20136927
doi: 10.1111/j.1467-7687.2009.00885.x
Bradford, E. E. F., Jentzsch, I. & Gomez, J. C. From self to social cognition: Theory of Mind mechanisms and their relation to executive functioning. Cognition 138, 21–34 (2015).
pubmed: 25704580
doi: 10.1016/j.cognition.2015.02.001
Lombardo, M. V.et al. MRC AIMS Consortium & Baron-Cohen, S. Atypical neural self-representation in autism. Brain 133, 611–624 (2010).
pubmed: 20008375
doi: 10.1093/brain/awp306
Ochsner, K. N.et al.. Reflecting upon feelings: An fMRI study of neural systems supporting the attribution of emotion to self and other. J. Cogn. Neurosci. 16, 1746–1772 (2004).
pubmed: 15701226
doi: 10.1162/0898929042947829
Thaler, H.et al. Typical pain experience but underestimation of others’ pain: Emotion perception in self and others in autism spectrum disorder. Autism 22, 751–762 (2018).
doi: 10.1177/1362361317701269
pubmed: 28691518
Ong, D. C., Zaki, J. & Goodman, N. D. Affective cognition: Exploring lay theories of emotion. Cognition 143, 141–162 (2015).
pubmed: 26160501
doi: 10.1016/j.cognition.2015.06.010
Ong, D. C., Goodman, N. D. & Zaki, J. Happier than thou? A self-enhancement bias in emotion attribution. Emotion 18, 116–126 (2018).
pubmed: 28406680
doi: 10.1037/emo0000309
Gray, M. A., Harrison, N. A., Wiens, S. & Critchley, H. D. Modulation of emotional appraisal by false physiological feedback during fMRI. PLoS One 2, e546 (2007).
pubmed: 17579718
pmcid: 1890305
doi: 10.1371/journal.pone.0000546
Lenggenhager, B., Azevedo, R. T., Mancini, A. & Aglioti, S. M. Listening to your heart and feeling yourself: Effects of exposure to interoceptive signals during the ultimatum game. Exp. Brain Res. 230, 233–241 (2013).
pubmed: 23873493
doi: 10.1007/s00221-013-3647-5
Strain, A. C., Azevedo, R. & D’Mello, S. K. Using a false biofeedback methodology to explore relationships between learners’ affect, metacognition, and performance. Contemp. Educ. Psychol. 38, 22–39 (2013).
doi: 10.1016/j.cedpsych.2012.08.001
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.[erratum appears in J Autism Dev Disord 2001 Dec; 31(6):603]. J. Autism Dev. Disord. 31, 5–17 (2001).
pubmed: 11439754
doi: 10.1023/A:1005653411471
Shah, P., Livingston, L. A., Callan, M. J. & Player, L. Trait autism is a better predictor of empathy than alexithymia. J. Autism Dev. Disord. 49, 3956–3964 (2019).
pubmed: 31172339
pmcid: 6751139
doi: 10.1007/s10803-019-04080-3
Shalev, I. & Uzefovsky, F. Empathic disequilibrium in two different measures of empathy predicts autism traits in neurotypical population. Mol. Autism 11, 1–13 (2020).
doi: 10.1186/s13229-020-00362-1
Stewart, G. R., Wallace, G. L., Cottam, M. & Charlton, R. A. Theory of mind performance in younger and older adults with elevated autistic traits. Autism Res. 13, 751–762 (2020).
pubmed: 31520519
doi: 10.1002/aur.2206
Klin, A. Attributing social meaning to ambiguous visual stimuli in higher-functioning autism and Asperger syndrome: The social attribution task. J. Child Psychol. Psychiatry Allied Discip. 41, 831–846 (2000).
doi: 10.1111/1469-7610.00671
Wilson, A. C. Do animated triangles reveal a marked difficulty among autistic people with reading minds?. Autism 25, 1175–1186 (2021).
pubmed: 33618541
pmcid: 8264645
doi: 10.1177/1362361321989152
McCubbin, J. A.et al. Cardiovascular-emotional dampening: The relationship between blood pressure and recognition of emotion. Psychosom. Med. 73, 743–750 (2011).
pubmed: 22042880
pmcid: 3210914
doi: 10.1097/PSY.0b013e318235ed55
Pury, C. L. S., McCubbin, J. A., Helfer, S. G., Galloway, C. & McMullen, L. J. Elevated resting blood pressure and dampened emotional response. Psychosom. Med. 66, 583–587 (2004).
pubmed: 15272107
doi: 10.1097/01.psy.0000130490.57706.88
Tomkins, S. Affect imagery consciousness: Volume I: The positive affects. (Springer publishing company, 1962).
