Instant transformation of learned repulsion into motivational “wanting”
Open accessAbstract
Background Learned cues for pleasant reward often elicit desire, which, in addicts, may become compulsive. According to the dominant view in addiction neuroscience and reinforcement modeling, such desires are the simple products of learning, coming from a past association with reward outcome.Results We demonstrate that cravings are more than merely the products of accumulated pleasure memories-even a repulsive learned cue for unpleasantness can become suddenly desired via the activation of mesocorticolimbic circuitry. Rats learned repulsion toward a Pavlovian cue (a briefly-inserted metal lever) that always predicted an unpleasant Dead Sea saltiness sensation. Yet, upon first reencounter in a novel sodium-depletion state to promote mesocorticolimbic reactivity (reflected by elevated Fos activation in ventral tegmentum, nucleus accumbens, ventral pallidum, and the orbitofrontal prefrontal cortex), the learned cue was instantly transformed into an attractive and powerful motivational magnet. Rats jumped and gnawed on the suddenly attractive Pavlovian lever cue, despite never having tasted intense saltiness as anything other than disgusting.Conclusions Instant desire transformation of a learned cue contradicts views that Pavlovian desires are essentially based on previously learned values (e.g., prediction error or temporal difference models). Instead desire is recomputed at reencounter by integrating Pavlovian information with the current brain/physiological state. This powerful brain transformation reverses strong learned revulsion into avid attraction. When applied to addiction, related mesocorticolimbic transformations (e.g., drugs or neural sensitization) of cues for already-pleasant drug experiences could create even more intense cravings. This cue/state transformation helps define what it means to say that addiction hijacks brain limbic circuits of natural reward.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Sodium depletion causes a robust and highly specific motivation to consume sodium, such that salt solutions that are negative/aversive in the replete state become preferred/rewarding in sodium-depleted animals.
“Sodium depletion causes a robust and highly specific motivation to consume sodium, such that salt solutions that are negative/aversive in the replete state become preferred/rewarding in sodium-depleted animals”
From FGF21 and the physiological regulation of macronutrient preference (2020) · cites this paper as [20]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
The neural basis of drug craving: An incentive-sensitization theory of addiction
Robinson, T. (1993) · Brain Research Reviews · doi:10.1016/0165-0173(93)90013-p · Cited by 7,346 · see citing works
Daw, N. D., Niv, Y., & Dayan, P. (2005) · Nature Neuroscience · doi:10.1038/nn1560 · Cited by 2,533 · see citing works
Integrative activity of the brain
Konorski, J. (1967) · University of Chicago Press eBooks · Cited by 2,043 · see citing works
Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction
Volkow, N. D., Wang, G.-J., Telang, F., Fowler, J. S., Logan, J., Childress, A.-R., Jayne, M., Ma, Y., & Wong, C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1544-06.2006 · Cited by 1,164 · see citing works
From prediction error to incentive salience: mesolimbic computation of reward motivation.
Berridge, K. C. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.07990.x · Cited by 700 · see citing works
Self-citationPeciña, S., & Berridge, K. C. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2329-05.2005 · Cited by 671 · see citing works
Self-citationUpdating dopamine reward signals
Schultz, W. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.012 · Cited by 651 · see citing works
Addiction as a Computational Process Gone Awry
Redish, A. D. (2004) · Science · doi:10.1126/science.1102384 · Cited by 534 · see citing works
Integrative Activity of the Brain: An Interdisciplinary Approach
Ochs, S. (1968) · JAMA · doi:10.1001/jama.1968.03140050055025 · Cited by 524 · see citing works
Disentangling pleasure from incentive salience and learning signals in brain reward circuitry
Smith, K. S., Berridge, K. C., & Aldridge, J. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101920108 · Cited by 464 · see citing works
Self-citationMahler, S. V., Smith, K. S., & Berridge, K. C. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301376 · Cited by 377 · see citing works
A Neural Computational Model of Incentive Salience
Zhang, J., Berridge, K. C., Tindell, A. J., Smith, K. S., & Aldridge, J. W. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000437 · Cited by 299 · see citing works
Self-citationCentral regulation of sodium appetite
Geerling, J. C., & Loewy, A. D. (2007) · Experimental Physiology · doi:10.1113/expphysiol.2007.039891 · Cited by 275 · see citing works
Ventral pallidum firing codes hedonic reward: when a bad taste turns good
Tindell, A. J., Smith, K. S., Peciña, S., Berridge, K. C., & Aldridge, J. W. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00576.2006 · Cited by 241 · see citing works
Self-citationEvent representation in Pavlovian conditioning: Image and action
Holland, P. C. (1990) · Cognition · doi:10.1016/0010-0277(90)90020-k · Cited by 229 · see citing works
Mahler, S. V., & Berridge, K. C. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3875-08.2009 · Cited by 223 · see citing works
Self-citationConditioned cues and the expression of stimulant sensitization in animals and humans
Vezina, P., & Leyton, M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.070 · Cited by 201 · see citing works
Fluharty, S. J., & Epstein, A. N. (1983) · Behavioral Neuroscience · doi:10.1037//0735-7044.97.5.746 · Cited by 199 · see citing works
The hunger for salt: An anthropological, physiological and medical analysis-by
(1984) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(84)90037-9 · Cited by 198 · see citing works
Faure, A., Reynolds, S. M., Richard, J. M., & Berridge, K. C. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4961-07.2008 · Cited by 193 · see citing works
Self-citationFluharty, S. J., & Epstein, A. N. (1983) · Behavioral Neuroscience · doi:10.1037/0735-7044.97.5.746 · Cited by 193 · see citing works
Thompson, R. H., & Swanson, L. W. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009112107 · Cited by 158 · see citing works
The hunger for salt. An anthropological, physiological and medical analysis
(1983) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(83)90123-4 · Cited by 148 · see citing works
Acquisition of sodium by rats: Interaction of innate mechanisms and latent learning.
