Skip to main content

Advertisement

SpringerLink
Log in

Responsivity to familiar versus unfamiliar social reward in children with autism

  • Psychiatry and Preclinical Psychiatric Studies - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

In autism spectrum disorders (ASD), social motivation theories suggest that the core social communication problems seen in children with ASD arise from diminished responsiveness to social reward. Although clinical and experimental data support these theories, the extent to which the reward deficit in ASD is unique for social rewards remains unclear. With the present investigation, we aimed to provide insight into the degree to which sociality as well as familiarity of reward incentives impact motivated goal-directed behavior in children with ASD. To do so, we directly compared the influence of familiar versus unfamiliar social reward relative to nonsocial, monetary reward in children with ASD relative to age- and IQ-matched typically developing controls (TDC) using a visual and auditory incentive go/nogo task with reward contingencies for successful response inhibitions. We found that children with ASD responded stronger to visual familiar and unfamiliar social reward as well as to nonsocial, monetary reward than TDC. While the present data are at odds with predictions made by social motivation theories, individual variations beyond clinical diagnosis, such as reward exposure across various social settings, help explain the pattern of results. The findings of this study stress the necessity for additional research on intra-individual as well as environmental factors that contribute to social reward responsiveness in individuals with ASD versus other neuropsychiatric disorders such as ADHD or conduct disorder.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abrams DA, Lynch CJ, Cheng KM, Phillips J, Supekar K, Ryali S, Uddin LQ, Menon V (2013) Underconnectivity between voice-selective cortex and reward circuitry in children with autism. Proc Natl Acad Sci USA 110(29):12060–12065

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Acevedo BP, Aron A, Fisher HE, Brown LL (2012) Neural correlates of long-term intense romantic love. Soc Cogn Affect Neurosci 7:145–159

    Article  PubMed Central  PubMed  Google Scholar 

  • Achenbach TM (1991) Manual for the child behavior checklist/4–18 and 1991 profile. University of Vermont, Department of Psychiatry, Burlington

    Google Scholar 

  • Aron A, Fisher H, Mashek DJ, Strong G, Li H, Brown LL (2005) Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol 94:327–337

    Article  PubMed  Google Scholar 

  • Assaf M, Hyatt CJ, Wong CG, Johnson MR, Schultz RT, Hendler T, Pearlson GD (2013) Mentalizing and motivation neural function during social interactions in autism spectrum disorders. NeuroImage Clin 3:321–331

    Article  PubMed Central  PubMed  Google Scholar 

  • Bartels A, Zeki S (2004) The neural correlates of maternal and romantic love. NeuroImage 21:1155–1166

    Article  PubMed  Google Scholar 

  • Bray S, O’Doherty J (2007) Neural coding of reward-prediction error signals during classical conditioning with attractive faces. J Neurophysiol 97:3036–3045

    Article  PubMed  Google Scholar 

  • Cascio CJ, Foss-Feig JH, Heacock JL, Newsom CR, Cowan RL, Benningfield MM, Rogers BP, Cao A (2012) Response of neural reward regions to food cues in autism spectrum disorders. J Neurodev Disord 4:9

    Article  PubMed Central  PubMed  Google Scholar 

  • Cascio CJ, Foss-Feig JH, Heacock J, Schauder KB, Loring WA, Rogers BP, Pryweller JR, Newsom CR, Cockhren J, Cao A et al (2013) Affective neural response to restricted interests in autism spectrum disorders. J Child Psychol Psychiatry 55(2):162–171

    Article  PubMed  Google Scholar 

  • Casey BJ, Tottenham N, Fossella J (2002) Clinical, imaging, lesion, and genetic approaches toward a model of cognitive control. Dev Psychobiol 40:237–254

    Article  CAS  PubMed  Google Scholar 

  • Ceponiene R, Lepistö T, Shestakova A, Vanhala R, Alku P, Näätänen R, Yaguchi K (2003) Speech-sound-selective auditory impairment in children with autism: they can perceive but do not attend. Proc Natl Acad Sci USA 100:5567–5572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chevallier C, Kohls G, Troiani V, Brodkin ES, Schultz RT (2012) The social motivation theory of autism. Trends Cogn Sci 16:231–239

