Regulation of motor pattern frequency by reversals in proprioceptive feedback

Proprioceptive sensory feedback has important functions for motor pattern generation in which phasic negative and positive feedback is used to coordinate neural and musculoskeletal dynamics. Whether and how feedback sign regulates the motor patterns in behaviorally relevant closed-loop conditions has not been fully elucidated. We characterized the feedback provided by the anterior gastric receptor (AGR), a muscle tendon organ in the stomatogastric nervous system of the crab Cancer pagurus, to the gastric mill motor pattern in intact animals. AGR innervates the protractor muscles and was activated either during the protraction or retraction phase of the rhythm. Experiments with neuromuscular preparations imply that this was due to isometric contractions of the protractor muscles and their passive stretch by the antagonistic retractor muscles. As AGR excited the protractors and inhibited the retractors independently of the timing of its activation, the timing switch changed AGR feedback from positive to negative. We tested the effects of this change in feedback sign on the motor pattern in the isolated nervous system by activating AGR at the corresponding phases of the rhythm, using intracellular current injection. When AGR was activated during the protractor phase and provided positive feedback, it prolonged the burst activities of protractor and retractor neurons and slowed ongoing rhythms. When activated during the retraction phase and thus provided negative feedback, burst durations decreased and the rhythm cycle frequency increased. Our study thus shows that the cycle frequency of centrally generated activity patterns can be regulated by switching the sign of phasic proprioceptive feedback.