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The Journal of Neuroscience, January 26, 2005, 25(4):923-935; doi:10.1523/JNEUROSCI.2301-04.2005

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Behavioral/Systems/Cognitive
Mechanisms of Rhythm Generation in a Spinal Locomotor Network Deprived of Crossed Connections: The Lamprey Hemicord

Lorenzo Cangiano and Sten Grillner

Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, SE-17177 Stockholm, Sweden

The spinal network coordinating locomotion in the lamprey serves as a model system, in which it has been possible to elucidate connectivity and cellular mechanisms using the isolated spinal cord. Locomotor burst activity alternates between the left and right side of a segment through reciprocal inhibition. We have recently shown that the burst generation itself in a hemisegment does not require inhibitory mechanisms. The focus of this study is the intrinsic operation of this hemisegmental burst-generating component of the locomotor network.

Brief electrical stimulation (0.3 s) of the hemicord evokes long-lasting bouts (>2 min) of bursts (2-15 Hz) in the mid to high-frequency range of locomotion. Bout release is an all-or-none phenomenon requiring a threshold intensity of stimulation and glutamatergic transmission within a population of excitatory interneurons, with axons extending over several segments. The progressive activity-dependent decrease in burst frequency that takes place during a bout is followed by a slow recovery process lasting >20 min. Intracellular recordings of single motoneurons, excitatory interneurons, and inhibitory interneurons show that locomotor bouts, in general, are accompanied by a marked depolarization. Membrane potential oscillations and spikes occur in phase with the ventral root (VR) bursts. Active motoneurons and interneurons fire one spike per VR burst, as also confirmed by axonal recordings. Thus, the reciprocal inhibition between opposite hemisegments in the intact cord not only ensures left-right alternation and lowers the locomotor frequency but also promotes a shift from single to multiple action potentials per cycle in network neurons.

Key words: locomotion; central pattern generator; spinal; lamprey; rhythm; synchrony

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Received June 11, 2004; revised December 2, 2004; accepted December 4, 2004.

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