A non-reward attractor theory of depression
Abstract
A non-reward attractor theory of depression is proposed based on the operation of the lateral orbitofrontal cortex and supracallosal cingulate cortex. The orbitofrontal cortex contains error neurons that respond to non-reward for many seconds in an attractor state that maintains a memory of the non-reward. The human lateral orbitofrontal cortex is activated by non-reward during reward reversal, and by a signal to stop a response that is now incorrect. Damage to the human orbitofrontal cortex impairs reward reversal learning. Not receiving reward can produce depression. The theory proposed is that in depression, this lateral orbitofrontal cortex non-reward system is more easily triggered, and maintains its attractor-related firing for longer. This triggers negative cognitive states, which in turn have positive feedback top-down effects on the orbitofrontal cortex non-reward system. Treatments for depression, including ketamine, may act in part by quashing this attractor. The mania of bipolar disorder is hypothesized to be associated with oversensitivity and overactivity in the reciprocally related reward system in the medial orbitofrontal cortex and pregenual cingulate cortex.
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Reversal learning depends on an intact orbitofrontal cortex to inhibit the previously learned response.
“Such reversal is known to depend on an intact orbitofrontal cortex to inhibit the prior learned response (Placek et al., 2013; Rolls, 2016).”
From The effects of early life stress on reward processing (2018) · cites this paper as Rolls, 2016
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Rolls, E. T., & Deco, G. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.001 · Cited by 65 · see citing works
Self-citationBeyond depression: Toward a process‐based approach to research, diagnosis, and treatment.
Forgeard, M. J. C., Haigh, E. A. P., Beck, A. T., Davidson, R. J., Henn, F. A., Maier, S. F., Mayberg, H. S., & Seligman, M. E. P. (2011) · Clinical Psychology Science and Practice · doi:10.1111/j.1468-2850.2011.01259.x · Cited by 63 · see citing works
Fabian Grabenhorst, B., & Rolls, E. T. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00352.2010 · Cited by 62 · see citing works
Self-citationSwann, A. C. (2009) · Current Psychiatry Reports · doi:10.1007/s11920-009-0073-2 · Cited by 62 · see citing works
Neuronal coding of implicit emotion categories in the subcallosal cortex in patients with depression
Laxton, A. W., Neimat, J. S., Davis, K. D., Womelsdorf, T., Hutchison, W. D., Dostrovsky, J. O., Hamani, C., Mayberg, H. S., & Lozano, A. M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.029 · Cited by 62 · see citing works
Luo, Q., Ge, T., Fabian Grabenhorst, B., Feng, J., & Rolls, E. T. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003265 · Cited by 60 · see citing works
Self-citationGe, T., Feng, J., Fabian Grabenhorst, B., & Rolls, E. T. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.08.047 · Cited by 58 · see citing works
Self-citationDeng, W., Rolls, E. T., Ji, X., Robbins, T. W., Banaschewski, T., Bokde, A. L. W., Bromberg, U., Buechel, C., Desrivières, S., Conrod, P., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23607 · Cited by 57 · see citing works
Self-citationRolls, E. T. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.06.017 · Cited by 39 · see citing works
Self-citationEvolution of the Emotional Brain
Rolls, E. T. (2017) · Springer eBooks · doi:10.1007/978-4-431-56559-8_12 · Cited by 35 · see citing works
Self-citationEvolution of the Brain, Cognition, and Emotion in Vertebrates
Watanabe, S., Hofman, M., & Shimizu, T. (2017) · Brain Science · doi:10.1007/978-4-431-56559-8 · Cited by 34 · see citing works
Stochastic cortical neurodynamics underlying the memory and cognitive changes in aging
Rolls, E. T., & Deco, G. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.12.003 · Cited by 33 · see citing works
Self-citationNon-reward neural mechanisms in the orbitofrontal cortex
Rolls, E. T., & Deco, G. (2016) · Cortex · doi:10.1016/j.cortex.2016.06.023 · Cited by 25 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Passingham, R.E.P., Wise, S.P., 2012. The Neurobiology of the Prefrontal Cortex. Oxford University Press, Oxford.
Cited by
Sorted by citations
The cingulate cortex and limbic systems for emotion, action, and memory
Rolls, E. T. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01945-2 · Cited by 859 · see citing works
Self-citationThe orbitofrontal cortex: reward, emotion and depression
Rolls, E. T., Cheng, W., & Feng, J. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa196 · Cited by 474 · see citing works
Self-citationMcTeague, L. M., Rosenberg, B. M., Lopez, J. W., Carreon, D. M., Huemer, J., Jiang, Y., Chick, C. F., Eickhoff, S. B., & Etkin, A. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.18111271 · Cited by 388 · see citing works
Cheng, W., Rolls, E. T., Qiu, J., Liu, W., Tang, Y., Huang, C.-C., Wang, X., Zhang, J., Lin, W., Zheng, L., et al. (2016) · Brain · doi:10.1093/brain/aww255 · Cited by 294 · see citing works
Self-citationFettes, P., Schulze, L., & Downar, J. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00025 · Cited by 299 · see citing works
Cheng, W., Rolls, E. T., Ruan, H., & Feng, J. (2018) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2018.1941 · Cited by 291 · see citing works
The effects of early life stress on reward processing
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.002 · Cited by 192 · see citing works
Feffer, K., Fettes, P., Giacobbe, P., Daskalakis, Z. J., Blumberger, D. M., & Downar, J. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2017.11.011 · Cited by 116 · see citing works
Connections of the human orbitofrontal cortex and inferior frontal gyrus
Heather Hsu, C.-C., Rolls, E. T., Huang, C.-C., Chong, S. T., Zac Lo, C.-Y., Feng, J., & Lin, C.-P. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa160 · Cited by 67 · see citing works
Self-citationRolls, E. T. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.013 · Cited by 62 · see citing works
Deng, W., Rolls, E. T., Ji, X., Robbins, T. W., Banaschewski, T., Bokde, A. L. W., Bromberg, U., Buechel, C., Desrivières, S., Conrod, P., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23607 · Cited by 57 · see citing works
Self-citationKuniishi, H., Yamada, D., Wada, K., Yamada, M., & Sekiguchi, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0837-3 · Cited by 47 · see citing works
Fettes, P., Peters, S., Giacobbe, P., Blumberger, D. M., & Downar, J. (2017) · Brain Stimulation · doi:10.1016/j.brs.2016.11.008 · Cited by 31 · see citing works
Orbitofrontal cortex: a ‘non-rewarding’ new treatment target in depression?
Downar, J. (2019) · Current Biology · doi:10.1016/j.cub.2018.11.057 · Cited by 31 · see citing works
Nunes, A., Pavlova, B., Cunningham, J. E. A., Nuñez, J.-J., Quilty, L. C., Foster, J. A., Harkness, K. L., Ho, K., Lam, R. W., Li, Q. S., et al. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.06.023 · Cited by 5 · see citing works
- Authors
- Rolls, E. T.
- Affiliations
- University of Warwick (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2016-09
- Volume
- 68
- Pages
- 47-58
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2371895244
- Cited by
- 180
- References
- 118
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 22 · 2023: 13 · 2022: 24 · 2021: 15 · 2020: 21 · 2019: 21 · 2018: 17 · 2017: 15 · 2016: 7 · 2015: 1
- FWCI
- 2.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- Funders
- 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
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- depression, lateral orbitofrontal cortex, ketamine, mania, bipolar disorder, medial orbitofrontal cortex, top-down feedback
- MeSH terms
- Depression, Gyrus Cinguli, Humans, Reward, Prefrontal Cortex
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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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