Yonsei Med J.  2015 May;56(3):705-711. 10.3349/ymj.2015.56.3.705.

Abnormal Brain Activity in Social Reward Learning in Children with Autism Spectrum Disorder: An fMRI Study

Affiliations
  • 1Neuroscience Research Institute, Gachon University of Medicine and Science, Incheon, Korea.
  • 2Division of Child and Adolescent Psychiatry, Department of Psychiatry and Institute of Behavioral Science in Medicine, Yonsei Autism Laboratory, Yonsei University College of Medicine, Seoul, Korea. kacheon@yuhs.ac
  • 3Department of Art Therapy, Daegu Cyber University, Daegu, Korea.
  • 4Department of Psychiatry, Konyang University College of Medicine, Daejeon, Korea.

Abstract

PURPOSE
We aimed to determine whether Autism Spectrum Disorder (ASD) would show neural abnormality of the social reward system using functional MRI (fMRI).
MATERIALS AND METHODS
27 ASDs and 12 typically developing controls (TDCs) participated in this study. The social reward task was developed, and all participants performed the task during fMRI scanning.
RESULTS
ASDs and TDCs with a social reward learning effect were selected on the basis of behavior data. We found significant differences in brain activation between the ASDs and TDCs showing a social reward learning effect. Compared with the TDCs, the ASDs showed reduced activity in the right dorsolateral prefrontal cortex, right orbitofrontal cortex, right parietal lobe, and occipital lobe; however, they showed increased activity in the right parahippocampal gyrus and superior temporal gyrus.
CONCLUSION
These findings suggest that there might be neural abnormality of the social reward learning system of ASDs. Although this study has several potential limitations, it presents novel findings in the different neural mechanisms of social reward learning in children with ASD and a possible useful biomarker of high-functioning ASDs.

Keyword

ASDs; social reward leaning; fMRI

MeSH Terms

Brain/*physiopathology
Brain Mapping
Case-Control Studies
Child
Child Development Disorders, Pervasive/*physiopathology
Female
Functional Neuroimaging/*methods
Humans
Magnetic Resonance Imaging/methods
Male
Neural Pathways/*physiopathology
Psychiatric Status Rating Scales
Republic of Korea
*Reward
*Social Behavior

Figure

  • Fig. 1 Behavioral results of the subjects. (A) Comparison between the ASDs and TDCs who showed a social reward learning effect. There was no significant difference between the two groups. (B) Comparison between different ASDs subgroups. LE, subgroup with a social reward learning effect; nLE, subgroup without a social reward learning effect; ASD, Autism Spectrum Disorder; TDC, typically developing control.

  • Fig. 2 Different brain activation maps of ASDs and TDCs with a social reward learning effect. (A) Different brain activation maps of the ASDs> the TDCs contrast. The parahippocampal gyrus and superior temporal cortex were observed (ANOVA analysis with random effect GLM, p<0.01, uncorrected). (B) Different brain activation maps of the TDCs> the ASDs contrast. The dorsolateral prefrontal cortex, orbitofrontal cortex and parietal lobe were observed (ANOVA analysis with random effect GLM, p<0.01, uncorrected). ANOVA, analysis of variance; GLM, general linear model; ASD, Autism Spectrum Disorder; TDC, typically developing control; PG, parahippocampal gyrus; STG, superior temporal gyrus; DLPFC, dorsolateral prefrontal cortex; OFC, orbitofrontal cortex.


