SUMMARY Sensory input is pervasive among motor networks and continuously adapts motor patterns to changing circumstances. To elucidate common principles of sensorimotor integration, it is beneficial to characterize sensory influences on motor network operation and compare these influences between species. To facilitate such comparison, we have studied the influence of the anterior gastric receptor (AGR) – a proprioceptor that has been characterized in detail in two lobster species – on the pyloric (filtering of food) and gastric mill (chewing of food) motor patterns in the crab Cancer pagurus. AGR has a bipolar cell body in the stomatogastric ganglion; it was activated by tension increase in gastric mill powerstroke muscles. While two spike initiation zones accounted for its spontaneous activity, active membrane properties (sag potentials, spike frequency adaptation) contributed to the AGR response to current injections. When activated, AGR diminished spike activities in two pyloric motor neurons and prolonged the pyloric cycle period. Furthermore, AGR excited gastric mill protractor neurons, inhibited the retractor neuron and evoked phase-independent resetting of the gastric mill rhythm. Repetitive spike trains entrained the rhythm to both longer and shorter cycle periods. All AGR actions seemed to be mediated via at least two premotor projection neurons in the spatially distant commissural ganglia. The response of the gastric mill neurons was independent of AGR firing frequency. Our results suggest that homologous proprioceptors can elicit similar effects on motor patterns while utilizing different mechanisms. This work thus provides an initial framework for future studies to determine underlying common principles.
Synchronization of distributed neural circuits is required for many behavioral tasks, but the mechanisms that coordinate these circuits are largely unknown. The modular local circuits that control crayfish swimmerets are distributed in four segments of the CNS, but when the swimmeret system is active their outputs are synchronized with a stable intersegmental phase difference of 0.25, an example of metachronal synchronization (Izhikevich, 2007). In each module, coordinating neurons encode detailed information about each cycle of the module's motor output as bursts of spikes, and their axons conduct this information to targets in other segments. This information is both necessary and sufficient for normal intersegmental coordination. In a comprehensive set of recordings, we mapped the synaptic connections of two types of coordinating neurons onto their common target neurons in other segments. Both types of coordinating axons caused large, brief EPSPs in their targets. The shape indices of these EPSPs are tuned to transmit the information from each axon precisely. In each target neuron's own module, these bursts of EPSPs modified the phase of the module's motor output. Each axon made its strongest synapse onto the target neuron in the nearest neighboring segment. Its synapses onto homologous targets in more remote segments were progressively weaker. Each target neuron decodes information from several coordinating axons, and the strengths of their synapses differ systematically. These differences in synaptic strength weight information from each segment differently, which might account for features of the system's characteristic metachronal synchronization.
Sensorimotor integration is known to occur at the level of motor circuits as well as in upstream interneurons that regulate motor activity. Here we show, using the crab stomatogastric nervous system (STNS) as a model, that different sensory systems affect the same set of projection neurons. However, they have qualitatively different effects on their activities (excitation vs. inhibition), and these differences contribute to the selection of motor patterns from multifunctional circuits. We compare the actions of the proprioceptive anterior gastric receptor (AGR) and the inferior ventricular (IV) neurons, which relay chemosensory information from the brain to the STNS, on modulatory commissural neurons 1 and 5 (MCN1 and MCN5) and commissural projection neuron 2 (CPN2) and their resulting actions on the gastric mill central pattern generating circuit in the stomatogastric ganglion. When stimulated, AGR and the IV neurons affect all three projection neurons but elicit distinct gastric mill rhythms. The effects of both sensory pathways on the projection neurons differ in the type of excitation provided to CPN2 and MCN5 (electrical vs. chemical) and the effect on MCN1 (direct inhibition by AGR vs. polysynaptic excitation by the IV neurons). The latter is functionally important because a restoration of MCN1 activity during the AGR rhythm made it more similar to that elicited by IV neuron stimulation. Our results thus support the hypothesis that sensory pathways activate different combinations of projection neurons to select distinct outputs from the same neuronal circuit.
intact animals and in the isolated nervous system showed a great variability in firing frequency and temporal distribution of motor neuron bursts. Train stimulations with various stimulus frequencies (5·Hz, 10·Hz, 20·Hz) and inter-train intervals (2·s, 4·s, 8·s, 16·s, 32·s) revealed that augmentation acted in addition to facilitation. Augmentation increased muscle EJPs during stimulations with inter-train intervals of 16·s or less. The effects of augmentation increased with shorter inter-train intervals, but were independent of stimulus frequency.Augmentation also contributed to the electrical response of the muscle during gastric mill rhythms, which were obtained in vitro and in vivo, and was also reflected by an increase of muscle force and the slope of force development during repetitive train stimulation. We conclude that the augmentation of EJPs at the neuromuscular junction tunes the muscle response to support force production during rhythmic motor patterns.
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.
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