Amygdala and Orbitofrontal Cortex Lesions Differentially Influence Choices during Object Reversal Learning
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In nonhuman primates, interaction between the orbitofrontal cortex (OFC) and the amygdala (AMG) has been seen as critical for learning and subsequently changing associations between stimuli and reinforcement. However, it is still unclear what the precise role of the OFC is in altering these stimulus–reward associations, and recent research has questioned whether the AMG makes an essential contribution at all. To gain a better understanding of the role of these two structures in flexibly associating stimuli with reinforcement, we reanalyzed a set of previously published data from groups of monkeys with either OFC or AMG lesions that had been tested on an object reversal learning task. Based on trial-by-trial analyses of rewarded and unrewarded choices, we report two new findings. First, monkeys with OFC lesions were, compared with both control and AMG groups, unable to use correctly performed trials to optimally guide subsequent choices. Second, monkeys with AMG lesions showed the opposite pattern of behavior. This group benefited more than controls from correctly performed trials that followed an error. Finally, as has been reported by others, after a change in reward contingencies, monkeys with OFC lesions also showed a slightly greater tendency to choose the previously rewarded object. These findings demonstrate that the OFC and AMG make different contributions to object reversal learning not highlighted previously.
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Lesions of the orbital cortex produce a deficit in using reward as a guide to behavior.
“In addition, lesions of the orbital cortex produce a deficit in the ability to use reward as a guide to behavior (Rudebeck and Murray, 2008)”
From Neurocircuitry of Mood Disorders (2010) · cites this paper as Rudebeck and Murray, 2008
The Discussion reports that monkeys with orbitofrontal cortex lesions were impaired at using reward information to guide subsequent choices. The claim omits an important limit: this deficit was observed after a reversal, while initial discrimination learning was unaffected. (LLM, conf=0.88)
Experimental — accuracy not yet measuredPFo lesions cause an inefficiency in using positive feedback.
“This analysis shows that PFo lesions cause an inefficiency in using positive feedback (blue asterisks in Fig. 4B).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
Trial-by-trial analysis indicates both PFo and amygdala lesions influence the use of positive feedback, in opposite directions.
“A more detailed, trial-by-trial analysis indicates that both PFo and amygdala lesions influence the use of positive feedback. As Figure 4B shows, however, they do so in opposite directions.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
PFo lesions cause a deficit in using positive feedback, but not in the use of negative feedback.
“These findings indicate that PFo lesions cause a deficit in using positive feedback, but not in the use of negative feedback (91, but cf. 94).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
Selective bilateral amygdala lesions cause an improvement in using positive feedback to make future choices.
“In contrast to the deficits seen after PFo lesions, selective bilateral amygdala lesions cause an improvement in using positive feedback to make future choices (red asterisk in Fig. 4B).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
Even when two, three, or four correct rewarded responses intervene between an error and an upcoming choice, monkeys with PFo lesions make many more errors than intact controls.
“Even when two, three, or four correct (and rewarded) responses intervene between an error and an upcoming choice, monkeys with PFo lesions make many more errors than do intact control monkeys.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
After one correct rewarded trial following an error, monkeys with amygdala lesions outperform intact monkeys in future choices.
“After performing one correct (rewarded) trial following an error (the EC+1 trial type), monkeys with amygdala lesions out-perform intact monkeys in their future choices.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
Bilateral PFo lesions significantly slow reversal learning.
“Bilateral lesions of PFo (Figure 4A, blue), however, significantly slow reversal learning (91, 92), a finding that has been replicated many times (93).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
The PFo lesion group was inefficient in using positive feedback after rule changes, suggesting PFo plays an important role in valuation of rule representations as well as object representations.
“Like the monkeys studied by Rudebeck and Murray (91), the PFo lesion group studied by Buckley et al. was inefficient in using positive feedback after rule changes, suggesting that PFo plays an important role in the valuation of rule representations as well as object representations.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
Selective bilateral amygdala lesions have no effect on learning object-reward reversals.
“The red curve in Figure 4A illustrates that selective bilateral amygdala lesions have no effect on learning these object-reward reversals (75, 91).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
Updating of object-outcome and rule-outcome mappings needs to occur to make good choices in serial object-reversal and to optimize reward probability.
“This updating needs to occur in order to make good choices in the serial object-reversal task (91) and when making object choices that optimize the probability of reward (90).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [91]
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- Authors
- Rudebeck, P. H., & Murray, E. A.
- Affiliations
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2008-08-13
- Volume
- 28
- Issue
- 33
- Pages
- 8338-8343
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2556079
- OpenAlex
- W2046214338
- Cited by
- 148
- References
- 27
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 6 · 2023: 4 · 2022: 11 · 2021: 6 · 2020: 7 · 2019: 11 · 2018: 10 · 2017: 4 · 2016: 10 · 2015: 10 · 2014: 10 · 2013: 9 · 2012: 10
- FWCI
- 5.17
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Soochow University
- National Institutes of Health (Z99 MH999999)
- National Institute of Mental Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- amygdala, orbitofrontal cortex, lesion studies, non-human primates, stimulus-reward associations, error-based learning, reward contingency, choice behavior, neural basis of learning
- MeSH terms
- Amygdala, Animals, Choice Behavior, Frontal Lobe, Macaca mulatta, Male, Photic Stimulation, Reversal Learning, Prefrontal Cortex
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