    Article  PubMed Central  PubMed  Google Scholar 

  • Cohen J (1992) A power primer. Psychol Bull 112:155–159

    Article  CAS  PubMed  Google Scholar 

  • Constantino J, Gruber C (2005) The social responsiveness scale (SRS) manual. Western Psychological Services, Los Angeles

    Google Scholar 

  • Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, Alexander AL, Davidson RJ (2005) Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 8:519–526

    CAS  PubMed  Google Scholar 

  • Dawson G (2008) Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder. Dev Psychopathol 20:775–803

    Article  PubMed  Google Scholar 

  • Dawson G, Zanolli K (2003) Early intervention and brain plasticity in autism. In: Bock G, Goode J (eds) Autism: neural bases and treatment possibilities. Wiley, Chichester, pp 266–280

    Google Scholar 

  • Dawson G, Meltzoff AN, Osterling J, Rinaldi J (1998) Neuropsychological correlates of early symptoms of autism. Child Dev 69:1276–1285

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dawson G, Osterling J, Rinaldi J, Carver L, McPartland J (2001) 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

    Article  CAS  PubMed  Google Scholar 

  • Dawson G, Toth K, Abbott R, Osterling J, Munson J, Estes A, Liaw J (2004) Early social attention impairments in autism: social orienting, joint attention, and attention to distress. Dev Psychol 40:271–283

    Article  PubMed  Google Scholar 

  • Dawson G, Webb SJ, McPartland J (2005) Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol 27:403–424

    Article  PubMed  Google Scholar 

  • Delmonte S, Balsters JH, McGrath J, Fitzgerald J, Brennan S, Fagan AJ, Gallagher L (2012) Social and monetary reward processing in autism spectrum disorders. Mol Autism 3:7

    Article  PubMed Central  PubMed  Google Scholar 

  • Demurie E, Roeyers H, Baeyens D, Sonuga-Barke E (2011) Common alterations in sensitivity to type but not amount of reward in ADHD and autism spectrum disorders. J Child Psychol Psychiatry 52:1164–1173

    Article  PubMed  Google Scholar 

  • Demurie E, Roeyers H, Wiersema JR, Sonuga-Barke E (2013a) No evidence for inhibitory deficits or altered reward processing in ADHD: data from a new integrated monetary incentive delay go/no-go task. J Atten Disord. doi:10.1177/1087054712473179

  • Demurie E, Roeyers H, Baeyens D, Sonuga-Barke E (2013b) Domain-general and domain-specific aspects of temporal discounting in children with ADHD and autism spectrum disorders (ASD): a proof of concept study. Res Dev Disabil 34:1870–1880

    Article  PubMed  Google Scholar 

  • Dichter GS, Damiano CA, Allen JA (2012a) Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings. J Neurodev Disord 4:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Dichter GS, Felder JN, Green SR, Rittenberg AM, Sasson NJ, Bodfish JW (2012b) Reward circuitry function in autism spectrum disorders. Soc Cogn Affect Neurosci 7:160–172

    Article  PubMed Central  PubMed  Google Scholar 

  • Döpfner M, Lehmkuhl G (1998) Diagnostik-System für psychische Störungen im Kindes- und Jugendalter nach ICD-10 und DSM-IV. Huber Verlag, Bern

    Google Scholar 

  • Ewing L, Pellicano E, Rhodes G (2013) Using effort to measure reward value of faces in children with autism. PLoS One 8:e79493

    Article  PubMed Central  PubMed  Google Scholar 

  • Fabes RA, Fultz J, Eisenberg N, May-Plumlee T, Scott F (1989) Effects of rewards on children’s prosocial motivation: a socialization study. Dev Psychol 25:509–515

    Article  Google Scholar 

  • Freitag G (1970) An experimental study of the social responsiveness of children with autistic behaviors. J Exp Child Psychol 9:436–453

    Article  CAS  PubMed  Google Scholar 

  • Garretson HB, Fein D, Waterhouse L (1990) Sustained attention in children with autism. J Autism Dev Disord 20:101–114

    Article  CAS  PubMed  Google Scholar 

  • Geurts HM, Luman M, van Meel CS (2008) What’s in a game: the effect of social motivation on interference control in boys with ADHD and autism spectrum disorders. J Child Psychol Psychiatry 49:848–857

    Article  PubMed  Google Scholar 

  • Gewirtz JL, Baer DM (1958) Deprivation and satiation of social reinforcers as drive conditions. J Abnorm Soc Psychol 57:165–172

