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Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill

Nature Neuroscience volume 12, pages 333–341 (2009)Cite this article

Abstract

The learning of new skills is characterized by an initial phase of rapid improvement in performance and a phase of more gradual improvements as skills are automatized and performance asymptotes. Using in vivo striatal recordings, we observed region-specific changes in neural activity during the different phases of skill learning, with the associative or dorsomedial striatum being preferentially engaged early in training and the sensorimotor or dorsolateral striatum being engaged later in training. Ex vivo recordings from medium spiny striatal neurons in brain slices of trained mice revealed that the changes observed in vivo corresponded to regional- and training-specific changes in excitatory synaptic transmission in the striatum. Furthermore, the potentiation of glutamatergic transmission observed in dorsolateral striatum after extensive training was preferentially expressed in striatopallidal neurons, rather than striatonigral neurons. These findings demonstrate that region- and pathway-specific plasticity sculpts the circuits involved in the performance of the skill as it becomes automatized.

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Figure 1: In vivo recordings of neuronal activity in the DMS and DLS striatal regions during different phases of skill learning.
Figure 2: Ex vivo striatal field potential recordings in the DMS and DLS during different phases of skill learning.
Figure 3: Ex vivo striatal whole cell recordings in the DMS and DLS during the different phases of skill learning.
Figure 4: Training results in region-specific changes in excitability and in threshold to spike in the DLS and the DMS.
Figure 5: Extensive training results in pathway-specific plasticity.

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Acknowledgements

We thank T. Gremel and X. Jin for comments on the manuscript. This research was supported by the Division of Intramural Clinical and Basic Research of the National Institute on Alcohol Abuse and Alcoholism, US National Institutes of Health.

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Authors and Affiliations

  1. Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, US National Institutes of Health, 5625 Fishers Lane, MSC 9411, Bethesda, 20852-9411, Maryland, USA

    Henry H Yin, Shweta Prasad Mulcare, Monica R F Hilário, Emily Clouse, Terrell Holloway, Margaret I Davis, David M Lovinger & Rui M Costa

  2. Department of Psychology and Neuroscience, Center for Cognitive Neuroscience, Duke University, 103 Research Drive, Box 91050, Durham, 27708, North Carolina, USA

    Henry H Yin

  3. Laboratory of Clinical and Translational Studies, National Institute on Alcohol Abuse and Alcoholism, US National Institutes of Health, 10 Center Drive, Bethesda, 20892-1108, Maryland, USA

    Anita C Hansson

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Contributions

H.H.Y. planned the experiments, conducted the behavioral experiments and in vivo and ex vivo recordings, performed data analyses and wrote the manuscript. S.P.M. performed ex vivo field recordings and data analyses. M.R.F.H. performed lesions, histology and behavioral experiments. E.C. and T.H. performed behavioral experiments; M.I.D. carried out immunohistochemistry; A.C.H. performed the dopamine binding experiments; D.M.L. contributed to experimental design and the writing of the manuscript; and R.M.C. planned and supervised experiments, contributed to behavioral experiments, histology and in vivo recordings, performed data analyses and wrote the manuscript.

Corresponding author

Correspondence to Rui M Costa.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5, Supplementary Table 1 and Supplementary Methods (PDF 312 kb)

Supplementary Video 1

Naive mouse in rotarod 30 min after D1 + D2 dopamine receptor blockade. Note that the mouse is akinetic at the base of the rotarod, and once it is placed on the rotarod, it immediately falls. Reflexes are unaffected. (MPG 1818 kb)

Supplementary Video 2

Overtrained mouse 30 min after D1 + D2 dopamine receptor blockade. Note that the mouse is akinetic at the base of the rotarod, and once it is placed in the rotarod, it runs on the rod. (MPG 1962 kb)

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Yin, H., Mulcare, S., Hilário, M. et al. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 12, 333–341 (2009). https://doi.org/10.1038/nn.2261

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