The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood

Liana Romaniuk (Corresponding Author), Anca-Larisa Sandu-Giuraniuc, Gordon D. Waiter, Christopher J. McNeil, Shen Xueyi, Matthew A. Harris, Jennifer A. Macfarlane, Stephen M. Lawrie, Ian J. Deary, Alison D. Murray, Mauricio R. Delgardo, J. Douglas Steele, Andrew M. McIntosh, Heather C. Whalley

Research output: Contribution to journalArticle

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Abstract

Background: The majority of reward learning neuroimaging studies have not focussed on the motivational aspects of behaviour, such as the inherent value placed on choice itself. The experience and affective value of personal control may have particular relevance for psychiatric disorders including depression. Methods/Design: In this study, we adapted an fMRI reward task that probed the value placed on exerting control over one’s decisions, termed ‘choice value’, in 122 healthy participants. We examined activation associated with choice value; personally-chosen versus passively-received rewards; and reinforcement learning metrics such as prediction error. Relationships were tested between measures of motivational orientation (categorised as Autonomy, Control and Impersonal), and subclinical depressive symptomatology. Results: Anticipating personal choice activated left insula, cingulate, right inferior frontal cortex and ventral striatum (P<0.05 FWE-corrected). Ventral striatal activations to choice were diminished in those with subclinical depressive symptomatology. Personally-chosen rewards were associated with greater activation of the insula/IFG, cingulate cortex, hippocampus, thalamus and substantia nigra compared to rewards that were passively received. In people who felt little control over their own behaviour (Impersonal orientation), prediction error signals in nucleus accumbens were stronger during passive trials. Discussion: The choice value component is a significant addition to traditional reward tasks. It allows reward networks to be viewed through the lens of an individual’s beliefs and preferences in making decisions, relating to themes critical to psychiatric illness such as motivational anhedonia and self-esteem. This tool may help identify illness subgroups according to the environmental and genetic contributors to self-motivation.
Original languageEnglish
Pages (from-to)190-199
Number of pages10
JournalBiological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume4
Issue number2
Early online date9 Oct 2018
DOIs
Publication statusPublished - Feb 2019

Keywords

  • depression
  • imaging
  • locus of causality
  • perceived control
  • reward learning
  • value of choice
  • Reward learning
  • Imaging
  • Locus of causality
  • Depression
  • Value of choice
  • Perceived control
  • SELF-DETERMINATION
  • PERSPECTIVE
  • STIMULI
  • MOTIVATION
  • GENERAL CAUSALITY ORIENTATIONS
  • ANATOMY
  • REGRET
  • COGNITIVE CONTROL
  • NEURAL MODEL
  • FMRI

ASJC Scopus subject areas

  • Clinical Neurology
  • Biological Psychiatry
  • Cognitive Neuroscience
  • Radiology Nuclear Medicine and imaging

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  • Cite this

    Romaniuk, L., Sandu-Giuraniuc, A-L., Waiter, G. D., McNeil, C. J., Xueyi, S., Harris, M. A., Macfarlane, J. A., Lawrie, S. M., Deary, I. J., Murray, A. D., Delgardo, M. R., Steele, J. D., McIntosh, A. M., & Whalley, H. C. (2019). The Neurobiology of Personal Control During Reward Learning and Its Relationship to Mood. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(2), 190-199. https://doi.org/10.1016/j.bpsc.2018.09.015