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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.

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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.

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Acknowledgements

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.

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

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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)

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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). https://doi.org/10.1038/nn1817

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