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The Journal of Neuroscience, July 14, 2004, 24(28):6315-6325; doi:10.1523/JNEUROSCI.0965-04.2004
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Behavioral/Systems/Cognitive
The Construction of Movement with Behavior-Specific and Behavior-Independent Modules
Jian Jing,
Elizabeth C. Cropper,
Itay Hurwitz, and
Klaudiusz R. Weiss
Department of Physiology and Biophysics, Mount Sinai School of Medicine, New York, New York 10029-6574
Growing evidence suggests that different forms of complex motor acts are constructed through flexible combinations of a small number of modules in interneuronal networks. It remains to be established, however, whether a module simply controls groups of muscles and functions as a computational unit for use in multiple behaviors (behavior independent) or whether a module controls multiple salient features that define one behavior and is used primarily for that behavior (behavior specific). We used the Aplysia feeding motor network to examine the two proposals by studying the functions of identifiable interneurons. We identified three types of motor programs that resemble three types of behaviors that Aplysia produce: biting, swallowing, and rejection. Two ingestive programs (biting, swallowing) are defined by two movement parameters of the feeding apparatus (the radula): one is the same in both programs (phasing of radula closure motoneurons relative to radula protraction-retraction), whereas the other parameter (protraction duration) is different in the two programs. In each program, these two parameters were specified together by an individual neuron, but the neurons in each were different (B40 for biting, B30 for swallowing). These findings support the existence of behavior-specific modules. Furthermore, neuron B51 was found to mediate a phase that can be flexibly added on to both ingestive and egestive-rejection programs, suggesting that B51 may be a behavior-independent module. The functional interpretation of the role played by these modules is supported by the patterns of synaptic connectivity that they make. Thus, both behavior-specific and behavior-independent modules are used to construct complex behaviors.
Key words: module; modular organization; Aplysia; feeding; spinal system; motor programs; movement parameter coding; interneuron; central pattern generator
Received Jan 29, 2004;
revised June 1, 2004;
accepted June 2, 2004.
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