Pronin, E. Chapter 1 The Introspection Illusion. Adv. Exp. Soc. Psychol. 41, 1–67 (2009).
doi: 10.1016/S0065-2601(08)00401-2
Friston, K. A theory of cortical responses. Philos. Trans. R. Soc. B Biol. Sci. 360, 815–836 (2005).
doi: 10.1098/rstb.2005.1622
Seth, A. K. & Friston, K. J. Active interoceptive inference and the emotional brain. Philos. Trans. R. Soc. B Biol. Sci. 371, 1708 (2016).
doi: 10.1098/rstb.2016.0007
Seth, A. K. Interoceptive inference, emotion, and the embodied self. Trends Cogn. Sci. 17, 565–573 (2013).
pubmed: 24126130
doi: 10.1016/j.tics.2013.09.007
Garfinkel, S. N., Minati, L., Gray, M. A., Seth, A. K., Dolan, R. J. & Critchley, H. D. Fear from the heart: Sensitivity to fear stimuli depends on individual heartbeats. J. Neurosci. 34, 6573–6582 (2014).
pubmed: 24806682
pmcid: 4012313
doi: 10.1523/JNEUROSCI.3507-13.2014
Tomova, L., von Dawans, B., Heinrichs, M., Silani, G. & Lamm, C. Is stress affecting our ability to tune into others? Evidence for gender differences in the effects of stress on self-other distinction. Psychoneuroendocrinology 43, 95–104 (2014).
pubmed: 24703175
doi: 10.1016/j.psyneuen.2014.02.006
Dziobek, I.et al. Dissociation of cognitive and emotional empathy in adults with asperger syndrome using the multifaceted empathy test (MET). J. Autism Dev. Disord. 38, 464–473 (2008).
pubmed: 17990089
doi: 10.1007/s10803-007-0486-x
DuBois, D., Ameis, S. H., Lai, M. C., Casanova, M. F. & Desarkar, P. Interoception in autism spectrum disorder: A review. Int. J. Dev. Neurosci. 52, 104–111 (2016).
pubmed: 27269967
doi: 10.1016/j.ijdevneu.2016.05.001
Schilbach, L. Towards a second-person neuropsychiatry. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150081–20150116 (2016).
doi: 10.1098/rstb.2015.0081
Tei, S.et al. Egocentric biases and atypical generosity in autistic individuals. Autism Res. 12, 1598–1608 (2019).
doi: 10.1002/aur.2130
pubmed: 31102339
Lamm, C., Bukowski, H. & Silani, G. From shared to distinct self-other representations in empathy: Evidence from neurotypical function and socio-cognitive disorders. Philos. Trans. R. Soc. B Biol. Sci. 371, 1686 (2016).
doi: 10.1098/rstb.2015.0083
Iodice, P., Porciello, G., Bufalari, I., Barca, L. & Pezzulo, G. An interoceptive illusion of effort induced by false heart-rate feedback. Proc. Natl. Acad. Sci. USA 116, 13897–13902 (2019).
pubmed: 31235576
pmcid: 6628799
doi: 10.1073/pnas.1821032116
Garfinkel, S. N. & Critchley, H. D. Threat and the body: How the heart supports fear processing. Trends Cogn. Sci. 20, 34–46 (2016).
pubmed: 26628111
doi: 10.1016/j.tics.2015.10.005
Wacker, R., Bölte, S. & Dziobek, I. Women know better what other women think and feel: Gender effects on mindreading across the adult life span. Front. Psychol. 8, 1324 (2017).
