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J Neurophysiol 83: 232-259, 2000;
0022-3077/00 $5.00
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The Journal of Neurophysiology Vol. 83 No. 1 January 2000, pp. 232-259
Copyright ©2000 by the American Physiological Society

The Neuromuscular Transform Constrains the Production of Functional Rhythmic Behaviors

Vladimir Brezina and Klaudiusz R. Weiss

Department of Physiology and Biophysics and Fishberg Research Center for Neurobiology, Mount Sinai School of Medicine, New York, New York 10029

Brezina, Vladimir and Klaudiusz R. Weiss. The Neuromuscular Transform Constrains the Production of Functional Rhythmic Behaviors. J. Neurophysiol. 83: 232-259, 2000. We continue our study of the properties and the functional role of the neuromuscular transform (NMT). The NMT is an input-output relation that formalizes the processes by which patterns of motor neuron firing are transformed to muscle contractions. Because the NMT acts as a dynamic, nonlinear, and modifiable filter, the transformation is complex. In the preceding paper we developed a framework for analysis of the NMT and identified with it principles by which the NMT transforms different firing patterns to contractions. The ultimate question is functional, however. In sending different firing patterns through the NMT, the nervous system is seeking to command different functional behaviors, with specific contraction requirements. To what extent do the contractions that emerge from the NMT actually satisfy those requirements? In this paper we extend our analysis to address this issue. We define representative behavioral tasks and corresponding measures of performance, for a single neuromuscular unit, for two antagonistic units, and, in a real illustration, for the accessory radula closer (ARC)-opener neuromuscular system of Aplysia. We focus on cyclical, rhythmic behaviors which reveal the underlying principles particularly clearly. We find that, although every pattern of motor neuron firing produces some state of muscle contraction, only a few patterns produce functional behavior, and even fewer produce efficient functional behavior. The functional requirements thus dictate certain patterns to the nervous system. But many desirable functional behaviors are not possible with any pattern. We examine, in particular, how rhythmic behaviors degrade and disintegrate as the nervous system attempts to speed up their cycle frequency. This happens because, with fixed properties, the NMT produces only a limited range of contraction shapes that are kinetically well matched to the firing pattern only on certain time scales. Thus the properties of the NMT constrain and restrict the production of functional behaviors. In the following paper, we see how the constraint may be alleviated and the range of functional behaviors expanded by appropriately tuning the properties of the NMT through neuromuscular plasticity and modulation.




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