Separate neural substrates for skill learning and performance in the ventral and dorsal striatum
Abstract
It is widely accepted that the striatum of the basal ganglia is a primary substrate for the learning and performance of skills. We provide evidence that two regions of the rat striatum, ventral and dorsal, play distinct roles in instrumental conditioning (skill learning), with the ventral striatum being critical for learning and the dorsal striatum being important for performance but, notably, not for learning. This implies an actor (dorsal) versus director (ventral) division of labor, which is a new variant of the widely discussed actor-critic architecture. Our results also imply that the successful performance of a skill can ultimately result in its establishment as a habit outside the basal ganglia.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
It is unlikely that striatal regions differ functionally in terms of their respective contributions to learning versus performance.
“It is unlikely therefore, that these regions differ functionally in terms of their respective contributions to learning vs performance [10,11].”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [11]
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
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
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. G. (1998) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.1998.712192 · Cited by 27,225 · see citing works
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. (2005) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.2004.842673 · Cited by 25,263 · see citing works
Getting formal with dopamine and reward
Schultz, W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00967-4 · Cited by 2,574 · see citing works
Alexander, G. E., Crutcher, M. D., & DeLong, M. R. (1990) · PubMed · Cited by 2,422 · see citing works
Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning
O'Doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K., & Dolan, R. J. (2004) · Science · doi:10.1126/science.1094285 · Cited by 2,088 · see citing works
(1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62678-3 · Cited by 1,961 · see citing works
A neostriatal habit learning system in humans
Knowlton, B. J., Mangels, J. A., & Squire, L. R. (1996) · Science · doi:10.1126/science.273.5280.1399 · Cited by 1,777 · see citing works
Haber, S. N., Fudge, J. L., & McFarland, N. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02369.2000 · Cited by 1,610 · see citing works
Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans
Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J., & Frith, C. D. (2006) · Nature · doi:10.1038/nature05051 · Cited by 1,584 · see citing works
Temporal difference models and reward-related learning in the human brain
O'Doherty, J. P., Dayan, P., Friston, K., Critchley, H., & Dolan, R. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00169-7 · Cited by 1,522 · see citing works
Yin, H. H., Knowlton, B. J., & Balleine, B. W. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03095.x · Cited by 1,226 · see citing works
Dopamine neurons report an error in the temporal prediction of reward during learning
Hollerman, J. R., & Schultz, W. (1998) · Nature Neuroscience · doi:10.1038/1124 · Cited by 1,103 · see citing works
The role of the dorsomedial striatum in instrumental conditioning
Yin, H. H., Ostlund, S. B., Knowlton, B. J., & Balleine, B. W. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04218.x · Cited by 1,099 · see citing works
O’Reilly, R. C., & Frank, M. J. (2005) · Neural Computation · doi:10.1162/089976606775093909 · Cited by 1,066 · see citing works
Self-citationMotivational control of goal-directed action
Dickinson, A., & Balleine, B. (1994) · Animal Learning & Behavior · doi:10.3758/bf03199951 · Cited by 995 · see citing works
Packard, M. G., Hirsh, R., & White, N. M. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01465.1989 · Cited by 971 · see citing works
Frank, M. J. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929052880093 · Cited by 925 · see citing works
Reward, Motivation, and Reinforcement Learning
Dayan, P., & Balleine, B. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00963-7 · Cited by 855 · see citing works
Different time courses of learning-related activity in the prefrontal cortex and striatum.
Pasupathy, A., & Miller, E. K. (2005) · Nature · doi:10.1038/nature03287 · Cited by 712 · see citing works
Haber, S. N., Kim, K.-S., Mailly, P., & Calzavara, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0271-06.2006 · Cited by 686 · see citing works
Joel, D., & Weiner, I. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00575-8 · Cited by 614 · see citing works
Houk, J. C., & Wise, S. P. (1995) · Cerebral Cortex · doi:10.1093/cercor/5.2.95 · Cited by 594 · see citing works
Corbit, L. H., & Balleine, B. W. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4507-04.2005 · Cited by 589 · see citing works
Frank, M. J., & Claus, E. D. (2006) · Psychological Review · doi:10.1037/0033-295x.113.2.300 · Cited by 578 · see citing works
Corbit, L. H., Muir, J. L., & Balleine, B. W. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03251.2001 · Cited by 564 · see citing works
Packard, M. G., & McGaugh, J. L. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.3.439 · Cited by 555 · see citing works
Packard, M. G., & McGaugh, J. L. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.3.439 · Cited by 528 · see citing works
Haruno, M., & Kawato, M. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00382.2005 · Cited by 433 · see citing works
Joel, D., & Weiner, I. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90536-3 · Cited by 430 · see citing works
Striatal activation during acquisition of a cognitive skill.
