Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Separate neural substrates for skill learning and performance in the ventral and dorsal striatum


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Effects of muscimol and AP-5 in the ventral striatum on the instrumental task.
Figure 2: Response latencies (seconds) after injections in the ventral and dorsal striatum.
Figure 3: Effects of muscimol and AP-5 in the dorsal striatum on the instrumental task.
Figure 4: The effect of muscimol in dorsal striatum on subsequent test performance.
Figure 5: The effect of pavlovian pretraining on instrumental performance.
Figure 6: The effect of pavlovian pretraining on a pavlovian test.


  1. 1

    Packard, M.G., Hirsh, R. & White, N.M. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J. Neurosci. 9, 1465–1472 (1989).

    CAS  Article  Google Scholar 

  2. 2

    Kantak, K.M., Green-Jordan, K., Valencia, E., Kremin, T. & Eichenbaum, H.B. Cognitive task performance after lidocaine-induced inactivation of different sites within the basolateral amygdala and dorsal striatum. Behav. Neurosci. 115, 589–601 (2001).

    CAS  Article  Google Scholar 

  3. 3

    Packard, M.G. & McGaugh, J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behav. Neurosci. 106, 439–446 (1992).

    CAS  Article  Google Scholar 

  4. 4

    Nakamura, K. & Hikosaka, O. Role of dopamine in the primate caudate nucleus in reward modulation of saccades. J. Neurosci. 26, 5360–5369 (2006).

    CAS  Article  Google Scholar 

  5. 5

    Williams, Z.M. & Eskandar, E.N. Selective enhancement of associative learning by microstimulation of the anterior caudate. Nat. Neurosci. 9, 562–568 (2006).

    CAS  Article  Google Scholar 

  6. 6

    Featherstone, R.E. & McDonald, R.J. Dorsal striatum and stimulus-response learning: lesions of the dorsolateral, but not dorsomedial, striatum impair acquisition of a simple discrimination task. Behav. Brain Res. 150, 15–23 (2004).

    CAS  Article  Google Scholar 

  7. 7

    Poldrack, R.A., Prabhakaran, V., Seger, C.A. & Gabrieli, J.D. Striatal activation during memory acquisition of cognitive skill. Neuropsychology 13, 564–574 (1999).

    CAS  Article  Google Scholar 

  8. 8

    Knowlton, B.J., Mangels, J.A. & Squire, L.R. A neostriatal habit learning system in humans. Science 273, 1399–1402 (1996).

    CAS  Article  Google Scholar 

  9. 9

    Hernandez, P.J., Sadeghian, K. & Kelley, A.E. Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens. Nat. Neurosci. 5, 1327–1331 (2002).

    CAS  Article  Google Scholar 

  10. 10

    O'Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452–454 (2004).

    CAS  Article  Google Scholar 

  11. 11

    Alexander, G.E., Crutcher, M.D. & DeLong, M.R. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog. Brain Res. 85, 119–146 (1990).

    CAS  Article  Google Scholar 

  12. 12

    Haber, S.N., Fudge, J.L. & McFarland, N.R. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci. 20, 2369–2382 (2000).

    CAS  Article  Google Scholar 

  13. 13

    Haber, S.N., Kim, K., Mailly, P. & Calzavara, R. Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J. Neurosci. 26, 8368–8376 (2006).

    CAS  Article  Google Scholar 

  14. 14

    Seger, C.A. & Cincotta, C.M. The role of the caudate nucleus in human classification learning. J. Neurosci. 25, 2941–2951 (2005).

    CAS  Article  Google Scholar 

  15. 15

    Corbit, L.H., Muir, J.L. & Balleine, B.W. The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between core and shell. J. Neurosci. 21, 3251–3260 (2001).

    CAS  Article  Google Scholar 

  16. 16

    Sutton, R.S. & Barto, A.G. Reinforcement Learning: An Introduction. (MIT Press, Cambridge, Massachusetts, USA, 1998).

    Google Scholar 

  17. 17

    Houk, J.C. & Wise, S.P. Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action. Cereb. Cortex 5, 95–110 (1995).

    CAS  Article  Google Scholar 

  18. 18

    Corbit, L.H. & Balleine, B.W. Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer. J. Neurosci. 25, 962–970 (2005).

    CAS  Article  Google Scholar 

  19. 19

    Holland, P.C. Relations between pavlovian-instrumental transfer and reinforcer devaluation. J. Exp. Psychol. Anim. Behav. Process. 30, 104–117 (2004).

    Article  Google Scholar 

  20. 20

    Hernandez, P.J., Schiltz, C.A. & Kelley, A.E. Dynamic shifts in corticostriatal expression patterns of the immediate early genes Homer 1a and Zif268 during early and late phases of instrumental training. Learn. Mem. 13, 599–608 (2006).

    CAS  Article  Google Scholar 

  21. 21

    Han, J.S., McMahan, R.W., Holland, P. & Gallagher, M. The role of an amygdalo-nigrostriatal pathway in associative learning. J. Neurosci. 17, 3913–3919 (1997).

    CAS  Article  Google Scholar 

  22. 22

    Andrzejewski, M.E., Sadeghian, K. & Kelley, A.E. Central amygdalar and dorsal striatal NMDA receptor involvement in instrumental learning and spontaneous behavior. Behav. Neurosci. 118, 715–729 (2004).

    CAS  Article  Google Scholar 

  23. 23

    Haruno, M. & Kawato, M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J. Neurophysiol. 95, 948–959 (2005).

    Article  Google Scholar 

  24. 24

    Rodriguez, P.F., Aron, A.R. & Poldrack, R.A. Ventral-striatal/nucleus-accumbens sensitivity to prediction errors during classification learning. Hum. Brain Mapp. 27, 306–313 (2006).

