Distinct patterns of striatal medium spiny neuron activity during the natural sleep-wake cycle.
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.
Mahon
Séverine
S
Institut National de la Santé et de la Recherche Médicale, Unité 667, Collège de France, 75231 Paris Cedex 05, France. severine.mahon@college-de-france.fr
Vautrelle
Nicolas
N
Pezard
Laurent
L
Slaght
Seán J
SJ
Deniau
Jean-Michel
JM
Chouvet
Guy
G
Charpier
Stéphane
S
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D003342:Corpus Striatum / Q000502:physiology*; D004569:Electroencephalography / Q000379:methods; D008297:Male; D009474:Neurons / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D012890:Sleep / Q000502:physiology*; D014851:Wakefulness / Q000502:physiology*