Skip to main content
Log in

Role of contingency in striatal response to incentive in adolescents with anxiety

  • Published:
Cognitive, Affective, & Behavioral Neuroscience Aims and scope Submit manuscript

Abstract

This study examines the effect of contingency on reward function in anxiety. We define contingency as the aspect of a situation in which the outcome is determined by one’s action—that is, when there is a direct link between one’s action and the outcome of the action. Past findings in adolescents with anxiety or at risk for anxiety have revealed hypersensitive behavioral and neural responses to higher value rewards with correct performance. This hypersensitivity to highly valued (salient) actions suggests that the value of actions is determined not only by outcome magnitude, but also by the degree to which the outcome is contingent on correct performance. Thus, contingency and incentive value might each modulate reward responses in unique ways in anxiety. Using fMRI with a monetary reward task, striatal response to cue anticipation is compared in 18 clinically anxious and 20 healthy adolescents. This task manipulates orthogonally reward contingency and incentive value. Findings suggest that contingency modulates the neural response to incentive magnitude differently in the two groups. Specifically, during the contingent condition, right-striatal response tracks incentive value in anxious, but not healthy, adolescents. During the noncontingent condition, striatal response is bilaterally stronger to low than to high incentive in anxious adolescents, while healthy adolescents exhibit the expected opposite pattern. Both contingency and reward magnitude differentiate striatal activation in anxious versus healthy adolescents. These findings may reflect exaggerated concern about performance and/or alterations of striatal coding of reward value in anxious adolescents. Abnormalities in reward function in anxiety may have treatment implications.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–81.

    Article  PubMed  Google Scholar 

  • Bar-Haim, Y., Fox, N. A., Benson, B., Guyer, A. E., Williams, A., Nelson, E. E., ... Ernst, M. (2009). Neural correlates of reward processing in adolescents with a history of inhibited temperament. Psychological Science, 20(8), 1009–1018.

    Article  PubMed Central  PubMed  Google Scholar 

  • Berns, G. S., & Bell, E. (2012). Striatal topography of probability and magnitude information for decisions under uncertainty. NeuroImage, 59(4), 3166.

    Article  PubMed Central  PubMed  Google Scholar 

  • Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry, 36(4), 545–553.

    Article  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, 165–70.

    Article  PubMed Central  PubMed  Google Scholar 

  • Blackford, J. U., & Pine, D. S. (2012). Neural substrates of childhood anxiety disorders: a review of neuroimaging findings. Child and Adolescent Psychiatric Clinics of North America, 21(3), 501–525.

    Article  PubMed Central  PubMed  Google Scholar 

  • Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., ... Fox, N. A. (2009). Stable Early Maternal Report of Behavioral Inhibition Predicts Lifetime Social Anxiety Disorder in Adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 48(9), 928–935.

    Article  Google Scholar 

  • Cohen, M. S. (1997). Parametric analysis of fMRI data using linear systems methods. NeuroImage, 6(2), 93–103.

    Article  PubMed  Google Scholar 

  • Cooper, J. C., & Knutson, B. (2008). Valence and salience contribute to nucleus accumbens activation. NeuroImage, 39(1), 538–47.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–73.

    Article  PubMed  Google Scholar 

  • Dreher, J. C., Kohn, P., & Berman, K. F. (2006). Neural coding of distinct statistical properties of reward information in humans. Cerebral Cortex, 16(4), 561–573.

    Article  PubMed  Google Scholar 

  • Dugas, M. J., Buhr, K., & Ladouceur, R. (2004). The Role of Intolerance of Uncertainty in Etiology and Maintenance. In R. G. Heimberg, C. L. Turk, & D. S. Mennin (Eds.), Generalized anxiety disorder: Advances in research and practice (pp. 143–163). New York: Guilford Press.

    Google Scholar 

  • Ernst, M., Daniele, T., & Frantz, K. (2011). New perspectives on adolescent motivated behavior: Attention and conditioning. Developmental Cognitive Neuroscience, 1(4), 377–389.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fox, N. A., Henderson, H. A., Marshall, P. J., Nichols, K. E., & Ghera, M. M. (2005). Behavioral inhibition: linking biology and behavior within a developmental framework. Annual Review of Psychology, 56, 235–262.

    Article  PubMed  Google Scholar 

  • Guyer, A. E., Choate, V. R., Detloff, A., Benson, B., Nelson, E. E., Perez-Edgar, K., ... Ernst, M. (2012). Striatal functional alteration during incentive anticipation in pediatric anxiety disorders. The American Journal of Psychiatry, 169(2), 205–212.