Poldrack, R. A., Prabhakaran, V., Seger, C. A., & Gabrieli, J. D. E. (1999) · Neuropsychology · doi:10.1037//0894-4105.13.4.564 · Cited by 428 · see citing works
Striatal activation during acquisition of a cognitive skill.
Poldrack, R. A., Prabhakaran, V., Seger, C. A., & Gabrieli, J. D. E. (1999) · Neuropsychology · doi:10.1037/0894-4105.13.4.564 · Cited by 428 · see citing works
The Roles of the Caudate Nucleus in Human Classification Learning
Seger, C. A., & Cincotta, C. M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3401-04.2005 · Cited by 403 · see citing works
Relations between Pavlovian-instrumental transfer and reinforcer devaluation
Holland, P. C. (2004) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037/0097-7403.30.2.104 · Cited by 388 · see citing works
Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits
BALLEINE, B. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.061 · Cited by 326 · see citing works
Motivational control after extended instrumental training
Dickinson, A., Balleine, B. W., Watt, A. A., González, F., & Boakes, R. A. (1995) · Animal Learning & Behavior · doi:10.3758/bf03199935 · Cited by 286 · see citing works
Miyachi, S., Hikosaka, O., & Lu, X. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1213-7 · Cited by 262 · see citing works
Selective enhancement of associative learning by microstimulation of the anterior caudate
Williams, Z. M., & Eskandar, E. N. (2006) · Nature Neuroscience · doi:10.1038/nn1662 · Cited by 235 · see citing works
Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens
Hernandez, P. J., Sadeghian, K., & Kelley, A. E. (2002) · Nature Neuroscience · doi:10.1038/nn973 · Cited by 186 · see citing works
Role of Dopamine in the Primate Caudate Nucleus in Reward Modulation of Saccades
Nakamura, K., & Hikosaka, O. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4853-05.2006 · Cited by 179 · see citing works
Atallah, H. E., Frank, M. J., & O’Reilly, R. C. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.06.004 · Cited by 163 · see citing works
Self-citationThe Role of an Amygdalo-Nigrostriatal Pathway in Associative Learning
Han, J., McMahan, R. W., Holland, P. C., & Gallagher, M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03913.1997 · Cited by 154 · see citing works
Prediction Error during Retrospective Revaluation of Causal Associations in Humans
Corlett, P. R., Aitken, M. R. F., Dickinson, A., Shanks, D. R., Honey, G. D., Honey, R. A. E., Robbins, T. W., Bullmore, E. T., & Fletcher, P. C. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.022 · Cited by 144 · see citing works
The associative striatum: Organization of cortical projections to the dorsocentral striatum in rats
Reep, R. L., Cheatwood, J. L., & Corwin, J. V. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10868 · Cited by 125 · see citing works
Ventral–striatal/nucleus–accumbens sensitivity to prediction errors during classification learning
Rodriguez, P. F., Aron, A. R., & Poldrack, R. A. (2006) · Human Brain Mapping · doi:10.1002/hbm.20186 · Cited by 122 · see citing works
Featherstone, R. E., & McDonald, R. J. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00218-3 · Cited by 98 · see citing works
Corlett, P. R., Aitken, M. R. F., Dickinson, A., Shanks, D. R., Honey, G. D., Honey, R. A. E., Robbins, T. W., Bullmore, E. T., & Fletcher, P. C. (2004) · Neuron · doi:10.1016/s0896-6273(04)00756-1 · Cited by 98 · see citing works
Brain Dynamics and the Striatal Complex
Miller, R. J., & Wickens, J. (2000) · CRC Press eBooks · doi:10.1201/9781482283556 · Cited by 66 · see citing works
Kantak, K. M., Green-Jordan, K., Valencia, E., Kremin, T., & Eichenbaum, H. (2001) · Behavioral Neuroscience · doi:10.1037//0735-7044.115.3.589 · Cited by 53 · see citing works
Hernandez, P. J., Schiltz, C. A., & Kelley, A. E. (2006) · Learning & Memory · doi:10.1101/lm.335006 · Cited by 53 · see citing works
Overlap and interdigitation of cortical and thalamic afferents to dorsocentral striatum in the rat
Cheatwood, J. L., Corwin, J. V., & Reep, R. L. (2005) · Brain Research · doi:10.1016/j.brainres.2004.12.049 · Cited by 41 · see citing works
Kantak, K. M., Green-Jordan, K., Valencia, E., et al. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.3.589 · Cited by 39 · see citing works
Andrzejewski, M. E., Sadeghian, K., & Kelley, A. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.4.715 · Cited by 36 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
Wood, W., & Rünger, D. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033417 · Cited by 1,445 · see citing works
Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum
Corbit, L. H., Nie, H., & Janak, P. H. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.02.024 · Cited by 486 · see citing works
Yin, H. H., Ostlund, S. B., & Balleine, B. W. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06422.x · Cited by 416 · see citing works
A dual operator view of habitual behavior reflecting cortical and striatal dynamics