    Article  CAS  Google Scholar 

  • Gleissner U, von Ondarza G, Freitag H, Karlmeier A (2003) Auswahl einer HAWIK-III-Kurzform für Kinder und Jugendliche mit Epilepsie. Z Für Neuropsychol. 14:3–11

    Article  Google Scholar 

  • Gossen A, Groppe SE, Winkler L, Kohls G, Herrington J, Schultz RT, Gründer G, Spreckelmeyer KN (2013) Neural evidence for an association between social proficiency and sensitivity to social reward. Soc Cogn Affect Neurosci. doi:10.1093/scan/nst033

  • Grossman JB, Carter A, Volkmar FR (1997) Social behavior in autism. Ann N Y Acad Sci 807:440–454

    Article  CAS  PubMed  Google Scholar 

  • Hudry K, Slaughter V (2009) Agent familiarity and emotional context influence the everyday empathic responding of young children with autism. Res Autism Spectr Disord 3:74–85

    Article  Google Scholar 

  • Jones W, Klin A (2013) Attention to eyes is present but in decline in 2–6-month-old infants later diagnosed with autism. Nature 504:427–431

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones EJH, Webb SJ, Estes A, Dawson G (2013) Rule learning in autism: the role of reward type and social context. Dev Neuropsychol 38:58–77

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamp-Becker I, Mattejat F, Wolf-Ostermann K, Remschmidt H (2005) The Marburg Rating Scale for Asperger’s syndrome (MBAS): a screening instrument for high-functioning autistic disorders. Z Für Kinder- Jugendpsychiatrie Psychother 33:15–26

    Article  Google Scholar 

  • Kanner L (1943) Autistic disturbances of affective contact. Nerv Child 2:217–250

    Google Scholar 

  • Kasari C, Sigman M, Yirmiya N (1993) Focused and social attention of autistic children in interactions with familiar and unfamiliar adults: a comparison of autistic, mentally retarded, and normal children. Dev Psychopathol 5:403–414

    Article  Google Scholar 

  • Klin A (1991) Young autistic children’s listening preferences in regard to speech: a possible characterization of the symptom of social withdrawal. J Autism Dev Disord 21:29–42

    Article  CAS  PubMed  Google Scholar 

  • Knott F, Lewis C, Williams T (1995) Sibling interaction of children with learning disabilities: a comparison of autism and Down’s syndrome. J Child Psychol Psychiatry 36:965–976

    Article  CAS  PubMed  Google Scholar 

  • Koegel RL, Koegel LK, McNerney EK (2001) Pivotal areas in intervention for autism. J Clin Child Psychol 30:19–32

    Article  CAS  PubMed  Google Scholar 

  • Kohls G, Peltzer J, Herpertz-Dahlmann B, Konrad K (2009a) Differential effects of social and non-social reward on response inhibition in children and adolescents. Dev Sci 12:614–625

    Article  PubMed  Google Scholar 

  • Kohls G, Herpertz-Dahlmann B, Konrad K (2009b) Hyperresponsiveness to social rewards in children and adolescents with attention-deficit/hyperactivity disorder (ADHD). Behav Brain Funct 5:20

    Article  PubMed Central  PubMed  Google Scholar 

  • Kohls G, Peltzer J, Schulte-Rüther M, Kamp-Becker I, Remschmidt H, Herpertz-Dahlmann B, Konrad K (2011) Atypical brain responses to reward cues in autism as revealed by event-related potentials. J Autism Dev Disord 41:1523–1533

    Article  PubMed  Google Scholar 

  • Kohls G, Chevallier C, Troiani V, Schultz RT (2012) Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications. J Neurodev Disord 4:10

    Article  PubMed Central  PubMed  Google Scholar 

  • Kohls G, Schulte-Rüther M, Nehrkorn B, Müller K, Fink GR, Kamp-Becker I, Herpertz-Dahlmann B, Schultz RT, Konrad K (2013a) Reward system dysfunction in autism spectrum disorders. Soc Cogn Affect Neurosci 8:565–572

    Article  PubMed Central  PubMed  Google Scholar 

  • Kohls G, Perino MT, Taylor JM, Madva EN, Cayless SJ, Troiani V, Price E, Faja S, Herrington JD, Schultz RT (2013b) The nucleus accumbens is involved in both the pursuit of social reward and the avoidance of social punishment. Neuropsychologia 51:2062–2069

