Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging
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Event-related functional magnetic resonance imaging was used to measure blood oxygenation level-dependent responses in 13 young healthy human volunteers during performance of a probabilistic reversal-learning task. The task allowed the separate investigation of the relearning of stimulus-reward associations and the reception of negative feedback. Significant signal change in the right ventrolateral prefrontal cortex was demonstrated on trials when subjects stopped responding to the previously relevant stimulus and shifted responding to the newly relevant stimulus. Significant signal change in the region of the ventral striatum was also observed on such reversal errors, from a region of interest analysis. The ventrolateral prefrontal cortex and ventral striatum were not significantly activated by the other, preceding reversal errors, or when subjects received negative feedback for correct responses. Moreover, the response on the final reversal error, before shifting, was not modulated by the number of preceding reversal errors, indicating that error-related activity does not simply accumulate in this network. The signal change in this ventral frontostriatal circuit is therefore associated with reversal learning and is uncontaminated by negative feedback. Overall, these data concur with findings in rodents and nonhuman primates of reversal-learning deficits after damage to ventral frontostriatal circuitry, and also support recent clinical findings using this task.
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The common deficits produced on probabilistic learning and ED-shifting here suggest effects of the drug on neural circuits including the right ventro-lateral PFC (BA47).
“However, the common deficits produced on probabilistic learning and ED-shifting here suggest effects of the drug on neural circuits including the right ventro-lateral PFC (BA47), as both of these tasks are associated with activations of this region [44].”
From Dissociable effects of acute SSRI (escitalopram) on executive, learning and emotional functions in healthy humans (2018) · cites this paper as [44]
The Imaging data section reports right ventrolateral PFC activation during probabilistic reversal learning. The Discussion reports a similar ventrolateral PFC activation during attentional set shifting in Monchi et al., but notes that the shifting effect could not be separated from negative feedback; our copy does not identify the region as BA47. The drug deficits described as occurring “here” are the citing authors’ findings, not findings of this imaging study. (LLM, conf=0.83)
Experimental — accuracy not yet measuredThe right lateral prefrontal cortex, and more specifically the right vlPFC, is recruited during hypothesis evaluation; activity in the right vlPFC is associated with effortful inhibition, detecting and resolving conflicts between beliefs and logic, and rejecting inappropriate hypotheses in accordance with new evidence.
“Several studies indicate that the right lateral prefrontal cortex, and more specifically the right vlPFC, is recruited during hypothesis evaluation.”
From Divergent hemispheric reasoning strategies: reducing uncertainty versus resolving inconsistency (2014) · cites this paper as Cools et al., 2002
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredCools et al. (2002) showed that the right vlPFC is active during the last trial before a hypothesis switch in the Wisconsin Card Sorting Test (WCST) and this activity is independent of the receipt of negative feedback.
“Cools et al. (2002) showed that the right vlPFC is active during the last trial before a hypothesis switch in the Wisconsin Card Sorting Test (WCST) and this activity is independent of the receipt of negative feedback”
From Divergent hemispheric reasoning strategies: reducing uncertainty versus resolving inconsistency (2014) · cites this paper as Cools et al. (2002)
The Discussion reports right ventrolateral PFC activity at the final reversal error and says the effect was uncontaminated by negative feedback. But the Experimental design describes a probabilistic reversal-learning task using two visual patterns, not the Wisconsin Card Sorting Test; the WCST attribution is unsupported. (LLM, conf=0.90)
Experimental — accuracy not yet measuredBrain regions subserving reversal learning, such as the ventromedial prefrontal cortex, appear to be particularly implicated in severe hoarding.
“brain regions subserving reversal learning, such as the ventromedial prefrontal cortex (Cools et al., 2002; Fellows and Farah, 2003) appear to be particularly implicated in severe hoarding (Mataix-Cols et al., 2011)”
From The profile of executive function in OCD hoarders and hoarding disorder (2014) · cites this paper as Cools et al., 2002
The striatum, amygdala, and hippocampus are important for reversal learning.
“Other brain regions important for reversal learning are the striatum (Cools et al 2002, Rogers et al 2000), amygdala (Izquierdo et al 2013, Schoenbaum et al 2003, Wassum & Izquierdo 2015) and the hippocampus (Mala et al 2015).”
From Prefrontal cortex executive processes affected by stress in health and disease (2018) · cites this paper as Cools et al 2002
Studies using repeated/serial reversals find that the vlPFC is involved in both human fMRI and animal lesion studies.
“However, studies using repeated/serial reversals, which foster the development and application of rules, find that the vlPFC is involved in both human fMRI (Cools et al., 2002; Remijnse et al., 2005; Mitchell et al., 2008; Hampshire et al., 2012) and animal lesion studies (Rygula et al., 2010; Rudebeck et al., 2013).”
From Explicit and implicit emotion regulation: a multi-level framework (2017) · cites this paper as Cools et al., 2002
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“However, studies using repeated/serial reversals, which foster the development and application of rules, find that the vlPFC is involved in both human fMRI (Cools et al., 2002; Remijnse et al., 2005; Mitchell et al., 2008; Hampshire et al., 2012) and animal le-”
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- Authors
- Cools, R., Clark, L., Owen, A. M., & Robbins, T. W.
- Affiliations
- University of Cambridge (GB)
- MRC Cognition and Brain Sciences Unit (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-06-01
- Volume
- 22
- Issue
- 11
- Pages
- 4563-4567
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6758810
- OpenAlex
- W2114022439
- Cited by
- 784
- References
- 35
- Citations by year
- 2026: 19 · 2025: 25 · 2024: 32 · 2023: 22 · 2022: 25 · 2021: 34 · 2020: 26 · 2019: 28 · 2018: 29 · 2017: 33 · 2016: 46 · 2015: 35 · 2014: 36 · 2013: 36 · 2012: 33
- FWCI
- 13.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Parkinson's UK
- Medical Research Council
- 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
- probabilistic reversal learning, ventrolateral prefrontal cortex, ventral striatum, negative feedback, stimulus-reward associations, reversal errors, cognitive flexibility, BOLD signal
- MeSH terms
- Adult, Behavior, Brain, Brain Mapping, Corpus Striatum, Female, Humans, Magnetic Resonance Imaging, Male, Neural Inhibition, Neurons, Probability Learning, Reversal Learning, Reward, Prefrontal Cortex, Feedback, Psychological
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