Orbitofrontal inactivation impairs reversal of Pavlovian learning by interfering with ‘disinhibition’ of responding for previously unrewarded cues
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Orbitofrontal cortex (OFC) is critical for reversal learning. Reversal deficits are typically demonstrated in complex settings that combine Pavlovian and instrumental learning. Yet recent work has implicated the OFC specifically in behaviors guided by cues and the features of the specific outcomes they predict. To test whether the OFC is important for reversing such Pavlovian associations in the absence of confounding instrumental requirements, we trained rats on a simple Pavlovian task in which two auditory cues were presented, one paired with a food pellet reward and the other presented without reward. After learning, we reversed the cue–outcome associations. For half the rats, OFC was inactivated prior to each reversal session. Inactivation of OFC impaired the ability of the rats to reverse conditioned responding. This deficit reflected the inability of inactivated rats to develop normal responding for the previously unrewarded cue; inactivation of OFC had no impact on the ability of the rats to inhibit responding to the previously rewarded cue. These data show that OFC is critical to reversal of Pavlovian responding, and that the role of OFC in this behavior cannot be explained as a simple deficit in response inhibition. Furthermore, the contrast between the normal inhibition of responding, reported here, and impaired inhibition of responding during Pavlovian over‐expectation, reported previously, suggests the novel hypothesis that OFC may be particularly critical for learning (or behavior) when it requires the subject to generate predictions about outcomes by bringing together or integrating disparate pieces of associative information.
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This is consistent with intact acquisition of Pavlovian responses but impaired reversal learning in OFC-lesioned animals.
“This is consistent with the reported intact acquisition of Pavlovian responses, but impaired reversal learning in OFC‐lesioned animals.”
From Behavioral flexibility in a mouse model for obsessive‐compulsive disorder: Impaired Pavlovian reversal learning in SAPAP3 mutants (2019) · cites this paper as [65]
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Tian, S., Huang, F., Gao, J., Li, P., Ouyang, X., Zhou, S., Deng, H., & Yan, Y. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.05.002 · Cited by 13 · see citing works
Mechanisms of higher-order learning in the amygdala
Gostolupce, D., Iordanova, M. D., & Lay, B. P. P. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113435 · Cited by 12 · see citing works
Sequential reversal learning: a new touchscreen schedule for assessing cognitive flexibility in mice
Odland, A. U., Sandahl, R., & Andreasen, J. T. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05687-6 · Cited by 12 · see citing works
Hervig, M. E.-S., Piilgaard, L., Božič, T., Alsiö, J., & Robbins, T. W. (2020) · Psychology & Neuroscience · doi:10.1037/pne0000221 · Cited by 11 · see citing works
Brown, A., & Chaudhri, N. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15862 · Cited by 9 · see citing works
Spatiotemporal Pavlovian head-fixed reversal learning task for mice
Yamamoto, K., Yamada, K., Yatagai, S., Ujihara, Y., & Toda, K. (2022) · Molecular Brain · doi:10.1186/s13041-022-00952-5 · Cited by 8 · see citing works
Hatakama, H., Asaoka, N., Nagayasu, K., Shirakawa, H., & Kaneko, S. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108926 · Cited by 8 · see citing works
Secondary motor cortex tracks decision value during the learning of a non-instructed task
Augusto, E., Kouskoff, V., Chenouard, N., Giraudet, M., Peltier, L., de Miranda, A., Louis, A., Alonso, L., & Gambino, F. (2025) · Cell Reports · doi:10.1016/j.celrep.2024.115152 · Cited by 7 · see citing works
Domain-Specific Cognitive Impairment Reflects Prefrontal Dysfunction in Aged Common Marmosets
Vanderlip, C. R., Asch, P. A., Reynolds, J. H., & Glavis‐Bloom, C. (2023) · eNeuro · doi:10.1523/eneuro.0187-23.2023 · Cited by 7 · see citing works
Allen, C. P., & Leri, F. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.12.025 · Cited by 7 · see citing works
Panayi, M. C., & Killcross, S. (2021) · Cerebral Cortex Communications · doi:10.1093/texcom/tgab010 · Cited by 7 · see citing works
Hasantash, M., Li, Y., Torres-Herraez, A., Kellendonk, C., & Anacker, C. (2025) · Science Advances · doi:10.1126/sciadv.adx7514 · Cited by 5 · see citing works
Dong, X., Zhornitsky, S., Wang, W., Le, T. M., Chen, Y., Chaudhary, S., Li, C.-S. R., & Zhang, S. (2022) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyac019 · Cited by 5 · see citing works
Neural correlates of recall and extinction in a rat model of appetitive Pavlovian conditioning.