    Article  PubMed  Google Scholar 

  • Konstantareas MM, Homatidis S (1992) Mothers’ and fathers’ self-report of involvement with autistic, mentally delayed, and normal children. J Marriage Fam 54:153

    Article  Google Scholar 

  • Kuhl PK, 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. Dev Sci 8:F1–F12

    Article  PubMed  Google Scholar 

  • Kylliäinen A, Wallace S, Coutanche MN, Leppänen JM, Cusack J, Bailey AJ, Hietanen JK (2012) Affective-motivational brain responses to direct gaze in children with autism spectrum disorder. J Child Psychol Psychiatry 53:790–797

    Article  PubMed  Google Scholar 

  • Leyfer OT, Folstein SE, Bacalman S, Davis NO, Dinh E, Morgan J, Tager-Flusberg H, Lainhart JE (2006) Comorbid psychiatric disorders in children with autism: interview development and rates of disorders. J Autism Dev Disord 36:849–861

    Article  PubMed  Google Scholar 

  • Lin A, Rangel A, Adolphs R (2012) Impaired learning of social compared to monetary rewards in autism. Front Neurosci 6:143

    Article  PubMed Central  PubMed  Google Scholar 

  • Lloyd-Fox S, Blasi A, Elwell CE, Charman T, Murphy D, Johnson MH (2013) Reduced neural sensitivity to social stimuli in infants at risk for autism. Proc Biol Sci 280:20123026

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lord C, Hopkins JM (1986) The social behavior of autistic children with younger and same-age nonhandicapped peers. J Autism Dev Disord 16:249–262

    Article  CAS  PubMed  Google Scholar 

  • Lord C, Rutter M, Le Couteur A (1994) Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24:659–685

    Article  CAS  PubMed  Google Scholar 

  • Lord C, Risi S, Lambrecht L, Cook EH Jr, Leventhal BL, DiLavore PC, Pickles A, Rutter M (2000) The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30:205–223

    Article  CAS  PubMed  Google Scholar 

  • Luman M, Oosterlaan J, Sergeant JA (2005) The impact of reinforcement contingencies on AD/HD: a review and theoretical appraisal. Clin Psychol Rev 25:183–213

    Article  PubMed  Google Scholar 

  • Luman M, Tripp G, Scheres A (2010) Identifying the neurobiology of altered reinforcement sensitivity in ADHD: a review and research agenda. Neurosci Biobehav Rev 34:744–754

    Article  PubMed  Google Scholar 

  • Matson JL, Benavidez DA, Compton LS, Paclawskyj T, Baglio C (1996) Behavioral treatment of autistic persons: a review of research from 1980 to the present. Res Dev Disabil 17:433–465

    Article  CAS  PubMed  Google Scholar 

  • Matthys W, van Goozen SH, de Vries H, Cohen-Kettenis PT, van Engeland H (1998) The dominance of behavioural activation over behavioural inhibition in conduct disordered boys with or without attention deficit hyperactivity disorder. J Child Psychol Psychiatry 39:643–651

    Article  CAS  PubMed  Google Scholar 

  • Mobbs D, Hassabis D, Seymour B, Marchant JL, Weiskopf N, Dolan RJ, Frith CD (2009) Choking on the money: reward-based performance decrements are associated with midbrain activity. Psychol Sci 20:955–962

    Article  PubMed Central  PubMed  Google Scholar 

  • Mundy P (1995) Joint attention and social−emotional approach behavior in children with autism. Dev Psychopathol 7:63–82

    Article  Google Scholar 

  • Munson J, Faja S, Meltzoff A, Abbott R, Dawson G (2008) Neurocognitive predictors of social and communicative developmental trajectories in preschoolers with autism spectrum disorders. J Int Neuropsychol Soc 14:956–966

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Connor K, Kirk I (2008) Brief report: atypical social cognition and social behaviours in autism spectrum disorder: a different way of processing rather than an impairment. J Autism Dev Disord 38:1989–1997

    Article  PubMed  Google Scholar 

  • Oberman LM, Ramachandran VS, Pineda JA (2008) Modulation of mu suppression in children with autism spectrum disorders in response to familiar or unfamiliar stimuli: the mirror neuron hypothesis. Neuropsychologia 46:1558–1565

