Pattern-Generating Role for Motoneurons in a Rhythmically Active Neuronal Network

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Abstract
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.