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The Journal of Neuroscience, November 23, 2005, 25(47):10941-10951; doi:10.1523/JNEUROSCI.0164-05.2005

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Behavioral/Systems/Cognitive
Emerging Patterns of Neuronal Responses in Supplementary and Primary Motor Areas during Sensorimotor Adaptation

Rony Paz,^1,2 Chen Natan,¹ Thomas Boraud,³ Hagai Bergman,^1,2 and Eilon Vaadia^1,2

¹Department of Physiology, Hadassah Medical School, and ²The Interdisciplinary Center for Neural Computation, The Hebrew University, Jerusalem 91120, Israel, and ³Laboratoire de Neurophysiologie, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5543, Université Victor Segalen, 33076 Bordeaux, France

Acquisition and retention of sensorimotor skills have been extensively investigated psychophysically, but little is known about the underlying neuronal mechanisms. Here we examine the evolution of neural activity associated with adaptation to new kinematic tasks in two cortical areas: the caudal supplementary motor area (SMA proper), and the primary motor cortex (MI). We investigate the hypothesis that adaptation starts at premotor areas, i.e., higher in the hierarchy of computation, until a stable representation is formed in primary areas. In accordance with previous studies, we found that adaptation can be characterized by two phases: an early phase that is accompanied by fast and substantial reduction of errors, followed by a late phase with slower and more moderate improvements in behavior. We used unsupervised clustering to separate the activity of the single cells into groups of cells with similar response patterns, under the assumption that each such subpopulation forms a functional unit. We specifically observed the number of clusters in each cortical area during early and late phases of the adaptation and found that the number of clusters is higher in the SMA during early phases of adaptation. In contrast, a higher number of clusters was observed in MI only during late phases. Our results suggest a new approach to analyze responses of large populations of neurons and use it to show a hierarchy of dynamic reorganization of functional groups during adaptation.

Key words: motor learning; visuomotor rotations; unsupervised clustering; motor cortex; plasticity; extracellular; monkeys

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Received Sep 28, 2004; revised September 13, 2005; accepted October 16, 2005.

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