    Article  PubMed Central  PubMed  Google Scholar 

  • Guyer, A. E., Lau, J. Y., McClure-Tone, E. B., Parrish, J., Shiffrin, N. D., Reynolds, R. C., ... Nelson, E. E. (2008). Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry, 65(11), 1303–1312.

    Article  PubMed Central  PubMed  Google Scholar 

  • Guyer, A. E., Nelson, E. E., Perez-Edgar, K., Hardin, M. G., Roberson-Nay, R., Monk, C. S., ... Ernst, M. (2006). Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition. Journal of Neuroscience, 26(24), 6399–6405.

    Article  PubMed  Google Scholar 

  • Haber, S. N. (2003). The primate basal ganglia: parallel and integrative networks. Journal of Chemical Neuroanatomy, 26, 317–30.

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Hardin, M. G., Perez-Edgar, K., Guyer, A. E., Pine, D. S., Fox, N. A., & Ernst, M. (2006). Reward and punishment sensitivity in shy and non-shy adults: Relations between social and motivated behavior. Personality and Individual Differences, 40(4), 699–711.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hardin, M. G., Pine, D. S., & Ernst, M. (2009). The influence of context valence in the neural coding of monetary outcomes. NeuroImage, 48(1), 249–257.

    Article  PubMed Central  PubMed  Google Scholar 

  • Helfinstein, S. M., Benson, B., Perez-Edgar, K., Bar-Haim, Y., Detloff, A., Pine, D. S., ... Ernst, M. (2011). Striatal responses to negative monetary outcomes differ between temperamentally inhibited and non-inhibited adolescents. Neuropsychologia, 49(3), 479–485.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hollingshead, A. B. (1975). Four-factor index of social status. In Unpublished manuscript. New Haven, CT: Yale University, Department of Sociology.

  • Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., ... Ryan, N. (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 980–988.

    Article  PubMed  Google Scholar 

  • Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 593–602.

    Article  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.

    Article  PubMed  Google Scholar 

  • Kovacs, M. (1992). Children's Depression Inventory. New York: Multi-Health Systems.

    Google Scholar 

  • Krain, A. L., Gotimer, K., Hefton, S., Ernst, M., Castellanos, F. X., Pine, D. S., & Milham, M. P. (2008). A Functional Magnetic Resonance Imaging Investigation of Uncertainty in Adolescents with Anxiety Disorders. Biological Psychiatry, 63(6), 563–568.

  • Krain, A. L., Hefton, S., Pine, D. S., Ernst, M., Castellanos, F. X., Klein, R. G., & Milham, M. P. (2006). An fMRI examination of developmental differences in the neural correlates of uncertainty and decision-making. Journal of Child Psychology and Psychiatry, 47(10), 1023–1030.

  • Leonardo, E. D., & Hen, R. (2008). Anxiety as a developmental disorder. Neuropsychopharmacology, 33(1), 134–140.

    Article  PubMed  Google Scholar 

  • Leotti, L. A., & Delgado, M. R. (2011). The inherent reward of choice. Psychological Science, 22, 1310–8.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lorian, C. N., & Grisham, J. R. (2010). The Safety Bias: Risk-Avoidance and Social Anxiety Pathology. Behaviour Change, 27(1), 29–41.

    Article  Google Scholar 

  • MacLeod, C., Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95, 15–20.

    Article  PubMed  Google Scholar 

  • McClure, E. B., Monk, C. S., Nelson, E. E., Parrish, J. M., Adler, A., Blair, R. J., ... Pine, D. S. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64(1), 97–106.

    Article  PubMed  Google Scholar 

  • Mogenson, G., Jones, D., & Yim, C. (1980). From motivation to action: Functional interface between the limbic system and the motor system. Progress in Neurobiology, 14, 69–97.

    Article  PubMed  Google Scholar 

  • Mogg, K., & Bradley, B. P. (1998). A Cognitive-motivational analysis of anxiety. Behaviour Research and Therapy, 36, 809–8481.

    Article  PubMed  Google Scholar 

  • Monk, C. S., Nelson, E. E., McClure, E. B., Mogg, K., Bradley, B. P., Leibenluft, E., ... Pine, D. S. (2006). Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. The American Journal of Psychiatry, 163(6), 1091–1097.

