Neural Mechanisms of Reward Prediction Error in Autism Spectrum Disorder

Maya G Mosner, R Edward McLaurin, Jessica L Kinard, Shabnam Hakimi, Jacob Parelman, Jasmine S Shah, Joshua Bizzell, Rachel K Greene, Paul M Cernasov, Erin Walsh, Merideth A Addicott, Tory Eisenlohr-Moul, R McKell Carter, Gabriel S Dichter, Maya G Mosner, R Edward McLaurin, Jessica L Kinard, Shabnam Hakimi, Jacob Parelman, Jasmine S Shah, Joshua Bizzell, Rachel K Greene, Paul M Cernasov, Erin Walsh, Merideth A Addicott, Tory Eisenlohr-Moul, R McKell Carter, Gabriel S Dichter

Abstract

Few studies have explored neural mechanisms of reward learning in ASD despite evidence of behavioral impairments of predictive abilities in ASD. To investigate the neural correlates of reward prediction errors in ASD, 16 adults with ASD and 14 typically developing controls performed a prediction error task during fMRI scanning. Results revealed greater activation in the ASD group in the left paracingulate gyrus during signed prediction errors and the left insula and right frontal pole during thresholded unsigned prediction errors. Findings support atypical neural processing of reward prediction errors in ASD in frontostriatal regions critical for prediction coding and reward learning. Results provide a neural basis for impairments in reward learning that may contribute to traits common in ASD (e.g., intolerance of unpredictability).

Figures

Figure 1
Figure 1
Greater activation in the ASD group relative to the TDC group in the left paracingulate gyrus during the signed prediction error (SPE) contrast. Color bar represents the range of z-values.
Figure 2
Figure 2
Greater activation in the ASD group relative to the TDC group in the left insula (top row) and in the right frontal pole (bottom row) during the threshold unsigned prediction error (UPE) contrast. Color bar represents the range of z-values.

