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Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills

Abstract

The ability to learn new skills and perfect them with practice applies not only to physical skills but also to abstract skills1, like motor planning or neuroprosthetic actions. Although plasticity in corticostriatal circuits has been implicated in learning physical skills2,3,4, it remains unclear if similar circuits or processes are required for abstract skill learning. Here we use a novel behavioural task in rodents to investigate the role of corticostriatal plasticity in abstract skill learning. Rodents learned to control the pitch of an auditory cursor to reach one of two targets by modulating activity in primary motor cortex irrespective of physical movement. Degradation of the relation between action and outcome, as well as sensory-specific devaluation and omission tests, demonstrate that these learned neuroprosthetic actions are intentional and goal-directed, rather than habitual. Striatal neurons change their activity with learning, with more neurons modulating their activity in relation to target-reaching as learning progresses. Concomitantly, strong relations between the activity of neurons in motor cortex and the striatum emerge. Specific deletion of striatal NMDA receptors impairs the development of this corticostriatal plasticity, and disrupts the ability to learn neuroprosthetic skills. These results suggest that corticostriatal plasticity is necessary for abstract skill learning, and that neuroprosthetic movements capitalize on the neural circuitry involved in natural motor learning.

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Figure 1: Volitional modulation of M1 neural activity in awake behaving rodents.
Figure 2: Learning intentional neuroprosthetic actions independently of movement.
Figure 3: Learning abstract skills is accompanied by corticostriatal plasticity.
Figure 4: Selective deletion of NMDARs in the striatum impairs brain–machine interface learning.

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Acknowledgements

We thank S. Venkatraman for the three-axis accelerometer, Y. Li for the RGS9L-Cre mice, K. Nakazawa for the NMDAR1-loxP mice, G. Luo for genotyping, M. Davis for advice on staining and G. Martins for performing immunohistochemistry. This work was supported by National Science Foundation CAREER Award 0954243, the Multiscale Systems Research Center and the Defense Advanced Research Projects Agency contract N66001-10-C-2008 to J.M.C., and the Division of Intramural Clinical and Basic Research of the National Institute on Alcohol Abuse and Alcoholism, Marie Curie International Reintegration Grant 239527 and European Research Council STG 243393 to R.M.C.

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Authors

Contributions

A.C.K., X.J., J.D.L., R.M.C. and J.M.C. designed experiments. A.C.K., X.J. and J.D.L. conducted experiments. A.C.K., X.J., R.M.C. and J.M.C. analysed data and wrote the paper.

Corresponding authors

Correspondence to Rui M. Costa or Jose M. Carmena.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary References and Supplementary Figures 1-13. (PDF 1335 kb)

Supplementary Movie 1

This file shows an example of locomotor activity for a control mouse with electrode implantation and used in the BMI experiments. (MOV 5295 kb)

Supplementary Movie 2

This file shows an example of locomotor activity for a RGS9L-Cre/Nr1f/fmouse with electrode implantation and used in the BMI experiments. (MOV 5462 kb)

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Koralek, A., Jin, X., Long II, J. et al. Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature 483, 331–335 (2012). https://doi.org/10.1038/nature10845

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