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The Journal of Neuroscience, October 7, 2009, 29(40):12653-12663; doi:10.1523/JNEUROSCI.1554-09.2009

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Behavioral/Systems/Cognitive
Long-Term Modifications in Motor Cortical Dynamics Induced by Intensive Practice

Bjørg E. Kilavik,^1,2 * Sébastien Roux,^1,3 * Adrián Ponce-Alvarez,¹ Joachim Confais,¹ Sonja Grün,² and Alexa Riehle^1,2

¹Institut de Neurosciences Cognitives de la Méditerranée–Centre National de la Recherche Scientifique, Université Aix-Marseille, 13402 Marseille, France, and ²RIKEN Brain Science Institute, Wako-Shi, Saitama 351-0198, Japan, and ³Bernstein Center for Computational Neuroscience, and Neurobiology and Biophysics, Institute of Biology III, Albert-Ludwigs-Universität, 79110 Freiburg, Germany

Correspondence should be addressed to Dr. Alexa Riehle, Institut de Neurosciences Cognitives de la Méditerranée–Centre National de la Recherche Scientifique, 31 chemin Joseph Aiguier, 13402 Marseille Cedex 20, France. Email: alexa.riehle{at}incm.cnrs-mrs.fr

The planning of goal-directed movements requires sensory, temporal, and contextual information to be combined. Sensorimotor functions are embedded in large neuronal networks, but it is unclear how networks organize their activity in space and time to optimize behavior. Temporal coordination of activity in many neurons within a network, e.g., spike synchrony, might be complementary to a firing rate code, allowing efficient computation with overall less population activity. Here we asked the question whether intensive practice induces long-term modifications in the temporal structure of synchrony and firing rate at the population level. Three monkeys were trained in a delayed pointing task in which the selection of movement direction depended on correct time estimation. The synchronous firing among pairs of simultaneously recorded neurons in motor cortex was analyzed using the "unitary event" technique. The evolution of synchrony in both time, within the trial, and temporal precision was then quantified at the level of an entire population of neurons by using two different quantification techniques and compared with the population firing rate. We find that the task timing was represented in the temporal structure of significant spike synchronization at the population level. During practice, the temporal structure of synchrony was shaped, with synchrony becoming stronger and more localized in time during late experimental sessions, in parallel with an improvement in behavioral performance. Concurrently, the average population firing rate mainly decreased. Performance optimization through practice might therefore be achieved by boosting the computational contribution of spike synchrony, allowing an overall reduction in population activity.

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Received April 1, 2009; revised Aug. 14, 2009; accepted Aug. 24, 2009.

Correspondence should be addressed to Dr. Alexa Riehle, Institut de Neurosciences Cognitives de la Méditerranée–Centre National de la Recherche Scientifique, 31 chemin Joseph Aiguier, 13402 Marseille Cedex 20, France. Email: alexa.riehle{at}incm.cnrs-mrs.fr

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