The Journal of Neuroscience, November 21, 2007, 27(47):12977-12988; doi:10.1523/JNEUROSCI.3299-07.2007
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Behavioral/Systems/Cognitive
Resonant or Not, Two Amplification Modes of Proprioceptive Inputs by Persistent Inward Currents in Spinal Motoneurons
Marin Manuel,
Claude Meunier,
Maud Donnet, and
Daniel Zytnicki
Laboratoire de Neurophysique et Physiologie, Centre National de la Recherche Scientifique/Université Paris-Descartes, Unite Mixte de Recherche 8119, 75270 Paris Cedex 06, France
Correspondence should be addressed to Dr. Marin Manuel, Laboratoire de Neurophysique et Physiologie, Unité Mixte de Recherche 8119, Centre National de la Recherche Scientifique/Université Paris-Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. Email: marin.manuel{at}univ-paris5.fr
Why do motoneurons possess two persistent inward currents (PICs), a fast sodium current and a slow calcium current? To answer this question, we replaced the natural PICs with dynamic clamp-imposed artificial PICs at the soma of spinal motoneurons of anesthetized cats. We investigated how PICs with different kinetics (1–100 ms) amplify proprioceptive inputs. We showed that their action depends on the presence or absence of a resonance created by the Ih current. In resonant motoneurons, a fast PIC enhances the resonance and amplifies the dynamic component of Ia inputs elicited by ramp-and-hold muscle stretches. This facilitates the recruitment of these motoneurons, which likely innervate fast contracting motor units developing large forces, e.g., to restore balance or produce ballistic movements. In nonresonant motoneurons, in contrast, a fast PIC easily triggers plateau potentials, which leads to a dramatic amplification of the static component of Ia inputs. This likely facilitates the recruitment of these motoneurons, innervating mostly slowly contracting and fatigue-resistant motor units, during postural activities. Finally, a slow PIC may switch a resonant motoneuron to nonresonant by counterbalancing Ih, thus changing the action of the fast PIC. A modeling study shows that Ih needs to be located on the dendrites to create the resonance, and it predicts that dendritic PICs amplify synaptic input in the same manner as somatic PICs.
Key words: proprioception; subthreshold resonance; persistent sodium current; persistent calcium current; hyperpolarization activated mixed cationic current; dynamic clamp
Received July 20, 2007;
revised Sept. 14, 2007;
accepted Oct. 6, 2007.
Correspondence should be addressed to Dr. Marin Manuel, Laboratoire de Neurophysique et Physiologie, Unité Mixte de Recherche 8119, Centre National de la Recherche Scientifique/Université Paris-Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. Email: marin.manuel{at}univ-paris5.fr
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