Extended habit training reduces dopamine mediation of appetitive response expression
Open accessAbstract
A wide range of behaviors is impaired after disruption of dopamine (DA) transmission, yet behaviors that are reflexive, automatic, or elicited by salient cues often remain intact. Responses triggered by strong external cues appear to be DA independent. Here, we examined the possibility that a single behavior may become DA independent as a result of extended training. Rats were trained to execute a head-entry response to a cue signaling food delivery. Vulnerability of the response to D1 or D2 receptor blockade was assessed on day 3, 7, or 17 of 28-trial-per-day training. During the early stages of training, the D1 receptor antagonist R(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine hydrochloride (SCH 23390) increased response latencies; however, the same behavior was unaffected by SCH 23390 in animals tested during the later stages of training. Other aspects of behavior such as locomotion and head-entry responses during the uncued intertrial interval remained vulnerable to SCH 23390 throughout the experiment. This D1-mediated response was unaffected by the D2 antagonist raclopride, even at a dose that strongly suppressed locomotion. The results provide strong evidence that a D1-dependent behavior becomes less dependent on DA with extended training. A number of fundamental neurobiological changes occur as behaviors become learned habits; at least for some responses, this change involves a shift from D1-mediated to D1-independent responding.
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Blockade of D1 receptors strongly disrupts rats' performance of a simple Pavlovian approach response to a sensory cue during early stages of training but has little or no disruptive effect in rats that receive extended training prior to dopamine antagonist challenge.
“As another example, blockade of D1 receptors strongly disrupts rats' performance of a simple Pavlovian approach response to a sensory cue during early stages of training, but has little or no disruptive effect in rats that receive extended training prior to dopamine antagonist challenge [46–47].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [46]
Some data indicate that over-trained responses can be independent of dopamine more generally.
“and of DA more generally [77]”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [77]
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Cites
Packard, M. G., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0007 · Cited by 1,505 · see citing works
Responses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987 · see citing works
SCH 23390, a potential benzazepine antipsychotic with unique interactions on dopaminergic systems.
Iorio, L. C., Barnett, A., Leitz, F. H., Houser, V. P., & Korduba, C. A. (1983) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)21599-3 · Cited by 896 · see citing works
Building neural representations of habits.
Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., & Graybiel, A. M. (1999) · Science · doi:10.1126/science.286.5445.1745 · Cited by 834 · see citing works
Salamone, J. D., & Correa, M. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00282-6 · Cited by 817 · see citing works
Anatomy of motor learning. I. Frontal cortex and attention to action
Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. J., & Passingham, R. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1313 · Cited by 624 · see citing works
Is the short-latency dopamine response too short to signal reward error?
Redgrave, P., Prescott, T. J., & Gurney, K. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01373-3 · Cited by 506 · see citing works
The basal ganglia and posture.
MARTIN, J. P. (1967) · Medical Entomology and Zoology · Cited by 470 · see citing works
Anatomy of Motor Learning. II. Subcortical Structures and Learning by Trial and Error
Jueptner, M., Frith, C., Brooks, D. J., Frackowiak, R. S. J., & Passingham, R. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1325 · Cited by 466 · see citing works
Book Review: Reward Signaling by Dopamine Neurons
Schultz, W. (2001) · The Neuroscientist · doi:10.1177/107385840100700406 · Cited by 343 · see citing works
Carli, M., Evenden, J. L., & Robbins, T. W. (1985) · Nature · doi:10.1038/313679a0 · Cited by 284 · see citing works
Beninger, R. J., & Hahn, B. (1983) · Science · doi:10.1126/science.6857251 · Cited by 254 · see citing works
Dopamine gating of forebrain neural ensembles
O’Donnell, P. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02463.x · Cited by 253 · see citing works
WILLED ACTION AND ITS IMPAIRMENTS
Jahanshahi, M. (1998) · Cognitive Neuropsychology · doi:10.1080/026432998381005 · Cited by 229 · see citing works
Horvitz, J. C. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00285-1 · Cited by 201 · see citing works
Self-citationThe use of conditioned suppression to evaluate the nature of neuroleptic-induced avoidance deficits.
Beninger, R. J., Mason, S. T., Phillips, A. G., & Fibiger, H. C. (1980) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)32116-6 · Cited by 144 · see citing works
Nucleus accumbens dopamine and work requirements on interval schedules
Correa, M., Carlson, B. B., Wisniecki, A., & Salamone, J. D. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00292-9 · Cited by 130 · see citing works
Carelli, R. M., Wolske, M., & West, M. O. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-05-01804.1997 · Cited by 114 · see citing works
An appetitively conditioned taste elicits a preferential increase in mesolimbic dopamine release
Mark, G. P., Smith, S. E., Rada, P. V., & Hoebel, B. G. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90327-1 · Cited by 101 · see citing works
Which Motor Disorder in Parkinson's Disease Indicates the True Motor Function of the Basal Ganglia?