Krieckhaus, E. E., & Wolf, G. (1968) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0025547 · Cited by 138 · see citing works
Palatability shift of a salt-associated incentive during sodium depletion.
Berridge, K. C., & Schulkin, J. A. (1989) · PubMed · Cited by 127 · see citing works
Self-citationDynamic Computation of Incentive Salience: “Wanting” What Was Never “Liked”
Tindell, A. J., Smith, K. S., Berridge, K. C., & Aldridge, J. W. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2499-09.2009 · Cited by 124 · see citing works
Self-citationDual Roles of Dopamine in Food and Drug Seeking: The Drive-Reward Paradox
Wise, R. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.001 · Cited by 95 · see citing works
Sensory preconditioning of flavors with a formalin-produced sodium need.
Fudim, O. K. (1978) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.4.3.276 · Cited by 65 · see citing works
Liedtke, W., McKinley, M. J., Walker, L., Zhang, H., Pfenning, A. R., Drago, J., Hochendoner, S. J., Hilton, D. L., Lawrence, A. J., & Denton, D. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109199108 · Cited by 62 · see citing works
Richter and sodium appetite: from adrenalectomy to molecular biology
Krause, E. G., & Sakai, R. R. (2007) · Appetite · doi:10.1016/j.appet.2007.01.015 · Cited by 54 · see citing works
Control of fluid palatability by exteroceptive Pavlovian signals.
Delamater, A. R., LoLordo, V. M., & Berridge, K. C. (1986) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.12.2.143 · Cited by 52 · see citing works
Self-citationSensory preconditioning of flavors with a formalin-produced sodium need.
Fudim, O. K. (1978) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.4.3.276 · Cited by 51 · see citing works
Lucas, L., Grillo, C. A., & McEwen, B. S. (2003) · Neuroendocrinology · doi:10.1159/000071312 · Cited by 41 · see citing works
Control of fluid palatability by exteroceptive Pavlovian signals.
Delamater, A. R., LoLordo, V. M., & Berridge, K. C. (1986) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.12.2.143 · Cited by 41 · see citing works
Self-citation"Innate recognition" aids rats in sodium regulation.
Krieckhaus, E. E. (1970) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0030020 · Cited by 39 · see citing works
Alheid, G. F., Shammah‐Lagnado, S. J., & Beltramino, C. A. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09294.x · Cited by 35 · see citing works
Salt Appetite in Sodium-Depleted or Sodium-Replete Conditions: Possible Role of Opioid Receptors
Lucas, L., Grillo, C. A., & McEwen, B. S. (2007) · Neuroendocrinology · doi:10.1159/000102536 · Cited by 33 · see citing works
Dickinson, A. (1986) · PubMed · Cited by 29 · see citing works
A latent cue preference based on sodium depletion in ratsPreprint
Stouffer, E. M., & White, N. M. (2005) · Learning & Memory · doi:10.1101/lm.96305 · Cited by 20 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [1]Toates F Motivational Systems 1986 New York Cambridge University Press
- [7]Rackham H Jones WHS Pliny the Elder (77AD) Natural history Cambridge Harvard University Press
- [20]Dickinson A Balleine B Hedonics cognitive motivation interface Pleasures of the Brain 2010 United States Oxford University Press 74 84
Cited by
Sorted by citations
Berridge, K. C., & Kringelbach, M. L. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.018 · Cited by 1,730 · see citing works
Self-citationLiking, wanting, and the incentive-sensitization theory of addiction
Berridge, K. C., & Robinson, T. E. (2016) · American Psychologist · doi:10.1037/amp0000059 · Cited by 1,440 · see citing works
Self-citationNeuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126 · see citing works
Dolan, R. J., & Dayan, P. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.007 · Cited by 977 · see citing works
Neurons for hunger and thirst transmit a negative-valence teaching signal
Betley, J. N., Xu, S., Cao, Z. F. H., Gong, R., Magnus, C. J., Yu, Y., & Sternson, S. M. (2015) · Nature · doi:10.1038/nature14416 · Cited by 704 · see citing works
Lindquist, K. A., Satpute, A. B., Wager, T. D., Weber, J., & Barrett, L. F. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv001 · Cited by 713 · see citing works