pubmed: 28824503
pmcid: 5539187
doi: 10.3389/fpsyg.2017.01324
Bird, G. & Cook, R. Mixed emotions: The contribution of alexithymia to the emotional symptoms of autism. Transl. Psychiatry 3, 1–8 (2013).
doi: 10.1038/tp.2013.61
Taylor, G. J., Michael Bagby, R. & Parker, J. D. A. The alexithymia construct: A potential paradigm for psychosomatic medicine. Psychosomatics 32, 153–164 (1991).
pubmed: 2027937
doi: 10.1016/S0033-3182(91)72086-0
Shah, P., Hall, R., Catmur, C. & Bird, G. Alexithymia, not autism, is associated with impaired interoception. Cortex 81, 215–220 (2016).
pubmed: 27253723
pmcid: 4962768
doi: 10.1016/j.cortex.2016.03.021
Ellard, K. K., Farchione, T. J. & Barlow, D. H. Relative effectiveness of emotion induction procedures and the role of personal relevance in a clinical sample: A comparison of film, images, and music. J. Psychopathol. Behav. Assess. 34, 232–243 (2012).
pubmed: 34611377
doi: 10.1007/s10862-011-9271-4
Out, C., Goudbeek, M. & Krahmer, E. Gradual positive and negative affect induction: The effect of verbalizing affective content. PLoS One 15, 1–20 (2020).
doi: 10.1371/journal.pone.0233592
Uhrig, M. K.et al. Emotion elicitation: A comparison of pictures and films. Front. Psychol. 7, (2016).
Kulke, L. & Hinrichs, M. A. B. Implicit Theory of Mind under realistic social circumstances measured with mobile eye-tracking. Sci. Rep. 11, 1–13 (2021).
doi: 10.1038/s41598-020-80614-5
Drimalla, H. et al. Towards the automatic detection of social biomarkers in autism spectrum disorder: Introducing the simulated interaction task (SIT). npj Digit. Med. 3, 1–10 (2020).
doi: 10.1038/s41746-020-0227-5
Lombardo, M. V. et al. Shared neural circuits for mentalizing about the self and others. J. Cogn. Neurosci. 22, 1623–1635 (2009).
doi: 10.1162/jocn.2009.21287
Zalla, T.et al. Feelings of regret and disappointment in adults with high-functioning autism. Cortex 58, 112–122 (2014).
pubmed: 25010486
doi: 10.1016/j.cortex.2014.05.008
Trilla, I., Weigand, A. & Dziobek, I. Affective states influence emotion perception: Evidence for emotional egocentricity. Psychol. Res. 85, 1005–1015 (2021).
pubmed: 32206856
doi: 10.1007/s00426-020-01314-3
MathWorks Inc. MATLAB release notes for R2018a [Software]. Retrieved from https://www.mathworks.com/help/release-notes/r2018a.html. (2018).
Brainard, D. H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).
pubmed: 9176952
doi: 10.1163/156856897X00357
Pelli, D. G. The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spat. Vis. 10, 437–442 (1997).
pubmed: 9176953
doi: 10.1163/156856897X00366
Kleiner, M., Brainard, D. & Pelli, D. “What’s new in Psychtoolbox-3?” Perception 36, Abstract Supplement (2007).
Billig, M. & Tajfel, H. Social categorization and similarity in intergroup behaviour. Eur. J. Soc. Psychol. 3, 27–52 (1973).
doi: 10.1002/ejsp.2420030103
Long, A. E., Pinel, E. C. & Yawger, G. C. When shared group membership signifies shared subjective experience: I-sharing and the minimal group paradigm. J. Soc. Psychol. 157, 389–406 (2017).
pubmed: 27668756
doi: 10.1080/00224545.2016.1239610
R Core Team. R: A Language and Environment for Statistical Computing. (2019).
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R. C. T. nlme: Linear and Nonlinear Mixed Effects Models. (2019).
Sen, S. & Bradshaw, L. Comparison of relative fit indices for diagnostic model selection. Appl. Psychol. Meas. 41, 422–438 (2017).
pubmed: 29881100
pmcid: 5978522
doi: 10.1177/0146621617695521