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Science 26 November 1999:
Vol. 286. no. 5445, pp. 1745 - 1749
DOI: 10.1126/science.286.5445.1745
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Reports

Building Neural Representations of Habits

Mandar S. Jog, 1* Yasuo Kubota, 2* Christopher I. Connolly, 3 Viveka Hillegaart, 4 Ann M. Graybiel 2dagger

Memories for habits and skills ("implicit or procedural memory") and memories for facts ("explicit or episodic memory") are built up in different brain systems and are vulnerable to different neurodegenerative disorders in humans. So that the striatum-based mechanisms underlying habit formation could be studied, chronic recordings from ensembles of striatal neurons were made with multiple tetrodes as rats learned a T-maze procedural task. Large and widely distributed changes in the neuronal activity patterns occurred in the sensorimotor striatum during behavioral acquisition, culminating in task-related activity emphasizing the beginning and end of the automatized procedure. The new ensemble patterns remained stable during weeks of subsequent performance of the same task. These results suggest that the encoding of action in the sensorimotor striatum undergoes dynamic reorganization as habit learning proceeds.

1 London Health Sciences Center, London, Ontario N6A 5A5, Canada.
2 Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
3 SRI International, 333 Ravenswood Avenue, Menlo Park, CA 94025, USA.
4 Department of Physiology and Pharmacology, Karolinska Institute, 17177 Stockholm, Sweden.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: graybiel{at}mit.edu

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   Abstract »    Full Text »
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