The neurobiology of personal control during reward learning and its relation to mood

Liana Romaniuk (Lead / Corresponding author), Anca-Larisa Sandu, 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. Delgado, John Steele, Andrew M. McIntosh, Heather C. Whalley

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Abstract

BACKGROUND: The majority of reward learning neuroimaging studies have not focused on the motivational aspects of behavior, 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: We adapted a functional magnetic resonance imaging 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 (categorized as autonomy, control, and impersonal) and subclinical depressive symptoms.

RESULTS: Anticipating personal choice activated left insula, cingulate, right inferior frontal cortex, and ventral striatum (p familywise error-corrected < .05). Ventral striatal activations to choice were diminished in participants with subclinical depressive symptoms. Personally chosen rewards were associated with greater activation of the insula and inferior frontal gyrus, cingulate cortex, hippocampus, thalamus, and substantia nigra compared with rewards that were passively received. In participants who felt they had little control over their own behavior (impersonal orientation), prediction error signals in nucleus accumbens were stronger during passive trials.

CONCLUSIONS: Previous findings regarding personal choice have been verified and advanced through the use of both reinforcement learning models and correlations with psychopathology. Personal choice has an impact on the extended reward network, potentially allowing these clinically important areas to be addressed in ways more relevant to personality styles, self-esteem, and symptoms such as motivational anhedonia.

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

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Neurobiology
Reward
Learning
Depression
Anhedonia
Corpus Striatum
Gyrus Cinguli
Nucleus Accumbens
Frontal Lobe
Substantia Nigra
Prefrontal Cortex
Psychopathology
Thalamus
Self Concept
Neuroimaging
Psychiatry
Personality
Hippocampus
Healthy Volunteers
Magnetic Resonance Imaging

Keywords

  • Depression
  • Imaging
  • Locus of causality
  • Perceived control
  • Reward learning
  • Value of choice

Cite this

Romaniuk, L., Sandu, A-L., Waiter, G. D., McNeil, C. J., Xueyi, S., Harris, M. A., ... Whalley, H. C. (2019). The neurobiology of personal control during reward learning and its relation to mood. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(2), 190-199. https://doi.org/10.1016/j.bpsc.2018.09.015
Romaniuk, Liana ; Sandu, Anca-Larisa ; Waiter, Gordon D. ; McNeil, Christopher J. ; Xueyi, Shen ; Harris, Matthew A. ; MacFarlane, Jennifer A. ; Lawrie, Stephen M. ; Deary, Ian J. ; Murray, Alison D. ; Delgado, Mauricio R. ; Steele, John ; McIntosh, Andrew M. ; Whalley, Heather C. / The neurobiology of personal control during reward learning and its relation to mood. In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging. 2019 ; Vol. 4, No. 2. pp. 190-199.
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Romaniuk, L, Sandu, A-L, Waiter, GD, McNeil, CJ, Xueyi, S, Harris, MA, MacFarlane, JA, Lawrie, SM, Deary, IJ, Murray, AD, Delgado, MR, Steele, J, McIntosh, AM & Whalley, HC 2019, 'The neurobiology of personal control during reward learning and its relation to mood', Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, vol. 4, no. 2, pp. 190-199. https://doi.org/10.1016/j.bpsc.2018.09.015

The neurobiology of personal control during reward learning and its relation to mood. / Romaniuk, Liana (Lead / Corresponding author); Sandu, Anca-Larisa; Waiter, Gordon D.; McNeil, Christopher J.; Xueyi, Shen; Harris, Matthew A.; MacFarlane, Jennifer A.; Lawrie, Stephen M.; Deary, Ian J.; Murray, Alison D.; Delgado, Mauricio R.; Steele, John; McIntosh, Andrew M.; Whalley, Heather C.

In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Vol. 4, No. 2, 02.2019, p. 190-199.

Research output: Contribution to journalArticle

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AU - Romaniuk, Liana

AU - Sandu, Anca-Larisa

AU - Waiter, Gordon D.

AU - McNeil, Christopher J.

AU - Xueyi, Shen

AU - Harris, Matthew A.

AU - MacFarlane, Jennifer A.

AU - Lawrie, Stephen M.

AU - Deary, Ian J.

AU - Murray, Alison D.

AU - Delgado, Mauricio R.

AU - Steele, John

AU - McIntosh, Andrew M.

AU - Whalley, Heather C.

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