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

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Romaniuk, Liana, Sandu, Anca-Larisa, Waiter, Gordon D., McNeil, Christopher J., Xueyi, Shen, Harris, Matthew A., Macfarlane, Jennifer A., Lawrie, Stephen M. +6 more·2019·Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

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: < .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.

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Crossref · 10.1016/j.bpsc.2018.09.015

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  • In healthy controls, personally chosen vs. passively received rewards elicit stronger activation in the striatum (ventral and dorsal) and PFC (inferior frontal gyrus), which is inversely related to depressive symptoms.

    “studies in healthy controls have shown that personally chosen vs. passively received rewards elicit stronger activation in the striatum (ventral and dorsal) and PFC (inferior frontal gyrus) [212-215], which is inversely related to depressive symptoms [212].”

    From Prefrontal cortex and depression (2022) · cites this paper as [212]

    The Discussion sections “Personally Earned Versus Passively Received Rewards” and “Anticipating Choice” distinguish two findings: personally chosen outcomes enhanced inferior frontal gyrus activation, while ventral striatal activation occurred during anticipation of choice and was lower in participants with more depressive symptoms. The paper does not establish stronger ventral and dorsal striatal responses to personally chosen versus passively received rewards, or link that outcome contrast to depressive symptoms. (LLM, conf=0.88)

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  1. [19]First M.B. Spitzer R.L. Gibbon M. Williams J.B.W. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P) 2002 Biometrics Research, New York State Psychiatric Institute New York

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Authors
Romaniuk, L., Sandu, 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., Delgado, M. R., Steele, J. D., McIntosh, A. M., & Whalley, H. C.
Affiliations
  • University of Edinburgh (GB)
  • University of Aberdeen (GB)
  • University of Dundee (GB)
  • Rutgers, The State University of New Jersey (US)
Corresponding author
Romaniuk, Liana
Venue
Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Publisher
Elsevier BV
Published
2019-02
Volume
4
Issue
2
Pages
190-199
ISSN
2451-9022 (ISSN-L)
OpenAlex
W2893097056
Cited by
26
References
51
Citations by year
2026: 1 · 2025: 4 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 6 · 2020: 6 · 2019: 2
FWCI
2.08
Type
journal article
Language
en
Open access
Locations
  • Biological Psychiatry Cognitive Neuroscience and Neuroimaging (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Discovery Research Portal (University of Dundee) (publishedVersion, cc-by)
  • Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
Funders
  • China Scholarship Council (201506040037)
  • Scottish Funding Council
  • Medical Research Council
  • Lister Institute of Preventive Medicine
  • Wellcome Trust (104036/Z/14/Z)
  • National Institutes of Health (DA027764)
  • Royal College of Physicians of Edinburgh
  • Biotechnology and Biological Sciences Research Council (MR/K026992/1)
  • University of Edinburgh
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Decision Sciences › General Decision Sciences › Decision-Making and Behavioral Economics
Keywords
personal control, choice value, reward learning, reinforcement learning, prediction error, subthreshold depression, mood, motivational orientation, ventral striatum, nucleus accumbens, insula, self-control
MeSH terms
Affect, Brain, Brain Mapping, Choice Behavior, Conditioning, Classical, Female, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Reward

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