Brown, A., Villaruel, F. R., & Chaudhri, N. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114248 · Cited by 2 · see citing works
Role Played by the Passage of Time in Reversal Learning
Goarin, E. H. F., Lingawi, N. W., & Laurent, V. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00075 · Cited by 4 · see citing works
Mueller, L. E., Konya, C., Sharpe, M. J., Wikenheiser, A. M., & Schoenbaum, G. M. (2024) · Current Biology · doi:10.1016/j.cub.2024.09.064 · Cited by 3 · see citing works
Self-citationThe Role of the Orbitofrontal Cortex in the Regulation of Fear Coping Strategies
Kuan, H.-Y., & Chang, C. (2024) · Journal of physiological investigation. · doi:10.4103/ejpi.ejpi-d-24-00072 · Cited by 3 · see citing works
Pochapski, J. A., Gómez‐A, A., Stringfield, S. J., Jaggers, H., Boettiger, C. A., Cunha, C. D., & Robinson, D. L. (2024) · Scientific Reports · doi:10.1038/s41598-024-64036-1 · Cited by 1 · see citing works
Lay, B. P. P., Choudhury, R., Esber, G. R., & Iordanova, M. D. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06198-2 · Cited by 1 · see citing works
Serotonergic modulation of cognition
Skandali, N. (2017) · Apollo (University of Cambridge) · doi:10.17863/cam.25255
Faculty Opinions recommendation of The neural basis of reversal learning: An updated perspective.
Hayden, B. Y. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.726221441.793565477
Cortex préfrontal et flexibilité comportementale : implication de la noradrénaline
Cerpa, J.-C. (2019) · theses.fr (ABES) · doi:10.70675/d4f665b9z3943z4c88z9b4bzbf11cd7cf8d1
DeCross, S. N., Kribakaran, S., Odriozola, P., Sheridan, M. A., Tottenham, N., Gee, D. G., & McLaughlin, K. A. (2026) · Journal of Affective Disorders · doi:10.1016/j.jad.2026.122012
- Authors
- Burke, K. A., Takahashi, Y. K., Correll, J., Leon Brown, P., & Schoenbaum, G.
- Affiliations
- University of Maryland, Baltimore (US)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2009-11
- Volume
- 30
- Issue
- 10
- Pages
- 1941-1946
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC2810348
- OpenAlex
- W2033316793
- Cited by
- 76
- References
- 51
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 6 · 2023: 2 · 2022: 8 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 2 · 2017: 2 · 2016: 4 · 2015: 8 · 2014: 7 · 2013: 5 · 2012: 4
- FWCI
- 2.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (R01AG027097)
- National Institute of Mental Health (R01MH080865)
- National Institute on Drug Abuse (R01DA015718, F31DA021989)
- 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
- orbitofrontal cortex, reversal learning, classical conditioning, response inhibition, disinhibition, cue-outcome associations, rats
- MeSH terms
- Animals, Baclofen, Conditioning, Classical, Drug Combinations, Inhibition, Psychological, Learning Disabilities, Muscimol, Reward, Prefrontal Cortex, GABA Agonists, Rats, Long-Evans, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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