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The Journal of Neuroscience, May 15, 1998, 18(10):3669-3688
Pattern-Generating Role for Motoneurons in a Rhythmically Active
Neuronal Network
Kevin
Staras,
György
Kemenes, and
Paul R.
Benjamin
Sussex Centre for Neuroscience, School of Biological Sciences,
University of Sussex, Falmer, Brighton, United Kingdom BN1 9QG
The role of motoneurons in central motor pattern generation was
investigated in the feeding system of the pond snail Lymnaea stagnalis, an important invertebrate model of behavioral rhythm generation. The neuronal network responsible for the three-phase feeding motor program (fictive feeding) has been characterized extensively and divided into populations of central pattern generator (CPG) interneurons, modulatory interneurons, and motoneurons. A
previous model of the feeding system considered that the motoneurons were passive followers of CPG interneuronal activity. Here we present
new, detailed physiological evidence that motoneurons that innervate
the musculature of the feeding apparatus have significant electrotonic
motoneuron interneuron connections, mainly confined to cells active
in the same phase of the feeding cycle (protraction, rasp, or swallow).
This suggested that the motoneurons participate in rhythm generation.
This was assessed by manipulating firing activity in the motoneurons
during maintained fictive feeding rhythms. Experiments showed that
motoneurons contribute to the maintenance and phase setting of the
feeding rhythm and provide an efficient system for phase-locking muscle
activity with central neural activity. These data indicate that the
distinction between motoneurons and interneurons in a complex CNS
network like that involved in snail feeding is no longer justified and
that both cell types are important in motor pattern generation. This is a distributed type of organization likely to be a general
characteristic of CNS circuitries that produce rhythmic motor
behavior.
Key words:
motoneuron; pattern generation; feeding system; molluscs; Lymnaea; electrotonic coupling; feedback
Copyright © 1998 Society for Neuroscience 0270-6474/98/18103669-20$05.00/0
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