Skip to main content

Advertisement

SpringerLink
Log in

Reward Circuitry Function in Autism During Face Anticipation and Outcomes

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate reward circuitry responses in autism during reward anticipation and outcomes for monetary and social rewards. During monetary anticipation, participants with autism spectrum disorders (ASDs) showed hypoactivation in right nucleus accumbens and hyperactivation in right hippocampus, whereas during monetary outcomes, participants with ASDs showed hyperactivation in left midfrontal and anterior cingulate gyrus. Groups did not differ in nucleus accumbens responses to faces. The ASD group demonstrated hyperactivation in bilateral amygdala during face anticipation that predicted social symptom severity and in bilateral insular cortex during face outcomes. These results add to the growing body of evidence that autism is characterized by altered functioning of reward circuitry. Additionally, atypical amygdala activation during the processing of social rewards may contribute to the development or expression of autistic features.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aberman, J. E., Ward, S. J., & Salamone, J. D. (1998). Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive-ratio performance. Pharmacology, Biochemistry and Behavior, 61(4), 341–348.

    Google Scholar 

  • Abler, B., Greenhouse, I., Ongur, D., Walter, H., & Heckers, S. (2007). Abnormal reward system activation in Mania. Neuropsychopharmacology.

  • Adcock, R. A., Thangavel, A., Whitfield-Gabrieli, S., Knutson, B., & Gabrieli, J. D. (2006). Reward-motivated learning: Mesolimbic activation precedes memory formation. Neuron, 50(3), 507–517.

    PubMed  Google Scholar 

  • Adolphs, R. (2010). What does the amygdala contribute to social cognition? Annals of the New York Academy of Sciences, 1191(1), 42–61.

    PubMed  Google Scholar 

  • Aharon, I., Etcoff, N., Ariely, D., Chabris, C. F., O’Connor, E., & Breiter, H. C. (2001). Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron, 32(3), 537–551.

    PubMed  Google Scholar 

  • Ashwin, C., Baron-Cohen, S., Wheelwright, S., O’Riordan, M., & Bullmore, E. T. (2007). Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome. Neuropsychologia, 45(1), 2–14.

    PubMed  Google Scholar 

  • Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001). The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31(1), 5–17.

    PubMed  Google Scholar 

  • Bechara, A., Damasio, H., & Damasio, A. R. (2000). Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex, 10(3), 295–307.

    PubMed  Google Scholar 

  • Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003). General multilevel linear modeling for group analysis in FMRI. Neuroimage, 20(2), 1052–1063.

    PubMed  Google Scholar 

  • Berridge, K. C. (1996). Food reward: brain substrates of wanting and liking. Neuroscience and Biobehavioral Reviews, 20(1), 1–25.

    PubMed  Google Scholar 

  • Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Research Reviews, 28(3), 309–369.

    PubMed  Google Scholar 

  • Bjork, J. M., & Hommer, D. W. (2007). Anticipating instrumentally obtained and passively-received rewards: a factorial fMRI investigation. Behavioural Brain Research, 177(1), 165–170.

    PubMed  Google Scholar 

  • Bodfish, J. W., Symons, F. W., & Lewis, M. H. (1999). The repetitive behavior scale-revised, Western Carolina Center Research Reports.

  • Bookheimer, S. Y., Wang, A. T., Scott, A., Sigman, M., & Dapretto, M. (2008). Frontal contributions to face processing differences in autism: Evidence from fMRI of inverted face processing. Journal of the International Neuropsychological Society, 14(6), 922–932.

    PubMed  Google Scholar 

  • Boyd, B. A., Conroy, M. A., Mancil, G. R., Nakao, T., & Alter, P. J. (2007). Effects of circumscribed interests on the social behaviors of children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(8), 1550–1561.

    PubMed  Google Scholar 

  • Brooks, R., & Meltzoff, A. N. (2002). The importance of eyes: how infants interpret adult looking behavior. Developmental Psychology, 38(6), 958–966.

    PubMed  Google Scholar 

  • Brown, J. W., & Braver, T. S. (2005). Learned predictions of error likelihood in the anterior cingulate cortex. Science, 307(5712), 1118–1121.