References

    1. Chevallier C., Kohls G., Troiani V., Brodkin E. S., Schultz R. T. The social motivation theory of autism. Trends in Cognitive Sciences. 2012;16(4):231–238. doi: 10.1016/j.tics.2012.02.007.
    1. Clements C. C., Zoltowski A. R., Yankowitz L. D., Yerys B. E., Schultz R. T., Herrington J. D. Evaluation of the social motivation hypothesis of autism. JAMA Psychiatry. 2018;75(8):797–808. doi: 10.1001/jamapsychiatry.2018.1100.
    1. Ruta L., Famà F. I., Bernava G. M., et al. Reduced preference for social rewards in a novel tablet based task in young children with autism spectrum disorders. Scientific Reports. 2017;7(1, article no. 3329) doi: 10.1038/s41598-017-03615-x.
    1. Stavropoulos K. K., Carver L. J. Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism. Molecular Autism. 2018;9(4) doi: 10.1186/s13229-018-0189-5.
    1. Berridge K. C. Evolving concepts of emotion and motivation. Frontiers in Psychology. 2018;9, article no. 1647 doi: 10.3389/fpsyg.2018.01647.
    1. Olney J. J., Warlow S. M., Naffziger E. E., Berridge K. C. Current perspectives on incentive salience and applications to clinical disorders. Current Opinion in Behavioral Sciences. 2018;22:59–69. doi: 10.1016/j.cobeha.2018.01.007.
    1. Kringelbach M. L., Berridge K. C. The affective core of emotion: linking pleasure, subjective well-being, and optimal metastability in the brain. Emotion Review. 2017;9(3):191–199. doi: 10.1177/1754073916684558.
    1. Sinha P., Kjelgaard M. M., Gandhi T. K., et al. Autism as a disorder of prediction. Proceedings of the National Acadamy of Sciences of the United States of America. 2014;111(42):15220–15225. doi: 10.1073/pnas.1416797111.
    1. Lin A., Rangel A., Adolphs R. Impaired learning of social compared to monetary rewards in autism. Frontiers in Neuroscience. 2012;6(143) doi: 10.3389/fnins.2012.00143.
    1. Mussey J. L., Travers B. G., Klinger L. G., Klinger M. R. Decision-making skills in ASD: performance on the iowa gambling task. Autism Research. 2015;8(1):105–114. doi: 10.1002/aur.1429.
    1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th. Vol. 17. Arlington, VA, USA: American Psychiatric Publishing; 2013.
    1. Munson J., Faja S., Meltzoff A., Abbott R., Dawson G. Neurocognitive predictors of social and communicative developmental trajectories in preschoolers with autism spectrum disorders. Journal of the International Neuropsychological Society. 2008;14(6):956–966. doi: 10.1017/S1355617708081393.
    1. Solomon M., Smith A. C., Frank M. J., Ly S., Carter C. S. Probabilistic reinforcement learning in adults with autism spectrum disorders. Autism Research. 2011;4(2):109–120. doi: 10.1002/aur.177.
    1. Choi U., Kim S., Sim H. J., et al. Abnormal brain activity in social reward learning in children with autism spectrum disorder: An fMRI study. Yonsei Medical Journal. 2015;56(3):705–711. doi: 10.3349/ymj.2015.56.3.705.
    1. Scott-Van Zeeland A. A., Dapretto M., Ghahremani D. G., Poldrack R. A., Bookheimer S. Y. Reward processing in autism. Autism Research. 2010;3(2):53–67. doi: 10.1002/aur.122.
    1. Schipul S. E., Just M. A. Diminished neural adaptation during implicit learning in autism. NeuroImage. 2016;125:332–341. doi: 10.1016/j.neuroimage.2015.10.039.
    1. Schipul S. E., Williams D. L., Keller T. A., Minshew N. J., Just M. A. Distinctive neural processes during learning in autism. Cerebral Cortex. 2012;22(4):937–950. doi: 10.1093/cercor/bhr162.
    1. O’Neill M., Schultz W. Predictive coding of the statistical parameters of uncertain rewards by orbitofrontal neurons. Behavioural Brain Research. 2018;355:90–94. doi: 10.1016/j.bbr.2018.04.041.
    1. Lawson R. P., Rees G., Friston K. J. An aberrant precision account of autism. Frontiers in Human Neuroscience. 2014;8, article no. 302 doi: 10.3389/fnhum.2014.00302.
    1. van de Cruys S., Evers K., van der Hallen R., et al. Precise minds in uncertain worlds: predictive coding in autism. Psychological Review. 2014;121(4):649–675. doi: 10.1037/a0037665.
    1. Gomot M., Wicker B. A challenging, unpredictable world for people with autism spectrum disorder. International Journal of Psychophysiology. 2012;83(2):240–247. doi: 10.1016/j.ijpsycho.2011.09.017.
    1. Robic S., Sonié S., Fonlupt P., et al. Decision-making in a changing world: a study in autism spectrum disorders. Journal of Autism and Developmental Disorders. 2015;45(6):1603–1613. doi: 10.1007/s10803-014-2311-7.
    1. Watt N., Wetherby A. M., Barber A., Morgan L. Repetitive and stereotyped behaviors in children with autism spectrum disorders in the second year of life. Journal of Autism and Developmental Disorders. 2008;38(8):1518–1533. doi: 10.1007/s10803-007-0532-8.
    1. Balsters J. H., Apps M. A., Bolis D., Lehner R., Gallagher L., Wenderoth N. Disrupted prediction errors index social deficits in autism spectrum disorder. Brain. 2016;140(1):235–246. doi: 10.1093/brain/aww287.
