Neural evidence for an association between social proficiency and sensitivity to social reward

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 5, 2014, Pages 661-670

  Gossen, Anna ^a,b   Groppe, Sarah E ^a,b   Winkler, Lina ^a,b   Kohls, Gregor ^c   Herrington, John ^c   Schultz, Robert T ^c   Gründer, Gerhard ^a,b   Spreckelmeyer, Katja N ^a,b,d  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b JARA TRANSLATIONAL BRAIN MEDICINE   (Germany)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Autism; Empathy; NAcc; Social interest; Social reward

Indexed keywords

ANTICIPATION; ASSOCIATION; BRAIN; BRAIN MAPPING; EMOTIONAL INTELLIGENCE; EMPATHY; HUMAN; MALE; NEUROPSYCHOLOGICAL TEST; NONVERBAL COMMUNICATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATTERN RECOGNITION; PERCEPTION; PERSONALITY; PHYSIOLOGY; QUESTIONNAIRE; REACTION TIME; REWARD; TASK PERFORMANCE; VIDEORECORDING; YOUNG ADULT;

ANTICIPATION, PSYCHOLOGICAL; BRAIN; BRAIN MAPPING; CUES; EMOTIONAL INTELLIGENCE; EMPATHY; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; NONVERBAL COMMUNICATION; PATTERN RECOGNITION, VISUAL; PERSONALITY; REACTION TIME; REWARD; SOCIAL PERCEPTION; SURVEYS AND QUESTIONNAIRES; TASK PERFORMANCE AND ANALYSIS; VIDEO RECORDING; YOUNG ADULT;

EID: 84886410696     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst033     Document Type: Article

References (68)

