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The Journal of Neuroscience, December 15, 2002, 22(24):10790-10800

Highly Variable Spike Trains Underlie Reproducible Sensorimotor Responses in the Medicinal Leech

Davide Zoccolan, Giulietta Pinato, and Vincent Torre

Scuola Internazionale Superiore di Studi Avanzati and Istituto Nazionale di Fisica della Materia, 34014 Trieste, Italy

The nervous system of the leech is a particularly suitable model to investigate neural coding of sensorimotor responses because it allows both observation of behavior and the simultaneous measurement of a large fraction of its underlying neuronal activity. In this study, we used a combination of multielectrode recordings, videomicroscopy, and computation of the optical flow to investigate the reproducibility of the motor response caused by local mechanical stimulation of the leech skin. We analyzed variability at different levels of processing: mechanosensory neurons, motoneurons, muscle activation, and behavior. Spike trains in mechanosensory neurons were very reproducible, unlike those in motoneurons. The motor response, however, was reproducible because of two distinct biophysical mechanisms. First, leech muscles contract slowly and therefore are poorly sensitive to the jitter of motoneuron spikes. Second, the motor response results from the coactivation of a population of motoneurons firing in a statistically independent way, which reduces the variability of the population firing. These data show that reproducible spike trains are not required to sustain reproducible behaviors and illustrate how the nervous system can cope with unreliable components to produce reliable action.

Key words: sensorimotor responses; optical flow; statistical independence; pooling variability; population coding; reproducibility of muscle contraction

Copyright © 2002 Society for Neuroscience  0270-6474/02/222410790-11$05.00/0


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