Craske, M. G., Meuret, A. E., Ritz, T., Treanor, M., & Dour, H. J. (2016) · Depression and Anxiety · doi:10.1002/da.22490 · Cited by 387 · see citing works
Model-based and model-free Pavlovian reward learning: Revaluation, revision, and revelation
Dayan, P., & Berridge, K. C. (2014) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-014-0277-8 · Cited by 357 · see citing works
Self-citation“Liking” and “wanting” in eating and food reward: Brain mechanisms and clinical implications
Morales, I., & Berridge, K. C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113152 · Cited by 346 · see citing works
Self-citationEvolving Concepts of Emotion and Motivation
Berridge, K. C. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.01647 · Cited by 273 · see citing works
Self-citationNeuroscience of Internet Pornography Addiction: A Review and Update
Love, T., Laier, C., Brand, M., Hatch, L., & Hajela, R. (2015) · Behavioral Sciences · doi:10.3390/bs5030388 · Cited by 262 · see citing works
Measuring wanting and liking from animals to humans: a systematic review
Pool, E., Sennwald, V., Delplanque, S., Brosch, T., & Sander, D. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.006 · Cited by 211 · see citing works
Volman, S. F., Lammel, S., Margolis, E. B., Kim, Y., Richard, J. M., Roitman, M. F., & Lobo, M. K. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3250-13.2013 · Cited by 168 · see citing works
Current perspectives on incentive salience and applications to clinical disorders
Olney, J. J., Warlow, S. M., Naffziger, E. E., & Berridge, K. C. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.01.007 · Cited by 157 · see citing works
Self-citationDopamine, reward learning, and active inference
FitzGerald, T. H. B., Dolan, R. J., & Friston, K. (2015) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2015.00136 · Cited by 112 · see citing works
FGF21 and the physiological regulation of macronutrient preference
Hill, C. M., Qualls-Creekmore, E., Berthoud, H.-R., Soto, P., Yu, S., McDougal, D. H., Münzberg, H., & Morrison, C. D. (2020) · Endocrinology · doi:10.1210/endocr/bqaa019 · Cited by 99 · see citing works
Murphy, M., Peters, K. Z., Denton, B. S., Lee, K. A., Chadchankar, H., & McCutcheon, J. E. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.12.011 · Cited by 42 · see citing works
Disrupting reconsolidation: memory erasure or blunting of emotional/motivational value?
Cogan, E. S., Shapses, M. A., Robinson, T. E., & Tronson, N. C. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-018-0082-0 · Cited by 25 · see citing works
Fortin, S. M., & Roitman, M. F. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.11.021 · Cited by 11 · see citing works
The Functions of Dopamine in Operant Conditioned Reflexes
Maiorov, V. I. (2019) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-019-00815-y · Cited by 10 · see citing works
State-dependent value representation: evidence from the striatum
Burke, C. J., Dreher, J.-C., Seymour, B., & Tobler, P. N. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00193 · Cited by 4 · see citing works
- Authors
- Robinson, M. J. F., & Berridge, K. C.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Robinson, Mike J.F.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2013-02
- Volume
- 23
- Issue
- 4
- Pages
- 282-289
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC3580026
- OpenAlex
- W2016865357
- Cited by
- 320
- References
- 41
- Citations by year
- 2026: 6 · 2025: 14 · 2024: 15 · 2023: 17 · 2022: 16 · 2021: 16 · 2020: 58 · 2019: 55 · 2018: 24 · 2017: 20 · 2016: 22 · 2015: 27 · 2014: 25 · 2013: 5
- FWCI
- 12.91
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH-63649, R01MH063649)
- National Institute on Drug Abuse (R01DA015188, DA015188-01-A1)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- craving, classical conditioning, mesocorticolimbic circuitry, Fos activation, ventral tegmental area, nucleus accumbens, ventral pallidum, orbitofrontal cortex, sodium depletion, addiction, natural reward, neural sensitization
- MeSH terms
- Animals, Brain, Conditioning, Classical, Cues, Female, Food Deprivation, Learning, Motivation, Reinforcement, Psychology, Reward, Sodium Chloride, Behavior, Addictive, Rats, Sprague-Dawley, Substance-Related Disorders, Rats, Pleasure
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