    CAS  Article  Google Scholar 

  25. 25

    Pessiglione, M., Seymour, B., Flandin, G., Dolan, R.J. & Frith, C.D. Dopamine-dependent prediction errors underpin reward-seeking behavior in humans. Nature 442, 1042–1045 (2006).

    CAS  Article  Google Scholar 

  26. 26

    Corlett, P.R. et al. Prediction error during retrospective revaluation of causal associations in humans: fMRI evidence in favor of associative model of learning. Neuron 44, 877–888 (2004).

    CAS  PubMed  Google Scholar 

  27. 27

    O'Doherty, J.P., Dayan, P., Friston, K., Critchley, H. & Dolan, R.J. Temporal difference models and reward-related learning in the human brain. Neuron 38, 329–337 (2003).

    CAS  Article  Google Scholar 

  28. 28

    Hollerman, J.R. & Schultz, W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1, 304–309 (1998).

    CAS  Article  Google Scholar 

  29. 29

    Miyachi, S., Hikosaka, O. & Lu, X. Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp. Brain Res. 146, 122–126 (2002).

    Article  Google Scholar 

  30. 30

    Reep, R.L., Cheatwood, J.L. & Corwin, J.V. The associative striatum: organization of cortical projections to the dorsocentral striatum in rats. J. Comp. Neurol. 467, 271–292 (2003).

    Article  Google Scholar 

  31. 31

    Cheatwood, J.L., Corwin, J.V. & Reep, R.L. Overlap and interdigitation of cortical and thalamic afferents to dorsocentral striatum in the rat. Brain Res. 1036, 90–100 (2005).

    CAS  Article  Google Scholar 

  32. 32

    Atallah, H.E., Frank, M.J. & O'Reilly, R.C. Hippocampus, cortex, and basal ganglia: insights from computational models of complementary learning systems. Neurobiol. Learn. Mem. 82, 253–267 (2004).

    Article  Google Scholar 

  33. 33

    Frank, M.J. Dynamic dopamine modulation of the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated parkinsonism. J. Cogn. Neurosci. 17, 51–72 (2005).

    Article  Google Scholar 

  34. 34

    Pasupathy, A. & Miller, E.K. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433, 873–876 (2005).

    CAS  Article  Google Scholar 

  35. 35

    Dickinson, A., Balleine, B.W., Watt, A., Gonzales, F. & Boakes, R.A. Overtraining and the motivational control of instrumental action. Anim. Learn. Behav. 22, 197–206 (1995).

    Article  Google Scholar 

  36. 36

    Dickinson, A. & Balleine, B. Motivational control of goal directed action. Anim. Learn. Behav. 22, 1–18 (1994).

    Article  Google Scholar 

  37. 37

    Dayan, P. & Balleine, B.W. Reward, motivation, and reinforcement learning. Neuron 36, 285–298 (2002).

    CAS  Article  Google Scholar 

  38. 38

    Yin, H.H., Ostlund, S.B., Knowlton, B.J. & Balleine, B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 22, 513–523 (2005).

    Article  Google Scholar 

  39. 39

    Yin, H.H., Knowlton, B.J. & Balleine, B.W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 19, 181–189 (2004).

    Article  Google Scholar 

  40. 40

    Balleine, B.W. Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits. Physiol. Behav. 86, 717–730 (2005).

    CAS  Article  Google Scholar 

  41. 41

    O'Reilly, R.C. & Frank, M.J. Making working memory work: a computational model of learning in the prefrontal cortex and basal ganglia. Neural Comput. 18, 283–328 (2006).

    Article  Google Scholar 

  42. 42

    Schultz, W. Getting formal with dopamine. Neuron 36, 241–263 (2002).

    CAS  Article  Google Scholar 

  43. 43

    Frank, M.J. & Claus, E.D. Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychol. Rev. 113, 300–326 (2006).

    Article  Google Scholar 

  44. 44

    Joel, D. & Weiner, I. The organization of the basal ganglia-thalamocortical circuits: open interconnected rather than closed segregated. Neuroscience 63, 363–379 (1994).

    CAS  Article  Google Scholar 

  45. 45

    Joel, D. & Weiner, I. Striatal contention scheduling and the split circuit scheme of basal ganglia-thalamocortical circuitry: from anatomy to behavior. In Brain Dynamics and the Striatal Complex (eds. Miller, R. & Wickens, J.R.) 209–236 (Harwood Academic Publishers, Amsterdam, 2000).

    Google Scholar 

  46. 46

    Joel, D. & Weiner, I. The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96, 451–474 (2000).

    CAS  Article  Google Scholar 

  47. 47

    Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Academic, San Diego, 1997).

    Google Scholar 

Download references


We thank M.J. Frank, T.E. Hazy and the members of the Computational Cognitive Neuroscience laboratory for comments on this manuscript. This work was supported by Defense Advanced Research Projects Agency–Office of Naval Research N00014-05-1-0880 and US National Institutes of Health MH069597-01.

Author information



Corresponding authors

Correspondence to Hisham E Atallah or Randall C O'Reilly.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Injection sites in ventral striatum for the acquisition groups. (PDF 362 kb)

Supplementary Fig. 2

Injection sites in ventral striatum for the test groups. (PDF 368 kb)

Supplementary Fig. 3

Injection sites in dorsal striatum for the acquisition groups. (PDF 360 kb)

Supplementary Fig. 4

Injection sites in dorsal striatum for the test groups. (PDF 581 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Atallah, H., Lopez-Paniagua, D., Rudy, J. et al. Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nat Neurosci 10, 126–131 (2007).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing