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State-dependent hyperpolarization of voltage threshold enhances motoneurone excitability during fictive locomotion in the cat

S. Krawitz, B. Fedirchuk, Y. Dai, L. M. Jordan and D. A. McCrea

1. Experiments were conducted on decerebrate adult cats to examine the effect of brainstem-evoked fictive locomotion on the threshold voltage (V_th) at which action potentials were initiated in hindlimb motoneurones. Measurements of the voltage threshold of the first spike evoked by intracellular injection of depolarizing ramp currents or square pulses were compared during control and fictive locomotor conditions. The sample of motoneurones included flexor and extensor motoneurones, and motoneurones with low and high rheobase currents.

2. In all 38 motoneurones examined, action potentials were initiated at more hyperpolarized membrane potentials during fictive locomotion than in control conditions (mean hyperpolarization -8.0 ± 5.5 mV; range -1.8 to -26.6 mV). Hyperpolarization of V_th occurred immediately at the onset of fictive locomotion and recovered in seconds (typically < 60 s) following the termination of locomotor activity.

3. The V_th of spikes occurring spontaneously without intracellular current injection was also reduced during locomotion.

4. Superimposition of rhythmic depolarizing current pulses on current ramps in the absence of locomotion did not lower V_th to the extent seen during fictive locomotion. We suggest that V_th hyperpolarization results from an as yet undetermined neuromodulatory process operating during locomotion and is not simply the result of the oscillations in membrane potential occurring during locomotion.The hyperpolarization of V_th for action potential initiation during locomotion is a state-dependent increase in motoneurone excitability. This V_th hyperpolarization may be a fundamental process in the generation of motoneurone activity during locomotion and perhaps other motor tasks.

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