    1. Ramnani N., Elliott R., Athwal B. S., Passingham R. E. Prediction error for free monetary reward in the human prefrontal cortex. Neuroimage. 2004;23(3):777–786.
    1. Addicott M. A., Oliver J. A., Joseph McClernon F. Nicotine increases anterior insula activation to expected and unexpected outcomes among nonsmokers. Psychopharmacology. 2017;234(7):1145–1154. doi: 10.1007/s00213-017-4550-8.
    1. Kohrs C., Angenstein N., Scheich H., Brechmann A. Human striatum is differentially activated by delayed, omitted, and immediate registering feedback. Frontiers in Human Neuroscience. 2012;6, article no. 243 doi: 10.3389/fnhum.2012.00243.
    1. Takemura H., Samejima K., Vogels R., Sakagami M., Okuda J., Lauwereyns J. Stimulus-dependent adjustment of reward prediction error in the midbrain. PLoS ONE. 2011;6(12):p. e28337. doi: 10.1371/journal.pone.0028337.
    1. Tom S. M., Fox C. R., Trepel C., Poldrack R. A. The neural basis of loss aversion in decision-making under risk. Science. 2007;315(5811):515–518. doi: 10.1126/science.1134239.
    1. Langdon A. J., Sharpe M. J., Schoenbaum G., Niv Y. Model-based predictions for dopamine. Current Opinion in Neurobiology. 2018;49:1–7. doi: 10.1016/j.conb.2017.10.006.
    1. Takahashi Y. K., Stalnaker T. A., Roesch M. R., Schoenbaum G. Effects of inference on dopaminergic prediction errors depend on orbitofrontal processing. Behavioral Neuroscience. 2017;131(2):127–134. doi: 10.1037/bne0000192.
    1. Garrison J., Erdeniz B., Done J. Prediction error in reinforcement learning: A meta-analysis of neuroimaging studies. Neuroscience & Biobehavioral Reviews. 2013;37(7):1297–1310. doi: 10.1016/j.neubiorev.2013.03.023.
    1. Hus V., Gotham K., Lord C. Standardizing ADOS domain scores: separating severity of social affect and restricted and repetitive behaviors. Journal of Autism and Developmental Disorders. 2014;44(10):2400–2412. doi: 10.1007/s10803-012-1719-1.
    1. Constantino J. N., Davis S. A., Todd R. D., et al. Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the Autism Diagnostic Interview-Revised. Journal of Autism and Developmental Disorders. 2003;33(4):427–433. doi: 10.1023/a:1025014929212.
    1. Uttl B. North american adult reading test: age norms, reliability, and validity. Journal of Clinical and Experimental Neuropsychology. 2010;24(8):1123–1137. doi: 10.1076/jcen.24.8.1123.8375.
    1. Axelrod B. N. Validity of the wechsler abbreviated scale of intelligence and other very short forms of estimating intellectual functioning. Assessment. 2016;9(1):17–23. doi: 10.1177/1073191102009001003.
    1. Caplin A., Dean M., Glimcher P. W., Rutledge R. B. Measuring beliefs and rewards: a neuroeconomic approach. The Quarterly Journal of Economics. 2010;125(3):923–960. doi: 10.1162/qjec.2010.125.3.923.
    1. Smith S. M., Jenkinson M., Woolrich M. W., et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23, supplement 1:S208–S219. doi: 10.1016/j.neuroimage.2004.07.051.
    1. Smith S. M. Fast robust automated brain extraction. Human Brain Mapping. 2002;17(3):143–155. doi: 10.1002/hbm.10062.
    1. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825–841. doi: 10.1016/S1053-8119(02)91132-8.
    1. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Medical Image Analysis. 2001;5(2):143–156. doi: 10.1016/S1361-8415(01)00036-6.
    1. Dichter G. S., Felder J. N., Green S. R., Rittenberg A. M., Sasson N. J., Bodfish J. W. Reward circuitry function in autism spectrum disorders. Social Cognitive and Affective Neuroscience. 2012;7(2):160–172. doi: 10.1093/scan/nsq095.
    1. Schmitz N., Rubia K., van Amelsvoort T., Daly E., Smith A., Murphy D. G. Neural correlates of reward in autism. The British Journal of Psychiatry. 2008;192(1):19–24. doi: 10.1192/bjp.bp.107.036921.
    1. Wang B. D. Simultaneous inference for fMRI data. 2000.
    1. Schultz W. Dopamine neurons and their role in reward mechanisms. Current Opinion in Neurobiology. 1997;7(2):191–197. doi: 10.1016/S0959-4388(97)80007-4.
    1. Woolrich M. W., Ripley B. D., Brady M., Smith S. M. Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage. 2001;14(6):1370–1386. doi: 10.1006/nimg.2001.0931.
    1. Gotham K., Pickles A., Lord C. Standardizing ADOS scores for a measure of severity in autism spectrum disorders. Journal of Autism and Developmental Disorders. 2009;39(5):693–705. doi: 10.1007/s10803-008-0674-3.
    1. D’Astolfo L., Rief W. Learning about expectation violation from prediction error paradigms – a meta-analysis on brain processes following a prediction error. Frontiers in Psychology. 2017;8, article no. 1253 doi: 10.3389/fpsyg.2017.01253.
    1. Singer T., Critchley H. D., Preuschoff K. A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences. 2009;13(8):334–340. doi: 10.1016/j.tics.2009.05.001.
    1. Waltz J. A., Schweitzer J. B., Gold J. M., et al. Patients with schizophrenia have a reduced neural response to both unpredictable and predictable primary reinforcers. Neuropsychopharmacology. 2009;34(6):1567–1577. doi: 10.1038/npp.2008.214.
