Autistic Traits Affect Reward Anticipation but not Reception.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
21 05 2020
21 05 2020
Historique:
received:
23
05
2019
accepted:
22
04
2020
entrez:
23
5
2020
pubmed:
23
5
2020
medline:
15
1
2021
Statut:
epublish
Résumé
Autism spectrum conditions (ASC) have been linked to aberrant reward processing, but it remains unclear whether it is a general dysfunction or limited to social stimuli, and whether it affects both phases of reward processing, namely anticipation and reception. We used event-related brain potentials and a population-based approach to investigate reward anticipation and reception to socially relevant (i.e., picture of experimenter's face showing approval/disapproval) and monetary rewards in 51 neurotypical individuals with varying levels of autistic traits. Higher autistic traits were associated with enhanced reward anticipation across reward types in the early anticipation phase (triggered by incentive cues), but not in the late anticipation phase (directly before reward reception), as reflected by the CNV component. The P3 component in response to reward reception showed a general increase for monetary outcomes, which was not modulated by autistic traits. These results suggest that higher autistic traits are related to enhanced reward anticipation, but do not modulate reward reception. No interaction between reward types and autistic traits was observed. We propose that the relevance of social rewards had higher reward value than commonly used pictures of strangers, which specifically normalised responses for individuals with high autistic traits.
Identifiants
pubmed: 32440002
doi: 10.1038/s41598-020-65345-x
pii: 10.1038/s41598-020-65345-x
pmc: PMC7242422
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8396Références
American Psychiatric Association. American Psychiatric Association, 2013. Diagnostic and statistical manual of mental disorders (5th ed.). American Journal of Psychiatry (2013).
Schultz, R. T. Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience 23, 125–141 (2005).
pubmed: 15749240
doi: 10.1016/j.ijdevneu.2004.12.012
Dawson, G., Webb, S. J. & McPartland, J. Understanding the Nature of Face Processing Impairment in Autism: Insights From Behavioral and Electrophysiological Studies. Dev. Neuropsychol. 27, 403–424 (2005).
pubmed: 15843104
doi: 10.1207/s15326942dn2703_6
Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S. & Schultz, R. T. The social motivation theory of autism. Trends in Cognitive Sciences 16, 231–238 (2012).
pubmed: 22425667
pmcid: 3329932
doi: 10.1016/j.tics.2012.02.007
Dziobek, I., Bahnemann, M., Convit, A. & Heekeren, H. R. The Role of the Fusiform-Amygdala System in the Pathophysiology of Autism. Arch. Gen. Psychiatry 67, 397–405 (2010).
pubmed: 20368515
doi: 10.1001/archgenpsychiatry.2010.31
Scott-Van Zeeland, A. A., Dapretto, M., Ghahremani, D. G., Poldrack, R. A. & Bookheimer, S. Y. Reward processing in autism. Autism Res. 3, 53–67 (2010).
pubmed: 20437601
pmcid: 3076289
Kohls, G. et al. Reward system dysfunction in autism spectrum disorders. Soc. Cogn. Affect. Neurosci. 8, 565–572 (2013).
pubmed: 22419119
doi: 10.1093/scan/nss033
Kohls, G. et al. Atypical brain responses to reward cues in autism as revealed by event-related potentials. J. Autism Dev. Disord. 41, 1523–2533 (2011).
pubmed: 21290174
doi: 10.1007/s10803-011-1177-1
Dichter, G. & Adolphs, R. Reward processing in autism: a thematic series. J. Neurodev. Disord. 4 (2012).
Kohls, G., Antezana, L., Mosner, M. G., Schultz, R. T. & Yerys, B. E. Altered reward system reactivity for personalized circumscribed interests in autism. Mol. Autism 9 (2018).