1. 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), 537-51.
2. Ashburner, J., Friston, K.J. (2005). Unified segmentation. Neuroimage, 26(3), 839-51.
3. Bagby, R.M., Parker, J.D., Taylor, G.J. (1994). The twenty-item Toronto Alexithymia Scale-I. Item selection and cross-validation of the factor structure. Journal of Psychosomatic Research, 38(1), 23-32.
4. Banissy, M.J., Garrido, L., Kusnir, F., Duchaine, B., Walsh, V., Ward, J. (2011). Superior facial expression, but not identity recognition, in mirror-touch synesthesia. Journal of Neuroscience, 31(5), 1820-4.
5. Baron-Cohen, S., Wheelwright, S. (2004). The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34(2), 163-75.
6. 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, 5-17.
7. Barton, J.J.S., Hefter, R.L., Cherkasova, M.V., Manoach, D.S. (2007). Investigations of face expertise in the social developmental disorders. Neurology, 69(9), 860-70.
8. Berthoz, S., Wessa, M., Kedia, G., Wicker, B., Grezes, J. (2008). Cross-cultural validation of the empathy quotient in a French-speaking sample. Canadian Journal of Psychiatry, 53(7), 469-77.
9. Chakrabarti, B., Bullmore, E., Baron-Cohen, S. (2006). Empathizing with basic emotions: Common and discrete neural substrates. Social Neuroscience, 1(3-4), 364-84.
10. Chevallier, C., Kohls, G., Troiani, V., Brodkin, E.S., Schultz, R.T. (2012). The social motivation theory of autism. Trends in Cognitive Sciences, 16(4), 231-9.
11. Clithero, J.A., Reeck, C., Carter, R.M., Smith, D.V., Huettel, S.A. (2011). Nucleus accumbens mediates relative motivation for rewards in the absence of choice. Frontiers Human Neuroscience, 5, 87.
12. Cloninger, C.R., Przybeck, T.R., Svrakic, D.M., Wetzel, R.D. (1994). The Temperament and Character Inventory: A Guide to its Development and Use. St. Louis, MO: Center for Psychobiology of Personality, Washington University.
13. Davis, M.H. (1983). Measuring individual differences in empathy: evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44(1), 113-26.
14. Davis, M.H. (1994). Empathy: A Social Psychological Approach. Boulder, CO: Westview Press.
15. Dawson, G., Bernier, R., Ring, R.H. (2012). Social attention: a possible early indicator of efficacy in autism clinical trials. Journal of Neurodevelopmental Disorders, 4(1), 11.
16. Dawson, G., Webb, S., Wijsman, E., et al. (2005). Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: implications for a model of abnormal development of social brain circuitry in autism. Development and Psychopathology, 17(3), 679-97.
17. Decety, J., Jackson, P.L. (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews, 3(2), 71-100.
18. Deutsch, F., Madle, R.A. (1975). Empathy: historic and current conceptualizations, measurement, and a cognitive theoretical perspective. Human Development, 18(4), 267-87.
19. Dichter, G., Richey, J., Rittenberg, A., Sabatino, A., Bodfish, J. (2011). Reward circuitry function in autism during face anticipation and outcomes. Journal of Autism and Developmental Disorders, 42(2), 147-60.
20. Dichter, G.S., Felder, J.N., Green, S.R., Rittenberg, A.M., Sasson, N.J., Bodfish, J.W. (2012). Reward circuitry function in autism spectrum disorders. Social Cognitive and Affective Neuroscience, 7(2), 160-72.
21. Downey, G., Feldman, S.I. (1996). Implications of rejection sensitivity for intimate relationships. Journal of Personality and Social Psychology, 70(6), 1327-43.
22. Elsabbagh, M., Mercure, E., Hudry, K., et al. (2012). Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism. Current Biology, 22(4), 338-42.
23. Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.P., Frith, C.D., Frackowiak, R.S.J. (1995). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping, 2, 189-210.
24. Grelotti, D.J., Gauthier, I., Schultz, R.T. (2002). Social interest and the development of cortical face specialization: what autism teaches us about face processing. Developmental Psychobiology, 40(3), 213-25.
25. Joseph, R.M., Tanaka, J. (2003). Holistic and part-based face recognition in children with autism. Journal of Child Psychology and Psychiatry, 44(4), 529-42.
26. Josephs, O., Turner, R., Friston, K.J. (1997). Event-related fMRI. Human Brain Mapping, 5, 243-8.
27. Kim, H., Adolphs, R., O'Doherty, J.P., Shimojo, S. (2007). Temporal isolation of neural processes underlying face preference decisions. Proceedings of the National Academy of Sciences of the United States of America, 104(46), 18253-8.
28. Kim, J., Lee, S.J. (2010). Reliability and validity of the Korean version of the empathy quotient scale. Psychiatry Investigation Psychiatry Investigation, 7(1), 24-30.
29. Kirsch, P., Schienle, A., Stark, R., et al. (2003). Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. Neuroimage, 20(2), 1086-95.
30. Klin, A., Sparrow, S.S., de Bildt, A., Cicchetti, D.V., Cohen, D.J., Volkmar, F.R. (1999). A normed study of face recognition in autism and related disorders. The Journal of Autism and Developmental Disorders, 29(6), 499-508.
31. Knutson, B., Adams, C.M., Fong, G.W., Hommer, D. (2001a). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21(16), RC159.
32. 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), 3683-7.
33. Knutson, B., Fong, G.W., Bennett, S.M., Adams, C.M., Hommer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. Neuroimage, 18(2), 263-72.
34. Knutson, B., Greer, S.M. (2008). Anticipatory affect: neural correlates and consequences for choice. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1511), 3771-86.
35. Kohls, G., Peltzer, J., Herpertz-Dahlmann, B., Konrad, K. (2009). Differential effects of social and non-social reward on response inhibition in children and adolescents. Developmental Science, 12(4), 614-25.