    1. Lamichhane B., Adhikari B. M., Dhamala M. Salience network activity in perceptual decisions. Brain Connectivity. 2016;6(7):558–571. doi: 10.1089/brain.2015.0392.
    1. Behrens T. E., Woolrich M. W., Walton M. E., Rushworth M. F. Learning the value of information in an uncertain world. Nature Neuroscience. 2007;10(9):1214–1221. doi: 10.1038/nn1954.
    1. De Martino B., Kumaran D., Holt B., Dolan R. J. The neurobiology of reference-dependent value computation. The Journal of Neuroscience. 2009;29(12):3833–3842. doi: 10.1523/JNEUROSCI.4832-08.2009.
    1. Preuschoff K., Quartz S. R., Bossaerts P. Human insula activation reflects risk prediction errors as well as risk. The Journal of Neuroscience. 2008;28(11):2745–2752. doi: 10.1523/JNEUROSCI.4286-07.2008.
    1. Koban L., Pourtois G. Brain systems underlying the affective and social monitoring of actions: An integrative review. Neuroscience & Biobehavioral Reviews. 2014;46:71–84. doi: 10.1016/j.neubiorev.2014.02.014.
    1. Craig A. D. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience. 2002;3(8):655–666. doi: 10.1038/nrn894.
    1. Reynolds S. M., Zahm D. S. Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. The Journal of Neuroscience. 2005;25(50):11757–11767. doi: 10.1523/JNEUROSCI.3432-05.2005.
    1. Mundy P. A review of joint attention and social-cognitive brain systems in typical development and autism spectrum disorder. European Journal of Neuroscience. 2018;47(6):497–514. doi: 10.1111/ejn.13720.
    1. Di Martino A., Ross K., Uddin L. Q., Sklar A. B., Castellanos F. X., Milham M. P. Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biological Psychiatry. 2009;65(1):63–74. doi: 10.1016/j.biopsych.2008.09.022.
    1. Dichter G. S., Belger A. Social stimuli interfere with cognitive control in autism. NeuroImage. 2007;35(3):1219–1230. doi: 10.1016/j.neuroimage.2006.12.038.
    1. Hubl D., Bölte S., Feineis-Matthews S., et al. Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology. 2003;61(9):1232–1237. doi: 10.1212/01.WNL.0000091862.22033.1A.
    1. Silani G., Bird G., Brindley R., Singer T., Frith C., Frith U. Levels of emotional awareness and autism: An fMRI study. Social Neuroscience. 2008;3(2):97–112. doi: 10.1080/17470910701577020.
    1. Dichter G. S., Felder J. N., Bodfish J. W. Autism is characterized by dorsal anterior cingulate hyperactivation during social target detection. Social Cognitive and Affective Neuroscience. 2009;4(3):215–226. doi: 10.1093/scan/nsp017.
    1. Dichter G. S., Richey J. A., Rittenberg A. M., Sabatino A., Bodfish J. W. Reward circuitry function in autism during face anticipation and outcomes. Journal of Autism and Developmental Disorders. 2012;42(2):147–160. doi: 10.1007/s10803-011-1221-1.
    1. Odriozola P., Uddin L. Q., Lynch C. J., Kochalka J., Chen T., Menon V. Insula response and connectivity during social and non-social attention in children with autism. Social Cognitive and Affective Neuroscience. 2016;11(3):433–444. doi: 10.1093/scan/nsv126.
    1. Yamada T., Itahashi T., Nakamura M., et al. Altered functional organization within the insular cortex in adult males with high-functioning autism spectrum disorder: evidence from connectivity-based parcellation. Molecular Autism. 2016;7(41) doi: 10.1186/s13229-016-0106-8.
    1. Tsujimoto S., Genovesio A., Wise S. P. Evaluating self-generated decisions in frontal pole cortex of monkeys. Nature Neuroscience. 2010;13(1):120–126.
    1. Tsujimoto S., Genovesio A., Wise S. P. Frontal pole cortex: encoding ends at the end of the endbrain. Trends in Cognitive Sciences. 2011;15(4):169–176. doi: 10.1016/j.tics.2011.02.001.
    1. Okuda J., Fujii T., Ohtake H., et al. Thinking of the future and past: the roles of the frontal pole and the medial temporal lobes. NeuroImage. 2003;19(4):1369–1380. doi: 10.1016/s1053-8119(03)00179-4.
    1. Livingston L. A., Happé F. Conceptualising compensation in neurodevelopmental disorders: Reflections from autism spectrum disorder. Neuroscience & Biobehavioral Reviews. 2017;80:729–742. doi: 10.1016/j.neubiorev.2017.06.005.
    1. Sherer M. R., Schreibman L. Individual behavioral profiles and predictors of treatment effectiveness for children with autism. Journal of Consulting and Clinical Psychology. 2005;73(3):525–538. doi: 10.1037/0022-006X.73.3.525.
    1. Spreckley M., Boyd R. Efficacy of applied behavioral intervention in preschool children with autism for improving cognitive, language, and adaptive behavior: a systematic review and meta-analysis. Journal of Pediatrics. 2009;154(3):338–344. doi: 10.1016/j.jpeds.2008.09.012.
    1. Vismara L. A., Rogers S. J. Behavioral treatments in autism spectrum disorder: What do we know? Annual Review of Clinical Psychology. 2010;6:447–468. doi: 10.1146/annurev.clinpsy.121208.131151.

Source: PubMed

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