Pankert, A., Pankert, K., Herpertz-Dahlmann, B., Konrad, K. & Kohls, G. Responsivity to familiar versus unfamiliar social reward in children with autism. J. Neural Transm. 121, 1199–1210 (2014).
pubmed: 24728874
doi: 10.1007/s00702-014-1210-6
Constantino, J. N. & Todd, R. D. Autistic Traits in the General Population: a Twin Study. Arch. Gen. Psychiatry 60, 524–530 (2003).
pubmed: 12742874
doi: 10.1001/archpsyc.60.5.524
Hurley, R. S. E., Losh, M., Parlier, M., Reznick, J. S. & Piven, J. The broad autism phenotype questionnaire. J. Autism Dev. Disord. 37, 1679–1690 (2007).
pubmed: 17146701
doi: 10.1007/s10803-006-0299-3
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. Autism Dev. Disord. 31, 5–17 (2001).
pubmed: 11439754
doi: 10.1023/A:1005653411471
Dichter, G. S., Richey, J. A., Rittenberg, A. M., Sabatino, A. & Bodfish, J. W. Reward circuitry function in autism during face anticipation and outcomes. J. Autism Dev. Disord. 42, 147–160 (2012).
pubmed: 22187105
doi: 10.1007/s10803-011-1221-1
Cox, A. et al. Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials. Soc. Cogn. Affect. Neurosci. 10, 1357–1364 (2015).
pubmed: 25752905
pmcid: 4590535
doi: 10.1093/scan/nsv024
Carter Leno, V., Naples, A., Cox, A., Rutherford, H. & Mcpartland, J. C. Common and distinct modulation of electrophysiological indices of feedback processing by autistic and psychopathic traits. Soc. Neurosci. 11, 455–466 (2016).
pubmed: 26471250
doi: 10.1080/17470919.2015.1108223
Pierce, K., Haist, F., Sedaghat, F. & Courchesne, E. The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain 127, 2703–2716 (2004).
pubmed: 15319275
doi: 10.1093/brain/awh289
Bellini, S. The Development of Social Anxiety in Adolescents With Autism Spectrum Disorders. Focus Autism Other Dev. Disabl. 21, 138–145 (2006).
doi: 10.1177/10883576060210030201
Moser, J. S., Huppert, J. D., Duval, E. & Simons, R. F. Face processing biases in social anxiety: An electrophysiological study. Biol. Psychol. 78, 93–103 (2008).
pubmed: 18353522
doi: 10.1016/j.biopsycho.2008.01.005
Berridge, K. C., Robinson, T. E. & Aldridge, J. W. Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr. Opin. Pharmacol. 9, 65–73 (2009).
pubmed: 19162544
pmcid: 2756052
doi: 10.1016/j.coph.2008.12.014
Beck, A. et al. Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics. Biol. Psychiatry 66, 734–742 (2009).
pubmed: 19560123
doi: 10.1016/j.biopsych.2009.04.035
Richey, J. A. et al. Common and distinct neural features of social and non-social reward processing in autism and social anxiety disorder. Soc. Cogn. Affect. Neurosci. 9, 367–377 (2014).
pubmed: 23223206
doi: 10.1093/scan/nss146
Stavropoulos, K. K. M. & Carver, L. J. Reward anticipation and processing of social versus nonsocial stimuli in children with and without autism spectrum disorders. J. Child Psychol. Psychiatry 55, 1398–1408 (2014).
pubmed: 24890037
doi: 10.1111/jcpp.12270
Dichter, G. S. et al. Reward circuitry function in autism spectrum disorders. Soc. Cogn. Affect. Neurosci. 7, 160–172 (2012).
pubmed: 21148176
doi: 10.1093/scan/nsq095
Schmitz, N. et al. Neural correlates of reward in autism. Br. J. Psychiatry 192, 19–24 (2008).
pubmed: 18174503
doi: 10.1192/bjp.bp.107.036921
Gonzalez-Gadea, M. L. et al. Neural markers of social and monetary rewards in children with Attention-Deficit/Hyperactivity Disorder and Autism Spectrum Disorder. Sci. Rep. 6, 30588 (2016).
pubmed: 27464551
pmcid: 4964357
doi: 10.1038/srep30588
Larson, M. J., South, M., Krauskopf, E., Clawson, A. & Crowley, M. J. Feedback and reward processing in high-functioning autism. Psychiatry Res. 187, 198–203 (2011).
pubmed: 21122921
doi: 10.1016/j.psychres.2010.11.006
McPartland, J. C. et al. Preserved reward outcome processing in ASD as revealed by event-related potentials. J. Neurodev. Disord. 4, 0 (2012).
doi: 10.1186/1866-1955-4-16
Groen, Y. et al. Error and feedback processing in children with ADHD and children with Autistic Spectrum Disorder: An EEG event-related potential study. Clin. Neurophysiol. 119, 2476–2493 (2008).
