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Distinct opioid circuits determine the palatability and the desirability of rewarding events
Open accessAbstract
It generally is assumed that a common neural substrate mediates both the palatability and the reward value of nutritive events. However, recent evidence suggests this assumption may not be true. Whereas opioid circuitry in both the nucleus accumbens and ventral pallidum has been reported to mediate taste-reactivity responses to palatable events, the assignment of reward or inventive value to goal-directed actions has been found to involve the basolateral amygdala. Here we found that, in rats, the neural processes mediating palatability and incentive value are indeed dissociable. Naloxone infused into either the ventral pallidum or nucleus accumbens shell blocked the increase in sucrose palatability induced by an increase in food deprivation without affecting the performance of sucrose-related actions. Conversely, naloxone infused into the basolateral amygdala blocked food deprivation-induced changes in sucrose-related actions without affecting sucrose palatability. This double dissociation of opioid-mediated changes in palatability and incentive value suggests that the role of endogenous opioids in reward processing does not depend on a single neural circuit. Rather, changes in palatability and in the incentive value assigned to rewarding events seem to be mediated by distinct neural processes.
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“For practical reasons, this research has focused on the amygdala’s role in signaling decreases in food value, but it probably signals increases in value, as well (84).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [84]
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“Instead, such responses are altered by blockage or stimulation of Nacc opioid receptors [44,49]”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [49]
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“suggesting that dissociable neurobiological substrates in the VS mediate motivational and hedonic processes.”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [49]
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Citations
Cites
Bayesian t tests for accepting and rejecting the null hypothesis
Rouder, J. N., Speckman, P. L., Sun, D., Morey, R. D., & Iverson, G. (2009) · Psychonomic Bulletin & Review · doi:10.3758/pbr.16.2.225 · Cited by 3,688
The somatic marker hypothesis and the possible functions of the prefrontal cortex
Damasio, A. R. (1996) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1996.0125 · Cited by 2,847 · cited 4×
“Pharmacol Biochem Behav 46(3):745–749.”
BackgroundResultInfluentialEmotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex
Cardinal, R. N., Parkinson, J. A., Hall, J., & Everitt, B. J. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00007-6 · Cited by 2,129
Food reward: brain substrates of wanting and liking
Berridge, K. C. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00033-b · Cited by 1,901
Goal-directed instrumental action: contingency and incentive learning and their cortical substrates
Balleine, B. W., & Dickinson, A. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00033-1 · Cited by 1,541
Self-citationAffective consciousness: core emotional feelings in animals and humans.
Panksepp, J. (2005) · Consciousness and Cognition · doi:10.1016/j.concog.2004.10.004 · Cited by 1,217
Motivational control of goal-directed action
Dickinson, A., & Balleine, B. (1994) · Animal Learning & Behavior · doi:10.3758/bf03199951 · Cited by 995
Self-citationKelley, A. E. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.11.015 · Cited by 942
Reward, Motivation, and Reinforcement Learning
Dayan, P., & Balleine, B. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00963-7 · Cited by 855
Self-citationPeciña, S., & Berridge, K. C. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2329-05.2005 · Cited by 671
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Zamyad, M., Abbasnejad, M., Esmaeili‐Mahani, S., Sheibani, V., & Raoof, M. (2020) · Experimental Brain Research · doi:10.1007/s00221-020-05961-1 · Cited by 6
Chometton, S., Guèvremont, G., Seigneur, J., Timofeeva, E., & Timofeev, I. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02161-z · Cited by 6
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Thiriet, M. (2012) · Biomathematical and biomechanical modeling of the circulatory and ventilatory systems · doi:10.1007/978-1-4614-4370-4_12 · Cited by 1
Абрамец, И. И., Кузнецов, Ю. В., Евдокимов, Д. В., & Зайка, Т. О. (2019) · Университетская клиника · doi:10.26435/uc.v0i2(31).303 · Cited by 1