    PubMed  Google Scholar 

  • Canli, T., Zhao, Z., Desmond, J. E., Kang, E., Gross, J., & Gabrieli, J. D. (2001). An fMRI study of personality influences on brain reactivity to emotional stimuli. Behavioral Neuroscience, 115(1), 33–42.

    PubMed  Google Scholar 

  • Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences USA, 100(9), 5497–5502.

    Google Scholar 

  • Chakrabarti, B., Kent, L., Suckling, J., Bullmore, E., & Baron-Cohen, S. (2006). Variations in the human cannabinoid receptor (CNR1) gene modulate striatal responses to happy faces. European Journal of Neuroscience, 23(7), 1944–1948.

    PubMed  Google Scholar 

  • Cloutier, J., Heatherton, T. F., Whalen, P. J., & Kelley, W. M. (2008). Are attractive people rewarding? Sex differences in the neural substrates of facial attractiveness. Journal of Cognitive Neuroscience, 20(6), 941–951.

    PubMed  Google Scholar 

  • Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., et al. (2003). 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, 33(4), 427–433.

    PubMed  Google Scholar 

  • Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C., Van Amelsvoort, T., Robertson, D. M., et al. (2000). The functional neuroanatomy of social behaviour: Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain, 123(Pt 11), 2203–2212.

    PubMed  Google Scholar 

  • Dalton, K. M., Kalin, N. H., Grist, T. M., & Davidson, R. J. (2005a). Neural-cardiac coupling in threat-evoked anxiety. Journal of Cognitive Neuroscience, 17(6), 969–980.

    PubMed  Google Scholar 

  • Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., et al. (2005b). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526.

    PubMed  Google Scholar 

  • Dapretto, M., Davies, M. S., Pfeifer, J. H., Scott, A. A., Sigman, M., Bookheimer, S. Y., et al. (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9(1), 28–30.

    PubMed  Google Scholar 

  • Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998). Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders, 28(6), 479–485.

    PubMed  Google Scholar 

  • Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., & Estes, A. (2004). Defining the early social attention impairments in autism: Social orienting, joint attention, and responses to emotions. Developmental Psychology, 40, 271–283.

    PubMed  Google Scholar 

  • Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27(3), 403–424.

    PubMed  Google Scholar 

  • de Lafuente, V., & Romo, R. (2006). Neural correlate of subjective sensory experience gradually builds up across cortical areas. Proceedings of the National Academy of Sciences USA, 103(39), 14266–14271.

    Google Scholar 

  • de Vignemont, F., & Singer, T. (2006). The empathic brain: How, when and why? Trends Cognitive Science, 10(10), 435–441.

    Google Scholar 

  • Deco, G., & Rolls, E. T. (2006). Decision-making and Weber’s law: A neurophysiological model. European Journal of Neuroscience, 24(3), 901–916.

    PubMed  Google Scholar 

  • Dichter, G. S., Felder, J., Green, S. R., Rittenberg, A. M., Sasson, N., & Bodfish, J. (2011). Reward circuitry function in autism spectrum disorders. Social Cognitive and Affective Neuroscience (in press).

  • Dichter, G. S., & Tomarken, A. J. (2008). The chronometry of affective startle modulation in unipolar depression. Journal of Abnormal Psychology, 117(1), 1–15.

    PubMed  Google Scholar 

  • Dillon, D. G., Holmes, A. J., Jahn, A. L., Bogdan, R., Wald, L. L., & Pizzagalli, D. A. (2008). Dissociation of neural regions associated with anticipatory versus consummatory phases of incentive processing. Psychophysiology, 45(1), 36–49.

    PubMed  Google Scholar 

  • Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews of Neuroscience, 1(1), 41–50.

    Google Scholar 

  • Emery, N. J. (2000). The eyes have it: The neuroethology, function and evolution of social gaze. Neuroscience and Biobehavioral Reviews, 24(6), 581–604.

    PubMed  Google Scholar 

  • Farroni, T., Csibra, G., Simion, F., & Johnson, M. H. (2002). Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences USA, 99(14), 9602–9605.

    Google Scholar 

  • Fischl, B., Sereno, M. I., & Dale, A. M. (1999a). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9(2), 195–207.

    PubMed  Google Scholar 

  • Fischl, B., Sereno, M. I., Tootell, R. B., & Dale, A. M. (1999b). High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping, 8(4), 272–284.