    Article  PubMed  Google Scholar 

  • Ortigue S, Bianchi-Demicheli F, Hamilton AF, Grafton ST (2007) The neural basis of love as a subliminal prime: an event-related functional magnetic resonance imaging study. J Cogn Neurosci 19:1218–1230

    Article  CAS  PubMed  Google Scholar 

  • Pierce K, Redcay E (2008) Fusiform function in children with an autism spectrum disorder is a matter of “who”. Biol Psychiatry 64:552–560

    Article  PubMed Central  PubMed  Google Scholar 

  • Pierce K, Müller RA, Ambrose J, Allen G, Courchesne E (2001) Face processing occurs outside the fusiform “face area” in autism: evidence from functional MRI. Brain J Neurol 124:2059–2073

    Article  CAS  Google Scholar 

  • Pierce K, Haist F, Sedaghat F, Courchesne E (2004) The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain J Neurol 127:2703–2716

    Article  Google Scholar 

  • Power TJ (1992) Contextual factors in vigilance testing of children with ADHD. J Abnorm Child Psychol 20:579–593

    Article  CAS  PubMed  Google Scholar 

  • Ruble LA (2001) Analysis of social interactions as goal-directed behaviors in children with autism. J Autism Dev Disord 31:471–482

    Article  CAS  PubMed  Google Scholar 

  • Rutter M, Bailey A, Lord C (2003) The social communication questionnaire. Western Psychological Services, Los Angeles

    Google Scholar 

  • Sasson NJ, Turner-Brown LM, Holtzclaw TN, Lam KSL, Bodfish JW (2008) Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism 1:31–42

    Article  Google Scholar 

  • Schultz RT (2005) Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci 23:125–141

    Article  PubMed  Google Scholar 

  • Scott-Van Zeeland AA, Dapretto M, Ghahremani DG, Poldrack RA, Bookheimer SY (2010) Reward processing in autism. Autism Res 3:53–67

    PubMed Central  PubMed  Google Scholar 

  • van der Meer JM, Oerlemans AM, van Steijn DJ, Lappenschaar MG, de Sonneville LM, Buitelaar JK, Rommelse NN (2012) Are autism spectrum disorder and attention-deficit/hyperactivity disorder different manifestations of one overarching disorder? Cognitive and symptom evidence from a clinical and population-based sample. J Am Acad Child Adolesc Psychiatry 51(11):1160–1172.e3. doi:10.1016/j.jaac.2012.08.024

    Google Scholar 

  • Van Hecke AV, Lebow J, Bal E, Lamb D, Harden E, Kramer A, Denver J, Bazhenova O, Porges SW (2009) Electroencephalogram and heart rate regulation to familiar and unfamiliar people in children with autism spectrum disorders. Child Dev 80:1118–1133

    Article  Google Scholar 

  • Vloet TD, Konrad K, Herpertz-Dahlmann B, Kohls G (2011) The effect of social and monetary reward on inhibitory control in boys with hyperkinetic conduct disorder. Z Für Kinder- Jugendpsychiatrie Psychother 39:341–349

    Article  Google Scholar 

  • Wing L, Gould J (1979) Severe impairments of social interaction and associated abnormalities in children: epidemiology and classification. J Autism Dev Disord 9:11–29

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank all young volunteers and their families who participated in this study. We also thank Astrid Pütz-Ebert for her help with data collection. This study was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft/DFG, IRTG 1328). We are also very grateful to two anonymous reviewers for their helpful comments on earlier versions of the manuscript.

Conflict of interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, RWTH Aachen University, Neuenhofer Weg 21, 52074, Aachen, Germany

    Azarakhsh Pankert, Kilian Pankert, Kerstin Konrad & Gregor Kohls

  2. Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, RWTH Aachen University, Neuenhofer Weg 21, 52074, Aachen, Germany

    Beate Herpertz-Dahlmann

Authors
  1. Azarakhsh Pankert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kilian Pankert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beate Herpertz-Dahlmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kerstin Konrad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gregor Kohls
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregor Kohls.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pankert, A., Pankert, K., Herpertz-Dahlmann, B. et al. Responsivity to familiar versus unfamiliar social reward in children with autism. J Neural Transm 121, 1199–1210 (2014). https://doi.org/10.1007/s00702-014-1210-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-014-1210-6

Keywords

Search

Navigation