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Balleine, B. W. (2021) · Nature Human Behaviour · doi:10.1038/s41562-021-01208-3 · Cited by 1
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Butlin, P. (2016) · Research Portal (King's College London) · Cited by 1
Schlingloff, D., Szabó, Í., Gulyas, E., Király, B., Kispal, R., Stephenson‐Jones, M., & Hangya, B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.23.639747 · Cited by 1
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Exton-McGuinness, M. T. J. (2014) · University of Birmingham Institutional Research Archive (University of Birmingham) · Cited by 1
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Thiriet, M. (2012) · Biomathematical and biomechanical modeling of the circulatory and ventilatory systems · doi:10.1007/978-1-4614-4370-4_3
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Inui, T., Shimura, T., Yoshioka, Y., Inui‐Yamamoto, C., & Ohzawa, I. (2014) · World Automation Congress (WAC) · doi:10.1109/wac.2014.6935794
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Yager, L. M. (2014) · Deep Blue (University of Michigan)
Simón, M. J., Zafra, M. A., & Puerto, A. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881119855982
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Geiger, B. M., Irene, M., & Pothos, E. N. (2020) · Neuromethods · doi:10.1007/978-1-0716-1146-3_2
Berridge, K. C. (2014) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.718235070.793489919
Thiriet, M. (2012) · Biomathematical and biomechanical modeling of the circulatory and ventilatory systems · doi:10.1007/978-1-4614-4370-4_11
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van Steenbergen, H., Eikemo, M., & Leknes, S. (2018) · doi:10.31234/osf.io/ws9dr
Palmer, D. B., Cayton, C. A., Scott, A., Lin, I., Newell, B., Weberg, M., & Richard, J. M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.22.541796
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/9780520412996-005
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.f
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.h
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.j
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.a
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/9780520412996-003
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.g
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Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.e
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.c
Simmons, D. (2025) · University of California Press eBooks · doi:10.1525/luminos.232.i
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Schlingloff, D., Szabó, Í., Gulyas, E., Király, B., Kispal, R., Stephenson‐Jones, M., & Hangya, B. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0415-25.2026 · Cited by 2
Mu opioid receptors in the habenula : dissecting reward and aversion in addiction
Boulos, L. (2017) · theses.fr (ABES) · doi:10.70675/4ec6ce3az48cbz4a77za34ezb8b76b41f629 · Cited by 1
Cortex préfrontal et flexibilité comportementale : implication de la noradrénaline
Cerpa, J.-C. (2019) · theses.fr (ABES) · doi:10.70675/d4f665b9z3943z4c88z9b4bzbf11cd7cf8d1
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Ramírez-Armenta, K., Feng, C., Martinez, A., Andrade, J. E., Quach, J., Paredes, N., Sias, A. C., Griffin, N. K., Sharpe, M. J., & Wassum, K. M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.21.733629
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Metadata
- Authors
- Wassum, K. M., Ostlund, S. B., Maidment, N. T., & Balleine, B. W.
- Affiliations
- University of California, Los Angeles (US)
- The University of Sydney (AU)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-07-28
- Volume
- 106
- Issue
- 30
- Pages
- 12512-12517
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2718390
- OpenAlex
- W2025466447
- Cited by
- 182
- References
- 41
- Citations by year
- 2026: 4 · 2025: 15 · 2024: 4 · 2023: 4 · 2022: 8 · 2021: 12 · 2020: 10 · 2019: 18 · 2018: 5 · 2017: 10 · 2016: 15 · 2015: 13 · 2014: 10 · 2013: 11 · 2012: 21
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R29MH056446, MH56446, R01MH056446, T32MH017140)
- National Institute on Drug Abuse (P50DA005010, DA05010, DA-09359, R01DA009359)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- endogenous opioids, palatability, incentive value, reward processing, nucleus accumbens shell, ventral pallidum, basolateral amygdala, food deprivation, sucrose, taste reactivity, naloxone, double dissociation, neural circuits
- MeSH terms
- Animals, Feeding Behavior, Food Deprivation, Food Preferences, Globus Pallidus, Male, Naloxone, Narcotic Antagonists, Neural Pathways, Nucleus Accumbens, Receptors, Opioid, Reward, Rats, Long-Evans, Rats
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