Distributed Motor Pattern Underlying Whole-Body Shortening in the Medicinal Leech

Abstract

Whole-body shortening was studied in the leech, Hirudo medicinalis, by a combination of videomicroscopy and multielectrode recordings. Video microscopy was used to monitor the animal behavior and muscle contraction. Eight suction pipettes were used to obtain simultaneous electrical recordings from fine roots emerging from ganglia. This vital escape reaction was rather reproducible. The coefficient of variation of the animal contraction during whole-body shortening was between 0.2 and 0.3. The great majority of all leech longitudinal motoneurons were activated during this escape reaction, in particular motoneurons 3, 4, 5, 8, 107, 108, and L. The firing pattern of all these motoneurons was poorly reproducible from trial to trial, and the coefficient of variation of their firing varied between 0.3 and 1.5 for different motoneurons. The electrical activity of pairs of coactivated motoneurons did not show any sign of correlation over a time window of 100 ms. Only the left and right motoneurons L in the same ganglion had a correlated firing pattern, resulting from their strong electrical coupling. As a consequence of the low correlation between coactivated motoneurons, the global electrical activity during whole-body shortening became reproducible with a coefficient of variation below 0.3 during maximal contraction. These results indicate that whole-body shortening is mediated by the coactivation of a large fraction of all leech motoneurons, i.e., it is a distributed process, and that coactivated motoneurons exhibit a significant statistical independence. Probably due to this statistical independence this vital escape reaction is smooth and reproducible.