Smith, K. S., & Graybiel, A. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.038 · Cited by 324 · 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
Early-life stress is associated with impairment in cognitive control in adolescence: An fMRI study
Mueller, S. C., Maheu, F. S., Dozier, M., Peloso, E., Mandell, D., Leibenluft, E., Pine, D. S., & Ernst, M. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.06.013 · Cited by 297 · see citing works
The hippocampal-striatal axis in learning, prediction and goal-directed behavior
Pennartz, C. M. A., Ito, R., Verschure, P. F. M. J., Battaglia, F. P., & Robbins, T. W. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.001 · Cited by 287 · see citing works
Plichta, M. M., Vasic, N., Wolf, R. C., Lesch, K.-P., Brummer, D., Jacob, C., Fallgatter, A. J., & Grön, G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.07.008 · Cited by 272 · see citing works
Exposure to the Taste of Alcohol Elicits Activation of the Mesocorticolimbic Neurocircuitry
Filbey, F. M., Claus, E., Audette, A. R., Niculescu, M., Banich, M. T., Tanabe, J., Du, Y. P., & Hutchison, K. E. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301513 · Cited by 270 · see citing works
Anticipatory reward processing in addicted populations: a focus on the monetary incentive delay task
Balodis, I. M., & Potenza, M. N. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.08.020 · Cited by 267 · see citing works
Neural structures mediating expression and extinction of platform-mediated avoidance
Bravo-Rivera, C., Roman-Ortiz, C., Brignoni-Perez, E., Sotres-Bayon, F., & Quirk, G. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0191-14.2014 · Cited by 206 · see citing works
Corticostriatal Interactions during Learning, Memory Processing, and Decision Making
Pennartz, C. M. A., Berke, J. D., Graybiel, A. M., Ito, R., Lansink, C. S., van der Meer, M., Redish, A. D., Smith, K. S., & Voorn, P. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3177-09.2009 · Cited by 213 · see citing works
Still at the Choice‐Point: Action Selection and Initiation in Instrumental Conditioning
BALLEINE, B. W., & OSTLUND, S. B. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.006 · Cited by 184 · see citing works
Guyer, A. E., Benson, B., Choate, V. R., Bar-Haim, Y., Perez-Edgar, K., Jarcho, J. M., Pine, D. S., Ernst, M., Fox, N. A., & Nelson, E. E. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000941 · Cited by 109 · see citing works
Piron, C., Kase, D., Topalidou, M., Goillandeau, M., Orignac, H., N'Guyen, T., Rougier, N., & Boraud, T. (2016) · Movement Disorders · doi:10.1002/mds.26542 · Cited by 66 · see citing works
Strong, P. V., Christianson, J. P., Loughridge, A. B., Amat, J., Maier, S. F., Fleshner, M., & Greenwood, B. N. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.041 · Cited by 61 · see citing works
Neuroprotection in focal cerebral ischemia owing to delayed treatment with melanocortins
Giuliani, D., Ottani, A., Mioni, C., Bazzani, C., Galantucci, M., Minutoli, L., Bitto, A., Zaffe, D., Botticelli, A. R., Squadrito, F., et al. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.05.025 · Cited by 44 · see citing works
Lin, H.-C., Pan, H.-C., Lin, S.-H., Lo, Y.-C., Shen, E. T.-H., Liao, L.-D., Liao, P.-H., Chien, Y.-W., Liao, K.-D., Jaw, F.-S., et al. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00087 · Cited by 29 · see citing works
Human habit neural circuitry may be perturbed in eating disorders
Wang, A. R., Kuijper, F. M., Barbosa, D. A. N., Hagan, K. E., Lee, E., Tong, E., Choi, E. Y., McNab, J. A., Bohon, C., & Halpern, C. H. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.abo4919 · Cited by 27 · see citing works
- Authors
- Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W., & O'Reilly, R. C.
- Affiliations
- University of Colorado Boulder (US)
- Corresponding author
- Atallah, Hisham E
- ORCID
- Rudy, Jerry W
- Venue
- Nature Neuroscience
- Published
- 2006-12-24
- Volume
- 10
- Issue
- 1
- Pages
- 126-131
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2095819174
- Cited by
- 241
- References
- 54
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 5 · 2020: 7 · 2019: 9 · 2018: 9 · 2017: 10 · 2016: 18 · 2015: 11 · 2014: 21 · 2013: 18 · 2012: 22
- FWCI
- 7.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01MH069597, MH 069597-01)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- ventral striatum, dorsal striatum, basal ganglia, skill acquisition, skill performance, operant conditioning, actor-critic architecture, habit formation
- MeSH terms
- Analysis of Variance, Animals, Behavior, Animal, Conditioning, Classical, Conditioning, Operant, Corpus Striatum, Male, Muscimol, Psychomotor Performance, Reaction Time, 2-Amino-5-phosphonovalerate, Excitatory Amino Acid Antagonists, 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.
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