    PubMed  Google Scholar 

  • Fletcher, P. C., & Henson, R. N. (2001). Frontal lobes and human memory: Insights from functional neuroimaging. Brain, 124(Pt 5), 849–881.

    PubMed  Google Scholar 

  • Forbes, E. E., Hariri, A. R., Martin, S. L., Silk, J. S., Moyles, D. L., Fisher, P. M., et al. (2009). Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. American Journal of Psychiatry, 166(1), 64–73.

    PubMed  Google Scholar 

  • Friedman, D. P., Aggleton, J. P., & Saunders, R. C. (2002). Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: Combined anterograde and retrograde tracing study in the Macaque brain. Journal of Comparative Neurology, 450(4), 345–365.

    PubMed  Google Scholar 

  • Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119(Pt 2), 593–609.

    PubMed  Google Scholar 

  • Gottfried, J. A., O’Doherty, J., & Dolan, R. J. (2003). Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science, 301(5636), 1104–1107.

    PubMed  Google Scholar 

  • Grelotti, D. J., Klin, A. J., Gauthier, I., Skudlarski, P., Cohen, D. J., Gore, J. C., et al. (2005). fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia, 43(3), 373–385.

    PubMed  Google Scholar 

  • Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35(1), 4–26.

    PubMed  Google Scholar 

  • Hadjikhani, N., Joseph, R. M., Snyder, J., & Tager-Flusberg, H. (2007). Abnormal activation of the social brain during face perception in autism. Human Brain Mapping, 28(5), 441–449.

    PubMed  Google Scholar 

  • Hayden, B. Y., Parikh, P. C., Deaner, R. O., & Platt, M. L. (2007). Economic principles motivating social attention in humans. Proceedings Biological Sciences, 274(1619), 1751–1756.

    Google Scholar 

  • Hempel, R. J., Tulen, J. H., van Beveren, N. J., van Steenis, H. G., Mulder, P. G., & Hengeveld, M. W. (2005). Physiological responsivity to emotional pictures in schizophrenia. Journal of Psychiatric Research, 39(5), 509–518.

    PubMed  Google Scholar 

  • Howes, O. D., & Kapur, S. (2009). The dopamine hypothesis of schizophrenia: Version III-the final common pathway. Schizophrenia Bulletin, 35(3), 549–562.

    PubMed  Google Scholar 

  • Hsu, M., Bhatt, M., Adolphs, R., Tranel, D., & Camerer, C. F. (2005). Neural systems responding to degrees of uncertainty in human decision-making. Science, 310(5754), 1680–1683.

    PubMed  Google Scholar 

  • Ikemoto, S., & Panksepp, J. (1999). The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking. Brain Research. Brain Research Reviews, 31(1), 6–41.

    PubMed  Google Scholar 

  • Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage, 17(2), 825–841.

    PubMed  Google Scholar 

  • Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143–156.

    PubMed  Google Scholar 

  • Johnson, S. A., Filliter, J. H., & Murphy, R. R. (2009). Discrepancies between self- and parent-perceptions of autistic traits and empathy in high functioning children and adolescents on the autism spectrum. J Autism Dev Disord.

  • Juckel, G., Schlagenhauf, F., Koslowski, M., Filonov, D., Wustenberg, T., Villringer, A., et al. (2006a). Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berlin), 187(2), 222–228.

    Google Scholar 

  • Juckel, G., Schlagenhauf, F., Koslowski, M., Wustenberg, T., Villringer, A., Knutson, B., et al. (2006b). Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage, 29(2), 409–416.

    PubMed  Google Scholar 

  • Juranek, J., Filipek, P. A., Berenji, G. R., Modahl, C., Osann, K., & Spence, M. A. (2006). Association between amygdala volume and anxiety level: Magnetic resonance imaging (MRI) study in autistic children. Journal of Child Neurology, 21(12), 1051–1058.

    PubMed  Google Scholar 

  • Kable, J. W., & Glimcher, P. W. (2007). The neural correlates of subjective value during intertemporal choice. Nature Neuroscience, 10(12), 1625–1633.

    PubMed  Google Scholar 

  • Kim, H., Shimojo, S., & O’Doherty, J. P. (2006). Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain. PLoS Biology, 4(8), e233.

