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The Journal of Neuroscience, September 9, 2009, 29(36):11246-11256; doi:10.1523/JNEUROSCI.3260-09.2009

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Behavioral/Systems/Cognitive
Fast Kinetics, High-Frequency Oscillations, and Subprimary Firing Range in Adult Mouse Spinal Motoneurons

Marin Manuel,^1,2 Caroline Iglesias,¹ Maud Donnet,¹ Félix Leroy,¹ C. J. Heckman,^2,3 and Daniel Zytnicki¹

¹Laboratoire de Neurophysique et Physiologie (Centre National pour la Recherche Scientifique, Unité Mixte de Recherche 8119), Université Paris Descartes, Paris 75006, France, and Departments of ²Physiology and ³Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611

Correspondence should be addressed to Marin Manuel, Department of Physiology, Northwestern University Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611. Email: marin.manuel{at}northwestern.edu

The fast contraction time of mouse motor units creates a unique situation in which motoneurons have to fire at low frequencies to produce small forces but also at very high frequency (much higher than in cat or rat motoneurons) to reach the fusion frequency of their motor units. To understand how this problem is solved, we performed intracellular recordings of adult mouse spinal motoneurons and investigated systematically their subthreshold properties and their discharge pattern. We show that mouse motoneurons have a much wider range of firing frequencies than cat and rat motoneurons because of three salient features. First, they have a short membrane time constant. This results in a higher cutoff frequency and a higher resonance frequency, which allow mouse motoneurons to integrate inputs at higher frequencies. Second, their afterhyperpolarization (AHP) is faster, allowing the motoneurons to discharge at a higher rate. Third, motoneurons display high-frequency (100–150 Hz) subthreshold oscillations during the interspike intervals. The fast membrane kinetics greatly favors the appearance of these oscillations, creating a "subprimary range" of firing. In this range, which has never been reported in cat and in rat spinal motoneurons, the oscillations follow the AHP and trigger spiking after a variable delay, allowing a discharge at low frequency but at the expense of an irregular rate.

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Received July 7, 2009; revised July 30, 2009; accepted Aug. 3, 2009.

Correspondence should be addressed to Marin Manuel, Department of Physiology, Northwestern University Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611. Email: marin.manuel{at}northwestern.edu

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