pubmed: 18824404
doi: 10.1016/j.clinph.2008.08.004
Grey Walter, W., Cooper, R., Aldridge, V. J., McCallum, W. C. & Winter, A. L. Contingent Negative Variation: an Electric Sign of Sensori-motor Association and Expectancy in the Human Brain. Nature 203, 380–384 (1964).
doi: 10.1038/203380a0
Broyd, S. J. et al. An electrophysiological Monetary Incentive Delay (e-MID) task: A way to decompose the different components of neural response to positive and negative monetary reinforcement. J. Neurosci. Methods 209, 40–49 (2012).
pubmed: 22659003
doi: 10.1016/j.jneumeth.2012.05.015
Wu, Y. & Zhou, X. The P300 and reward valence, magnitude, and expectancy in outcome evaluation. Brain Res. 1286, 114–122 (2009).
pubmed: 19539614
doi: 10.1016/j.brainres.2009.06.032
Knutson, B., Westdorp, A., Kaiser, E. & Hommer, D. FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task. Neuroimage 12, 20–27 (2000).
pubmed: 10875899
doi: 10.1006/nimg.2000.0593
Stavropoulos, K. K. M. & Carver, L. J. Effect of Familiarity on Reward Anticipation in Children with and without Autism Spectrum Disorders. PLoS One 9, e106667 (2014).
pubmed: 25184524
pmcid: 4153666
doi: 10.1371/journal.pone.0106667
Oumeziane, B. A., Schryer-Praga, J. & Foti, D. “Why don’t they ‘like’ me more?”: Comparing the time courses of social and monetary reward processing. Neuropsychologia 107, 48–59 (2017).
doi: 10.1016/j.neuropsychologia.2017.11.001
Oldfield, R. C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).
pubmed: 5146491
doi: 10.1016/0028-3932(71)90067-4
Nuske, H. J., Vivanti, G. & Dissanayake, C. Are emotion impairments unique to, universal, or specific in autism spectrum disorder? A comprehensive review. Cogn. Emot. 27, 1042–1061 (2013).
pubmed: 23387530
doi: 10.1080/02699931.2012.762900
Carver, C. S. & White, T. L. Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales. J. Pers. Soc. Psychol. 67, 319–333 (1994).
doi: 10.1037/0022-3514.67.2.319
Liebowitz, M. R., Gorman, J. M., Fyer, A. J. & Klein, D. F. Social Phobia: Review of a Neglected Anxiety Disorder. Arch. Gen. Psychiatry 42, 729–736 (1985).
pubmed: 2861796
doi: 10.1001/archpsyc.1985.01790300097013
South, M., Dana, J., White, S. E. & Crowley, M. J. Failure is not an option: Risk-taking is moderated by anxiety and also by cognitive ability in children and adolescents diagnosed with an autism spectrum disorder. J. Autism Dev. Disord. 41, 55–65 (2011).
pubmed: 20414800
doi: 10.1007/s10803-010-1021-z
South, M., Larson, M. J., Krauskopf, E. & Clawson, A. Error processing in high-functioning Autism Spectrum Disorders. Biol. Psychol. 85, 242–251 (2010).
pubmed: 20654684
doi: 10.1016/j.biopsycho.2010.07.009
Cremers, H. R., Veer, I. M., Spinhoven, P., Rombouts, S. A. R. B. & Roelofs, K. Neural sensitivity to social reward and punishment anticipation in social anxiety disorder. Front. Behav. Neurosci. 8, 1–9 (2015).
doi: 10.3389/fnbeh.2014.00439
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing (2017). Available at: http://www.r-project.org .
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Softw. 82, R package version 2.0-6 (2017).
Akaike, H. Information Theory and an Extension of the Maximum Likelihood Principle. in Selected Papers of Hirotugu Akaike. Springer Series in Statistics (Perspectives in Statistics) (eds. Parzen, E., Tanabe, K. & Kitagawa, G.) 199–213 (Springer, New York, NY, 1998).
Panasiti, M. S., Puzzo, I. & Chakrabarti, B. Autistic Traits Moderate the Impact of Reward Learning on Social Behaviour. Autism Res. 9, 471–479 (2016).
pubmed: 26280134
doi: 10.1002/aur.1523
Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).
doi: 10.1111/j.2041-210x.2012.00261.x
Rights, J. D. & Sterba, S. K. Quantifying Explained Variance in Multilevel Models: An Integrative Framework for Defining R-Squared Measures. Psychol. Methods (2018).