    Google Scholar 

  • Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry, 166(4), 467–475.

    PubMed  Google Scholar 

  • Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809–816.

    PubMed  Google Scholar 

  • Klin, A., Lin, D. J., Gorrindo, P., Ramsay, G., & Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459(7244), 257–261.

    PubMed  Google Scholar 

  • Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21(16), RC159.

    Google Scholar 

  • Knutson, B., & Cooper, J. C. (2005). Functional magnetic resonance imaging of reward prediction. Current Opinion in Neurology, 18(4), 411–417.

    PubMed  Google Scholar 

  • Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001b). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport, 12(17), 3683–3687.

    PubMed  Google Scholar 

  • Knutson, B., & Greer, S. M. (2008). Review. Anticipatory affect: neural correlates and consequences for choice. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences.

  • Knutson, B., Rick, S., Wimmer, G. E., Prelec, D., & Loewenstein, G. (2007). Neural predictors of purchases. Neuron, 53(1), 147–156.

    PubMed  Google Scholar 

  • Knutson, B., Westdorp, A., Kaiser, E., & Hommer, D. (2000). FMRI visualization of brain activity during a monetary incentive delay task. Neuroimage, 12(1), 20–27.

    PubMed  Google Scholar 

  • Kuhl, P. K., Coffey-Corina, S., Padden, D., & Dawson, G. (2005). Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. Developmental Science, 8, F1–F12.

    PubMed  Google Scholar 

  • Labar, K. S. (2007). Beyond fear emotional memory mechanisms in the human brain. Current Directions in Psychological Science, 16(4), 173–177.

    PubMed  Google Scholar 

  • Lam, K. S., & Aman, M. G. (2007). The repetitive behavior scale-revised: Independent validation in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(5), 855–866.

    PubMed  Google Scholar 

  • Le Van Quyen, M., Bragin, A., Staba, R., Crepon, B., Wilson, C. L., & Engel, J., Jr. (2008). Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. Journal of Neuroscience, 28(24), 6104–6110.

    PubMed  Google Scholar 

  • Liang, X., Zebrowitz, L. A., & Zhang, Y. (2010). Neural activation in the “reward circuit” shows a nonlinear response to facial attractiveness. Social Neuroscience, 5(3), 320–334.

    PubMed  Google Scholar 

  • Lombardo, M. V., Chakrabarti, B., & Baron-Cohen, S. (2009). The amygdala in autism: Not adapting to faces? American Journal of Psychiatry, 166(4), 395–397.

    PubMed  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Jr., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.

    PubMed  Google Scholar 

  • MacDonald, A. W., 3rd, Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835–1838.

    PubMed  Google Scholar 

  • Magno, E., Foxe, J. J., Molholm, S., Robertson, I. H., & Garavan, H. (2006). The anterior cingulate and error avoidance. Journal of Neuroscience, 26(18), 4769–4773.

    PubMed  Google Scholar 

  • McCabe, C., Mishor, Z., Cowen, P. J., & Harmer, C. J. (2010). Diminished neural processing of aversive and rewarding stimuli during selective serotonin reuptake inhibitor treatment. Biological Psychiatry, 67(5), 439–445.

    PubMed  Google Scholar 

  • Monk, C. S., Weng, S. J., Wiggins, J. L., Kurapati, N., Louro, H. M., Carrasco, M., et al. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry Neuroscience, 35(2), 105–114.

    PubMed  Google Scholar 

  • Munson, J., Dawson, G., Abbott, R., Faja, S., Webb, S. J., Friedman, S. D., et al. (2006). Amygdalar volume and behavioral development in autism. Archives of General Psychiatry, 63(6), 686–693.

    PubMed  Google Scholar 

  • Nishitani, N., Avikainen, S., & Hari, R. (2004). Abnormal imitation-related cortical activation sequences in Asperger’s syndrome. Annals of Neurology, 55(4), 558–562.

    PubMed  Google Scholar 

  • O’Doherty, J., Winston, J., Critchley, H., Perrett, D., Burt, D. M., & Dolan, R. J. (2003). Beauty in a smile: The role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia, 41(2), 147–155.

    PubMed  Google Scholar 

  • Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Brain Research. Cognitive Brain Research, 24(2), 190–198.

