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The Journal of Neuroscience, November 29, 2006, 26(48):12587-12595; doi:10.1523/JNEUROSCI.3987-06.2006

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Behavioral/Systems/Cognitive
Distinct Patterns of Striatal Medium Spiny Neuron Activity during the Natural Sleep–Wake Cycle

Séverine Mahon,^1 * Nicolas Vautrelle,^2,3 * Laurent Pezard,^4,5 Seán J. Slaght,⁶ Jean-Michel Deniau,^1,7 Guy Chouvet,^2,8 and Stéphane Charpier^1,7

¹Institut National de la Santé et de la Recherche Médicale, Unité 667, Collège de France, 75231 Paris Cedex 05, France, ²Laboratoire de Neuropharmacologie et de Neurochimie, Equipe d'accueil 512, Institut des Sciences Pharmaceutiques et Biologiques, Université Claude Bernard Lyon 1, 69373 Lyon, France, ³Departamento de Biofisica, Instituto de Fisiologia Celular, Universidad Nacional Autonoma de Mexico, Mexico City DF, 04510 Mexico, ⁴Centre National de la Recherche Scientifique–Unité Propre de Recherche 640, Hôpital de la Salpêtrière, 75651 Paris Cedex 13, France, ⁵Université René Descartes, 92774 Boulogne-Billancourt Cedex, France, ⁶North Middlesex University Hospital, London N18 1QX, United Kingdom, ⁷Université Pierre et Marie Curie, 75005 Paris, France, and ⁸Institut National de la Santé et de la Recherche Médicale, Unité 704, Université Joseph Fourier, 38041 Grenoble, France

Correspondence should be addressed to Séverine Mahon, Institut National de la Santé et de la Recherche Médicale, Unité 667, Collège de France, 75231 Paris Cedex 05, France. Email: severine.mahon{at}college-de-france.fr

Striatal medium-sized spiny neurons (MSNs) integrate and convey information from the cerebral cortex to the output nuclei of the basal ganglia. Intracellular recordings from anesthetized animals show that MSNs undergo spontaneous transitions between hyperpolarized and depolarized states. State transitions, regarded as necessary for eliciting action potential firing in MSNs, are thought to control basal ganglia function by shaping striatal output. Here, we use an anesthetic-free rat preparation to show that the intracellular activity of MSNs is not stereotyped and depends critically on vigilance state. During slow-wave sleep, much as during anesthesia, MSNs displayed rhythmic step-like membrane potential shifts, correlated with cortical field potentials. However, wakefulness was associated with a completely different pattern of temporally disorganized depolarizing synaptic events of variable amplitude. Transitions from slow-wave sleep to wakefulness converted striatal discharge from a cyclic brisk firing to an irregular pattern of action potentials. These findings illuminate different capabilities of information processing in basal ganglia networks, suggesting in particular that a novel style of striatal computation is associated with the waking state.

Key words: striatum; electroencephalogram; intracellular recordings; up and down states; slow-wave sleep; wakefulness

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Received Sept. 13, 2006; revised Oct. 12, 2006; accepted Oct. 26, 2006.

Correspondence should be addressed to Séverine Mahon, Institut National de la Santé et de la Recherche Médicale, Unité 667, Collège de France, 75231 Paris Cedex 05, France. Email: severine.mahon{at}college-de-france.fr

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