Marsden, C. D. (1984) · Novartis Foundation symposium · doi:10.1002/9780470720882.ch12 · Cited by 83 · see citing works
Horvitz, J. C., & Ettenberg, A. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.4.536 · Cited by 52 · see citing works
Self-citationDeficits in the evolution of hand preshaping in Parkinson’s disease
Schettino, L. F., Rajaraman, V., Jack, D., Adamovich, S., Sage, J., & Howard Poizner, A. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(03)00150-7 · Cited by 50 · see citing works
Fowler, S. C., & Liou, J.-R. (1998) · Psychopharmacology · doi:10.1007/s002130050742 · Cited by 49 · see citing works
Dopamine receptor antagonist properties of S 14506, 8-OH-DPAT, raclopride and clozapine in rodents
Protais, P., Chagraoui, A., Arbaoui, J., et al. (1994) · European Journal of Pharmacology · doi:10.1016/0014-2999(94)90277-1 · Cited by 37 · see citing works
Effects of neuroleptics on rate and duration of operant versus reflexive licking in rats
Gramling, S. E., & Fowler, S. C. (1985) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(85)90272-2 · Cited by 37 · see citing works
Similar Effects of D1/D2 Receptor Blockade on Feeding and Locomotor Behavior
Pitts, S. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00249-x · Cited by 36 · see citing works
Phillips, G., Setzu, E., Vugler, A., & Hitchcott, P. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00799-6 · Cited by 35 · see citing works
Voluntary vs autonomous control of repetitive finger tapping in a patient with Parkinson's disease
Frischer, M. (1989) · Neuropsychologia · doi:10.1016/0028-3932(89)90038-9 · Cited by 29 · see citing works
Dopamine Mechanisms and Cocaine Reward
Ikegami, A., & Duvauchelle, C. L. (2004) · International review of neurobiology · doi:10.1016/s0074-7742(04)62002-2 · Cited by 18 · see citing works
Stern, E. R., Horvitz, J. C., COTE, L. J., & Mangels, J. A. (2005) · Neuropsychology · doi:10.1037/0894-4105.19.1.54 · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits
Salamone, J. D., Correa, M., Farrar, A., & Mingote, S. M. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0668-9 · Cited by 1,000 · see citing works
Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill
Yin, H. H., Mulcare, S. P., Hilário, M. R. F., Clouse, E., Holloway, T., Davis, M. I., Hansson, A. C., Lovinger, D. M., & Costa, R. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2261 · Cited by 818 · see citing works
Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making
Frank, M. J. (2006) · Neural Networks · doi:10.1016/j.neunet.2006.03.006 · Cited by 706 · see citing works
Cortical and basal ganglia contributions to habit learning and automaticity
Ashby, F. G., Turner, B. O., & Horvitz, J. C. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.02.001 · Cited by 481 · see citing works
Self-citationAmphetamine Exposure Enhances Habit Formation
Nelson, A., & Killcross, S. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4305-05.2006 · Cited by 445 · see citing works
Zweifel, L. S., Parker, J. G., Lobb, C. J., Rainwater, A., Wall, V. Z., Fadok, J. P., Darvas, M., Kim, M. J., Mizumori, S. J. Y., Paladini, C. A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813415106 · Cited by 426 · see citing works
Contributions of the striatum to learning, motivation, and performance: an associative account
Liljeholm, M., & O’Doherty, J. P. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.07.007 · Cited by 317 · see citing works
A neurobiological theory of automaticity in perceptual categorization
Ashby, F. G., Ennis, J. M., & Spiering, B. J. (2007) · Psychological Review · doi:10.1037/0033-295x.114.3.632 · Cited by 286 · see citing works
Summerfield, C., & Tsetsos, K. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00070 · Cited by 167 · see citing works
Changes in activity of the striatum during formation of a motor habit
Tang, C., Pawlak, A. P., Prokopenko, V., & West, M. O. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05353.x · Cited by 122 · see citing works
Interaction of raclopride and preparatory interval effects on simple reaction time performance
MacDonald, C. J., & Meck, W. H. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.004 · Cited by 44 · see citing works
HORVITZ, J. C., CHOI, W. Y., MORVAN, C., EYNY, Y., & BALSAM, P. D. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.017 · Cited by 26 · see citing works
Self-citationBespalov, A. Y., Harich, S., Jongen-Rêlo, A.-L., van Gaalen, M. M., & Gross, G. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0875-z · Cited by 8 · see citing works
- Authors
- Choi, W. Y., Balsam, P. D., & Horvitz, J. C.
- Affiliations
- Columbia University (US)
- Boston College (US)
- Corresponding author
- Horvitz, Jon C.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-07-20
- Volume
- 25
- Issue
- 29
- Pages
- 6729-6733
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6725359
- OpenAlex
- W2116441431
- Cited by
- 122
- References
- 30
- Citations by year
- 2026: 1 · 2024: 23 · 2022: 5 · 2021: 2 · 2020: 1 · 2019: 4 · 2018: 3 · 2017: 3 · 2016: 2 · 2015: 4 · 2014: 6 · 2013: 5 · 2012: 5
- FWCI
- 3.75
- 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
- National Institutes of Health (5r29da011653-05)
- National Institute on Drug Abuse (R29 DA 11653, R21DA015210)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- dopamine, habit formation, dopamine D1 receptor, dopamine D2 receptor, SCH 23390, raclopride, locomotion, behavioral learning, rats
- MeSH terms
- Animals, Appetitive Behavior, Behavior, Animal, Benzazepines, Conditioning, Psychological, Dopamine, Habits, Male, Rats, Sprague-Dawley, Receptors, Dopamine D1, Dopamine Antagonists, Raclopride, Rats
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