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Cited by 462Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Direct Activation of the Ventral Striatum in Anticipation of Aversive Stimuli

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Jensen, Jimmy, McIntosh, Anthony R, Crawley, Adrian P, Mikulis, David J, Remington, Gary, Kapur, Shitij·2003·Neuron
DOI 10.1016/s0896-6273(03)00724-4
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Abstract

The brain "reward" system, centered on the limbic ventral striatum, plays a critical role in the response to pleasure and pain. The ventral striatum is activated in animal and human studies during anticipation of appetitive/pleasurable events, but its role in aversive/painful events is less clear. Here we present data from three human fMRI studies based on aversive conditioning using unpleasant cutaneous electrical stimulation and show that the ventral striatum is reliably activated. This activation is observed during anticipation and is not a consequence of relief after the aversive event. Further, the ventral striatum is activated in anticipation regardless of whether there is an opportunity to avoid the aversive stimulus or not. Our data suggest that the ventral striatum, a crucial element of the brain "reward" system, is directly activated in anticipation of aversive stimuli.

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  • Previous fMRI studies have implicated the striatum in avoidance of shock, pain, or aversive images or sounds.

    “Previous fMRI studies have implicated the striatum in avoidance of shock, pain, or aversive images or sounds (Jensen et al., 2003; Delgado et al., 2009; Levita et al., 2012; Seymour et al., 2012; Bolstad et al., 2013; Collins et al., 2014; Eldar et al., 2016; Schlund et al., 2016).”

    From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Jensen et al., 2003

  • Several studies observed striatal activation during cue presentation, but they compared the BOLD responses within subjects during a threatening cue associated with an avoidance response and a nonthreatening cue in a single cohort of subjects.

    “Several studies observed striatal activation during cue presentation, but they compared the BOLD responses withinsubjects during a threatening cue associated with an avoidance response and a nonthreatening cue in a single cohort of subjects (Jensen et al., 2003; Levita et al., 2012; Bolstad et al., 2013; Collins et al., 2014).”

    From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Jensen et al., 2003

  • The neuroimaging literature is profoundly inconsistent on the role of the striatum in aversive learning, with some studies reporting increased VS activity in aversive contexts and others reporting decreased activity.

    “the neuroimaging literature is profoundly inconsistent on this point, with some studies reporting increased VS activity in aversive contexts (Figure 2c) [62–64] and others reporting decreasing activity in this area during the prediction, learning, and receipt of aversive outcomes [65,66].”

    From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [63]

  • The ventral striatum plays a role in affective reactivity.

    “The VS plays a role in affective reactivity (Knutson, Westdorp, Kaiser, & Hommer, 2000; Sescousse, Caldu, Segura, & Dreher, 2013; Jensen et al., 2003; Levita et al., 2009)”

    From Feeling left out or just surprised? Neural correlates of social exclusion and overinclusion in adolescence (2020) · cites this paper as Jensen et al., 2003

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Authors
Jensen, J., McIntosh, A. R., Crawley, A. P., Mikulis, D. J., Remington, G., & Kapur, S.
Affiliations
  • Centre for Addiction and Mental Health (CA)
  • University of Toronto (CA)
Corresponding author
Kapur, Shitij
ORCID
Venue
Neuron
Publisher
Elsevier BV
Published
2003-12
Volume
40
Issue
6
Pages
1251-1257
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/s0896-6273(03)00724-4
OpenAlex
W1982327643
Cited by
455
References
53
Citations by year
2026: 6 · 2025: 10 · 2024: 5 · 2023: 41 · 2022: 8 · 2021: 14 · 2020: 14 · 2019: 13 · 2018: 21 · 2017: 15 · 2016: 19 · 2015: 27 · 2014: 32 · 2013: 25 · 2012: 34
FWCI
6.91
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Research Portal (King's College London) (submittedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
ventral striatum, aversive stimuli, anticipation, aversive conditioning, cutaneous electrical stimulation, reward systems, pain, avoidance, limbic system
MeSH terms
Adult, Avoidance Learning, Basal Ganglia, Electric Stimulation, Female, Humans, Magnetic Resonance Imaging, Male, Pain Measurement, Reward

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