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The Journal of Neuroscience, June 28, 2006, 26(26):7056-7070; doi:10.1523/JNEUROSCI.5277-05.2006

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Behavioral/Systems/Cognitive
Variability of Motor Neuron Spike Timing Maintains and Shapes Contractions of the Accessory Radula Closer Muscle of Aplysia

Yuriy Zhurov and Vladimir Brezina

Fishberg Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029

Correspondence should be addressed to Dr. Vladimir Brezina, Department of Neuroscience, Box 1065, Mount Sinai School of Medicine, 1 Gustave L. Levy Place, New York, NY 10029. Email: vladimir.brezina{at}mssm.edu

The accessory radula closer (ARC) muscle of Aplysia has long been studied as a typical "slow" muscle, one that would be assumed to respond only to the overall, integrated spike rate of its motor neurons, B15 and B16. The precise timing of the individual spikes should not much matter. However, but real B15 and B16 spike patterns recorded in vivo show great variability that extends down to the timing of individual spikes. By replaying these real as well as artificially constructed spike patterns into ARC muscles in vitro, we examined the consequences of this spike-level variability for contraction. Replaying the same pattern several times reproduces precisely the same contraction shape: the B15/B16–ARC neuromuscular transform is deterministic. However, varying the timing of the spikes produces very different contraction shapes and amplitudes. The transform in fact operates at an interface between "fast" and "slow" regimens. It is fast enough that the timing of individual spikes greatly influences the detailed contraction shape. At the same time, slow integration of the spike pattern through the nonlinear transform allows the variable spike timing to determine also the overall contraction amplitude. Indeed, the variability appears to be necessary to maintain the contraction amplitude at a robust level. This phenomenon is tuned by neuromodulators that tune the speed and nonlinearity of the transform. Thus, the variable timing of individual spikes does matter, in at least two, functionally significant ways, in this "slow" neuromuscular system.

Key words: spike timing; neural code; neuromodulators; neuromuscular system; motor control; feeding behavior

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Received Dec. 9, 2005; revised May 9, 2006; accepted May 23, 2006.

Correspondence should be addressed to Dr. Vladimir Brezina, Department of Neuroscience, Box 1065, Mount Sinai School of Medicine, 1 Gustave L. Levy Place, New York, NY 10029. Email: vladimir.brezina{at}mssm.edu

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