    Article  PubMed  Google Scholar 

  • Mueller, E. M., Nguyen, J., Ray, W. J., & Borkovec, T. D. (2010). Future-oriented decision-making in Generalized Anxiety Disorder is evident across different versions of the Iowa Gambling Task. Journal of Behavior Therapy and Experimental Psychiatry, 41(2), 165–171.

    Article  PubMed  Google Scholar 

  • Neter, J., Kutner, M. H., Machtsheim, C. J., & Wasserman, W. (1996). Applied linear statistical models (4th ed.). Chicago: Irwin.

    Google Scholar 

  • O’Doherty, J. P. (2004). Reward represantations and reward-related learning in the human brain: insights from neuroimaging. Current Opinion in Neurobiology, 14, 769–76.

    Article  PubMed  Google Scholar 

  • Perez-Edgar, K., & Fox, N. A. (2005). Temperament and anxiety disorders. Child and Adolescent Psychiatric Clinics of North America, 14(4), 681–706. viii.

    Article  PubMed  Google Scholar 

  • Pine, D. S., Helfinstein, S. M., Bar-Haim, Y., Nelson, E., & Fox, N. A. (2009). Challenges in Developing Novel Treatments for Childhood Disorders: Lessons from Research on Anxiety. Neuropsychopharmacology, 34(1), 213–228.

    Article  PubMed Central  PubMed  Google Scholar 

  • Richards, J. M., Plate, R. C., & Ernst, M. (2012). Neural systems underlying motivated behavior in adolescence: Implications for preventive medicine. Preventive Medicine, 55, S7–S16.

    Article  PubMed Central  PubMed  Google Scholar 

  • Roy, A. K., Gotimer, K., Kelly, A. M. C., Castellanos, F. X., Milham, M. P., & Ernst, M. (2011). Uncovering putative neural markers of risk avoidance. Neuropsychologia, 49(5), 937–944.

    Article  PubMed Central  PubMed  Google Scholar 

  • Shaffer, D., Gould, M. S., Brasic, J., Ambrosini, P., Fisher, P., Bird, H., & Aluwahlia, S. (1983). A children's global assessment scale (CGAS). Archives of General Psychiatry, 40(11), 1228–1231.

    Article  PubMed  Google Scholar 

  • Shechner, T., Britton, J. C., Pérez-Edgar, K., Bar-Haim, Y., Ernst, M., Fox, N. A., ... Pine, D. S. (2012). Attention biases, anxiety, and development: toward or away from threats or rewards? Depression and Anxiety, 29(4), 282–94.

    Article  PubMed Central  PubMed  Google Scholar 

  • Spielberger, C. D., Gorsuch, R. L., & Lushene, R. E. (1970). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.

    Google Scholar 

  • Talairach, J., & Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme Medical Publishers.

    Google Scholar 

  • Tricomi, E. M., Delgado, M. R., & Fiez, J. A. (2004). Modulation of caudate activity by action contingency. Neuron, 41(2), 281–292.

    Article  PubMed  Google Scholar 

  • Verduin, T. L., & Kendall, P. C. (2003). Differential occurrence of comorbidity within childhood anxiety disorders. Journal of Clinical Child and Adolescent Psychology, 32(2), 290–295.

    Article  PubMed  Google Scholar 

  • Weschler, D. (1999). Weschler abbreviated scale of intelligence (WASI). San Antonio: The Psychological Corporation.

    Google Scholar 

  • Zink, C. F., Pagnoni, G., Martin-Skurski, M. E., Chappelow, J. C., & Berns, G. S. (2004). Human striatal responses to monetary reward depend on saliency. Neuron, 42(3), 509–517.

    Article  PubMed  Google Scholar 

  • Zink, C. F., Pagnoni, G., Martin, M. E., Dhamala, M., & Berns, G. S. (2003). Human striatal response to salient nonrewarding stimuli. Journal of Neuroscience, 23(22), 8092–8097.

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Intramural Research Program of the National Institute of Mental Health (National Institutes of Health). We wish to thank the subjects and their families. We also wish to thank Rista Plate, Allison M Detloff, and Nevia Pavletic for their help in the study and manuscript preparation.

Financial Disclosures

The authors have no financial interests, relationships, or affiliations to disclose.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monique Ernst.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

(PDF 131 kb)

Fig. S2

(PDF 143 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Benson, B.E., Guyer, A.E., Nelson, E.E. et al. Role of contingency in striatal response to incentive in adolescents with anxiety. Cogn Affect Behav Neurosci 15, 155–168 (2015). https://doi.org/10.3758/s13415-014-0307-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3758/s13415-014-0307-6

Keywords

Navigation