    PubMed  Google Scholar 

  • Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54(5), 504–514.

    PubMed  Google Scholar 

  • Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the fusiform ‘face area’ in autism: Evidence from functional MRI. Brain, 124(Pt 10), 2059–2073.

    PubMed  Google Scholar 

  • Pinkham, A. E., Hopfinger, J. B., Pelphrey, K. A., Piven, J., & Penn, D. L. (2008). Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders. Schizophrenia Research, 99(1–3), 164–175.

    PubMed  Google Scholar 

  • Rademacher, L., Krach, S., Kohls, G., Irmak, A., Grunder, G., & Spreckelmeyer, K. N. (2010). Dissociation of neural networks for anticipation and consumption of monetary and social rewards. Neuroimage, 49(4), 3276–3285.

    PubMed  Google Scholar 

  • Rehme, A. K., Frommann, I., Peters, S., Block, V., Bludau, J., Quednow, B. B., Maier, W., Schutz, C., & Wagner, M. (2009). Startle cue-reactivity differentiates between light and heavy smokers. Addiction.

  • Ridderinkhof, K. R., Ullsperger, M., Crone, E. A., & Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306(5695), 443–447.

    PubMed  Google Scholar 

  • Roid, G. H., & Miller, L. J. (1997). Leiter international performance scale-revised. Woodale, IL: Stoelting Co.

    Google Scholar 

  • Rolls, E. T. (1996). The orbitofrontal cortex. In Philosophical Transactions of the royal society of London—series B: Biological sciences (Vol. 351, pp. 1433-1443).

  • Rolls, E. T., & Grabenhorst, F. (2008). The orbitofrontal cortex and beyond: From affect to decision-making. Progress in Neurobiology, 86(3), 216–244.

    PubMed  Google Scholar 

  • Sasson, N., Tsuchiya, N., Hurley, R., Couture, S. M., Penn, D. L., Adolphs, R., et al. (2007). Orienting to social stimuli differentiates social cognitive impairment in autism and schizophrenia. Neuropsychologia, 45(11), 2580–2588.

    PubMed  Google Scholar 

  • Sasson, N., Turner-Brown, L., Holtzclaw, T., Lam, K. S., & Bodfish, J. (2008). Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Research, 1, 31–42.

    PubMed  Google Scholar 

  • Schmitz, N., Rubia, K., van Amelsvoort, T., Daly, E., Smith, A., & Murphy, D. G. (2008). Neural correlates of reward in autism. British Journal of Psychiatry, 192, 19–24.

    PubMed  Google Scholar 

  • Schultz, W. (1998). Predictive reward signal of dopamine neurons. Journal of Neurophysiology, 80(1), 1–27.

    PubMed  Google Scholar 

  • Schultz, W. (2000). Multiple reward signals in the brain. Nature Reviews of Neuroscience, 1(3), 199–207.

    Google Scholar 

  • Schultz, R. T. (2005). Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23(2–3), 125–141.

    PubMed  Google Scholar 

  • Schultz, R. T., Gauthier, I., Klin, A., Fulbright, R. K., Anderson, A. W., Volkmar, F., et al. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry, 57(4), 331–340.

    PubMed  Google Scholar 

  • Scott-Van Zeeland, A. A., Dapretto, M., Ghahremani, D. G., Poldrack, R. A., & Bookheimer, S. Y. (2010). Reward processing in autism. Autism Research, 3(2), 53–67.

    PubMed  Google Scholar 

  • Shabel, S. J., & Janak, P. H. (2009). Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal. Proceedings of the National Academy of Sciences USA, 106(35), 15031–15036.

    Google Scholar 

  • Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303(5661), 1157–1162.

    PubMed  Google Scholar 

  • Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155.

    PubMed  Google Scholar 

  • Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl 1), S208–S219.

    PubMed  Google Scholar 

  • Smoski, M. J., Felder, J., Bizzell, J., Green, S. R., Ernst, M., Lynch, T. R., et al. (2009). fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. Journal of Affective Disorders, 118(1–3), 69–78.

    PubMed  Google Scholar 

  • Stice, E., Yokum, S., Bohon, C., Marti, N., & Smolen, A. (2010). Reward circuitry responsivity to food predicts future increases in body mass: moderating effects of DRD2 and DRD4. Neuroimage, 50(4), 1618–1625.