Pek, J. & Flora, D. B. Reporting effect sizes in original psychological research: A discussion and tutorial. Psychol. Methods 23, 208–225 (2018).
pubmed: 28277690
doi: 10.1037/met0000126
Bottini, S. Social reward processing in individuals with autism spectrum disorder: A systematic review of the social motivation hypothesis. Research in Autism Spectrum Disorders (2018).
Delmonte, S. et al. Social and monetary reward processing in autism spectrum disorders. Mol. Autism 3, (2012).
Sepeta, L. et al. Abnormal social reward processing in autism as indexed by pupillary responses to happy faces. J. Neurodev. Disord. 4, 17 (2012).
pubmed: 22958650
pmcid: 3461481
doi: 10.1186/1866-1955-4-17
Nuske, H. J., Vivanti, G. & Dissanayake, C. Reactivity to fearful expressions of familiar and unfamiliar people in children with autism: an eye-tracking pupillometry study. J. Neurodev. Disord. 6, 14 (2014).
pubmed: 24982695
pmcid: 4064262
doi: 10.1186/1866-1955-6-14
Stavropoulos, K. K. M., Viktorinova, M., Naples, A., Foss-Feig, J. & Mcpartland, J. C. Autistic traits modulate conscious and nonconscious face perception. Soc. Neurosci. 13, 40–51 (2018).
pubmed: 27750521
doi: 10.1080/17470919.2016.1248788
Foulkes, L., Bird, G., Gökçen, E., McCrory, E. & Viding, E. Common and distinct impacts of autistic traits and alexithymia on social reward. PLoS One 10, e0121018 (2015).
pubmed: 25853670
pmcid: 4390314
doi: 10.1371/journal.pone.0121018
Haffey, A., Press, C., O’Connell, G. & Chakrabarti, B. Autistic Traits Modulate Mimicry of Social but not Nonsocial Rewards. Autism Res. 6, 614–620 (2013).
pubmed: 23939872
doi: 10.1002/aur.1323
Puzzo, I., Cooper, N. R., Vetter, P. & Russo, R. EEG activation differences in the pre-motor cortex and supplementary motor area between normal individuals with high and low traits of autism. Brain Res. 1342, 104–110 (2010).
pubmed: 20435023
doi: 10.1016/j.brainres.2010.04.060
Brunia, C. H. M., van Boxtel, G. J. M. & Böcker, K. B. E. Negative Slow Waves as Indices of Anticipation: The Bereitschaftspotential, the Contingent Negative Variation, and the Stimulus-Preceding Negativity. in The Oxford Handbook of Event-Related Potential Components (2012).
Dawson, G., Osterling, J., Rinaldi, J., Carver, L. & McPartland, J. Brief Report: Recognition Memory and Stimulus-Reward Associations: Indirect Support for the Role of Ventromedial Prefrontal Dysfunction in Autism. J. Autism Dev. Disord. 31, 337–341 (2001).
pubmed: 11518486
doi: 10.1023/A:1010751404865
Kohls, G., Peltzer, J., Herpertz-Dahlmann, B. & Konrad, K. Differential effects of social and non-social reward on response inhibition in children and adolescents. Dev. Sci. 12, 614–625 (2009).
pubmed: 19635087
doi: 10.1111/j.1467-7687.2009.00816.x
Goldstein, R. Z. et al. The effect of graded monetary reward on cognitive event-related potentials and behavior in young healthy adults. Int. J. Psychophysiol. 62, 272–279 (2006).
pubmed: 16876894
pmcid: 2424251
doi: 10.1016/j.ijpsycho.2006.05.006
Balodis, I. M. & Potenza, M. N. Anticipatory Reward Processing in Addicted Populations: A Focus on the Monetary Incentive Delay Task. Biol. Psychiatry 77, 434–444 (2015).
pubmed: 25481621
doi: 10.1016/j.biopsych.2014.08.020
Insel, T. et al. Research Domain Criteria (RDoC): Toward a New Classification Framework for Research on Mental Disorders. Am. J. Psychiatry 167, 748–751 (2010).
pubmed: 20595427
doi: 10.1176/appi.ajp.2010.09091379