Reference

1. Seol KI, Song SH, Kim KL, Oh ST, Kim YT, Im WY, et al. A comparison of receptive-expressive language profiles between toddlers with autism spectrum disorder and developmental language delay. Yonsei Med J. 2014; 55:1721–1728.
Article
2. Samson AC, Phillips JM, Parker KJ, Shah S, Gross JJ, Hardan AY. Emotion dysregulation and the core features of autism spectrum disorder. J Autism Dev Disord. 2014; 44:1766–1772.
Article
3. Dichter GS. Functional magnetic resonance imaging of autism spectrum disorders. Dialogues Clin Neurosci. 2012; 14:319–351.
Article
4. Dalton KM, Holsen L, Abbeduto L, Davidson RJ. Brain function and gaze fixation during facial-emotion processing in fragile X and autism. Autism Res. 2008; 1:231–239.
Article
5. Doyle-Thomas KA, Goldberg J, Szatmari P, Hall GB. Neurofunctional underpinnings of audiovisual emotion processing in teens with autism spectrum disorders. Front Psychiatry. 2013; 4:48.
Article
6. Greimel E, Nehrkorn B, Fink GR, Kukolja J, Kohls G, Müller K, et al. Neural mechanisms of encoding social and non-social context information in autism spectrum disorder. Neuropsychologia. 2012; 50:3440–3449.
Article
7. von dem Hagen EA, Stoyanova RS, Baron-Cohen S, Calder AJ. Reduced functional connectivity within and between 'social' resting state networks in autism spectrum conditions. Soc Cogn Affect Neurosci. 2013; 8:694–701.
Article
8. Jones TB, Bandettini PA, Kenworthy L, Case LK, Milleville SC, Martin A, et al. Sources of group differences in functional connectivity: an investigation applied to autism spectrum disorder. Neuroimage. 2010; 49:401–414.
Article
9. Monk CS, Peltier SJ, Wiggins JL, Weng SJ, Carrasco M, Risi S, et al. Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage. 2009; 47:764–772.
Article
10. Chevallier C, Kohls G, Troiani V, Brodkin ES, Schultz RT. The social motivation theory of autism. Trends Cogn Sci. 2012; 16:231–239.
Article
11. Sakagami M, Watanabe M. Integration of cognitive and motivational information in the primate lateral prefrontal cortex. Ann N Y Acad Sci. 2007; 1104:89–107.
Article
12. Scott-Van Zeeland AA, Dapretto M, Ghahremani DG, Poldrack RA, Bookheimer SY. Reward processing in autism. Autism Res. 2010; 3:53–67.
Article
13. Gunji A, Goto T, Kita Y, Sakuma R, Kokubo N, Koike T, et al. Facial identity recognition in children with autism spectrum disorders revealed by P300 analysis: a preliminary study. Brain Dev. 2013; 35:293–298.
Article
14. Fan YT, Chen C, Chen SC, Decety J, Cheng Y. Empathic arousal and social understanding in individuals with autism: evidence from fMRI and ERP measurements. Soc Cogn Affect Neurosci. 2014; 9:1203–1213.
Article
15. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. Washington, DC: American Psychiatric Association;2000.
16. Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, et al. Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. J Autism Dev Disord. 2003; 33:427–433.
17. Constantino JN, Todd RD. Genetic structure of reciprocal social behavior. Am J Psychiatry. 2000; 157:2043–2045.
Article
18. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994; 24:659–685.
Article
19. Lord C, Risi S, Lambrecht L, Cook EH Jr, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000; 30:205–223.
20. Eshel N, Nelson EE, Blair RJ, Pine DS, Ernst M. Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia. 2007; 45:1270–1279.
Article
21. Teixeira S, Machado S, Velasques B, Sanfim A, Minc D, Peressutti C, et al. Integrative parietal cortex processes: neurological and psychiatric aspects. J Neurol Sci. 2014; 338:12–22.
Article
22. Murphy ER, Foss-Feig J, Kenworthy L, Gaillard WD, Vaidya CJ. Atypical Functional Connectivity of the Amygdala in Childhood Autism Spectrum Disorders during Spontaneous Attention to Eye-Gaze. Autism Res Treat. 2012; 2012:652408.
Article
23. Ross B. A novel type of auditory responses: temporal dynamics of 40-Hz steady-state responses induced by changes in sound localization. J Neurophysiol. 2008; 100:1265–1277.
Article
24. Just MA, Cherkassky VL, Keller TA, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain. 2004; 127(Pt 8):1811–1821.
Article
25. Paquette V, Lévesque J, Mensour B, Leroux JM, Beaudoin G, Bourgouin P, et al. "Change the mind and you change the brain": effects of cognitive-behavioral therapy on the neural correlates of spider phobia. Neuroimage. 2003; 18:401–409.
Article
26. Pagani M, Manouilenko I, Stone-Elander S, Odh R, Salmaso D, Hatherly R, et al. Brief Report: alterations in cerebral blood flow as assessed by PET/CT in adults with autism spectrum disorder with normal IQ. J Autism Dev Disord. 2012; 42:313–318.
Article
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