    PubMed  Google Scholar 

  • Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., et al. (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research, 168(3), 242–249.

    PubMed  Google Scholar 

  • Walton, M. E., Bannerman, D. M., Alterescu, K., & Rushworth, M. F. (2003). Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. Journal of Neuroscience, 23(16), 6475–6479.

    PubMed  Google Scholar 

  • Walton, M. E., Bannerman, D. M., & Rushworth, M. F. (2002). The role of rat medial frontal cortex in effort-based decision making. Journal of Neuroscience, 22(24), 10996–11003.

    PubMed  Google Scholar 

  • Weng, S. J., Carrasco, M., Swartz, J. R., Wiggins, J. L., Kurapati, N., Liberzon, I., Risi, S., Lord, C., & Monk, C. S. (2010). Neural activation to emotional faces in adolescents with autism spectrum disorders. J Child Psychol Psychiatry.

  • Weschler, D. (1999). Weschler abbreviated scale of intelligence (WASI). San Antonio, TX: Harcourt Assessment.

    Google Scholar 

  • Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron, 40(3), 655–664.

    PubMed  Google Scholar 

  • Williams, J. H. G. (2008). Self-other relations in social development and for mirror neurons and other brain bases. Autism Research, 1, 73–90.

    PubMed  Google Scholar 

  • Willner, P. (1983). Dopamine and depression: a review of recent evidence. III. The effects of antidepressant treatments. Brain Research, 287(3), 237–246.

    PubMed  Google Scholar 

  • Winston, J. S., O’Doherty, J., Kilner, J. M., Perrett, D. I., & Dolan, R. J. (2007). Brain systems for assessing facial attractiveness. Neuropsychologia, 45(1), 195–206.

    PubMed  Google Scholar 

  • Wise, R. A. (2008). Dopamine and reward: The anhedonia hypothesis 30 years on. Neurotoxicity Research, 14(2–3), 169–183.

    PubMed  Google Scholar 

  • Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage, 14(6), 1370–1386.

    PubMed  Google Scholar 

  • Xi, Z. X., & Gardner, E. L. (2008). Hypothesis-driven medication discovery for the treatment of psychostimulant addiction. Current Drug Abuse Reviews, 1(3), 303–327.

    PubMed  Google Scholar 

Download references

Acknowledgments

Assistance for this study was provided by the Neuroimaging Core and the Participant Registry Core of the UNC Carolina Institute for Developmental Disabilities (P30 HD03110). The authors thank Dr. Brian Knutson for kindly sharing the MID task, Josh Bizzell and Chris Petty for assistance with image analysis, and MRI technologists Susan Music, Natalie Goutkin, and Luke Poole for assistance with data acquisition.

Author information

Authors and Affiliations

  1. Carolina Institute for Developmental Disabilities, University of North Carolina at Chapel Hill School of Medicine, CB# 3366, 101 Manning Drive, Chapel Hill, NC, 27599-3366, USA

    Gabriel S. Dichter, J. Anthony Richey, Alison M. Rittenberg & James W. Bodfish

  2. Department of Psychiatry, University of North Carolina at Chapel Hill School of Medicine, CB# 7160, Chapel Hill, NC, 27599-7160, USA

    Gabriel S. Dichter & James W. Bodfish

  3. Duke-UNC Brain Imaging and Analysis Center, Duke University Medical Center, Durham, NC, 27710, USA

    Gabriel S. Dichter

  4. Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Box 3026, Durham, NC, 27710, USA

    Gabriel S. Dichter

  5. Department of Psychology, University of North Carolina at Chapel Hill, Davie Hall, Chapel Hill, NC, 27599-3270, USA

    Antoinette Sabatino

Authors
  1. Gabriel S. Dichter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Anthony Richey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alison M. Rittenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antoinette Sabatino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James W. Bodfish
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriel S. Dichter.

Additional information

Gabriel S. Dichter, and J. Anthony Richey contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 388 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dichter, G.S., Richey, J.A., Rittenberg, A.M. et al. Reward Circuitry Function in Autism During Face Anticipation and Outcomes. J Autism Dev Disord 42, 147–160 (2012). https://doi.org/10.1007/s10803-011-1221-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-011-1221-1

Keywords

Search

Navigation