36. Kohls, G., Peltzer, J., Schulte-Rüther, M., et al. (2011). Atypical brain responses to reward cues in autism as revealed by event-related potentials. Journal of Autism and Developmental Disorders, 41(11), 1523-33.
37. Kohls, G., Schulte-Rüther, M., Nehrkorn, B., et al. (2013). Reward system dysfunction in autism spectrum disorders. Social Cognitive and Affective Neuroscience, 8(5), 565-72.
38. Lancaster, J.L., Woldorff, M.G., Parsons, L.M., et al. (2000). Automated Talairach Atlas labels for functional brain mapping. Human Brain Mapping, 10(3), 120-31.
39. Lawrence, E.J., Shaw, P., Baker, D., Baron-Cohen, S., David, A.S. (2004). Measuring empathy: reliability and validity of the Empathy Quotient. Psychological Medicine, 34(5), 911-9.
40. Lin, A., Adolphs, R., Rangel, A. (2012). Impaired learning of social compared to monetary rewards in autism. Frontiers in Neuroscience, 6, 143.
41. Lubben, J., Gironda, M. (2004). Measuring social networks and assessing their benefits. In: Phillipson, C., Allan, G., Morgan, D., editors. Social Networks and Social Exclusion: Sociological and Policy Perspectives. Hampshire, United Kingdom: Ashgate, pp. 20-35.
42. Maldjian, J.A., Laurienti, P.J., Kraft, R.A., Burdette, J.H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19(3), 1233-9.
43. Mundy, P., Jarrold, W. (2010). Infant joint attention, neural networks and social cognition. Neural Network, 23(8-9), 985-97.
44. Mundy, P., Neal, R.A. (2000). Neural plasticity, joint attention, and a transactional social-orienting model of autism. In: Glidden, L.M., editor. International Review of Research in Mental Retardation Autism Vol. 23, pp. 139-68., San Diego, Academic Press.
45. O'Doherty, J.P., Buchanan, T.W., Seymour, B., Dolan, R.J. (2006). Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum. Neuron, 49(1), 157-66.
46. O'Doherty, J.P., Deichmann, R., Critchley, H.D., Dolan, R.J. (2002). Neural responses during anticipation of a primary taste reward. Neuron, 33(5), 815-26.
47. Parlade, M.V., Messinger, D.S., Delgado, C.E., Kaiser, M.Y., Van Hecke, A.V., Mundy, P.C. (2009). Anticipatory smiling: linking early affective communication and social outcome. Infant Behavior and Development, 32(1), 33-43.
48. Pierce, K., Conant, D., Hazin, R., Stoner, R., Desmond, J. (2011). Preference for geometric patterns early in life as a risk factor for autism. Archives of General Psychiatry, 68(1), 101-9.
49. Rademacher, L., Krach, S., Kohls, G., Irmak, A., Gründer, G., Spreckelmeyer, K.N. (2010). Dissociation of neural networks for anticipation and consumption of monetary and social rewards. Neuroimage, 49(4), 3276-85.
50. Schneider, D., Regenbogen, C., Kellermann, T., et al. (2012). Empathic behavioral and physiological responses to dynamic stimuli in depression. Psychiatry Research, 200(2-3), 294-305.
51. 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), 125-41.
52. Schultz, R.T., Gauthier, I., Klin, A., et al. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry, 57(4), 331-40.
53. 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.
54. Sims, T.B., Van Reekum, C.M., Johnstone, T., Chakrabarti, B. (2012). How reward modulates mimicry: EMG evidence of greater facial mimicry of more rewarding happy faces. Psychophysiology, 49(7), 998-1004.
55. Spreckelmeyer, K., Krach, S., Kohls, G., et al. (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience, 4(2), 158-65.
56. Spreckelmeyer, K., Rademacher, L., Paulus, F., Gründer, G. (2012). Neural activation during anticipation of opposite-sex and same-sex faces in heterosexual men and women. Neuroimage, 66C, 223-31.
57. Staebler, K., Helbing, E., Rosenbach, C., Renneberg, B. (2010). Rejection sensitivity and borderline personality disorder. Clinical Psychology and Psychotherapy, 18(4), 275-83.
58. Strathearn, L., Fonagy, P., Amico, J., Montague, P.R. (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology, 34(13), 2655-66.
59. Tanaka, J.W., Wolf, J.M., Klaiman, C., et al. (2012). The perception and identification of facial emotions in individuals with autism spectrum disorders using the Let's Face It! Emotion Skills Battery. Journal of Child Psychology and Psychiatry, 53(12), 1259-67.
60. Thut, G., Schultz, W., Roelcke, U., et al. (1997). Activation of the human brain by monetary reward. Neuroreport, 8(5), 1225-8.
61. Triesch, J., Teuscher, C., Deák, G.O., Carlson, E. (2006). Gaze following: why (not) learn it? Developmental Science, 9(2), 125-47.
62. Van Overwalle, F., Baetens, K. (2009). Understanding others' actions and goals by mirror and mentalizing systems: a meta-analysis. Neuroimage, 48(3), 564-84.
63. Vaughan Van Hecke, A., Mundy, P.C., Acra, C.F., et al. (2007). Infant joint attention, temperament, and social competence in preschool children. Child development, 78(1), 53-69.
64. Von Horn, A., Backman, L., Davidsson, T., Hansen, S. (2010). Empathizing, systemizing and finger length ratio in a Swedish sample. Scandinavian Journal of Psychology, 51(1), 31-7.
65. Wakabayashi, A., Baron-Cohen, S., Uchiyama, T., Yoshida, Y., Kuroda, M., Wheelwright, S. (2007). Empathizing and systemizing in adults with and without autism spectrum conditions: cross-cultural stability. Journal of Autism and Developmental Disorders, 37(10), 1823-32.
66. Weigelt, S., Koldewyn, K., Kanwisher, N. (2012). Face identity recognition in autism spectrum disorders: a review of behavioral studies. Neuroscience and Biobehavioral Reviews, 36(3), 1060-84.
67. Wiseman, T. (1996). A concept analysis of empathy. Journal of Advanced Nursing, 23(6), 1162-7.
68. Wolf, J.M., Tanaka, J.W., Klaiman, C., et al. (2008). Specific impairment of face-processing abilities in children with autism spectrum disorder using the Let's Face It! skills battery. Autism Research, 1(6), 329-40.