Coordination of Rhythmic Motor Activity by Gradients of Synaptic Strength in a Neural Circuit That Couples Modular Neural Oscillators

Abstract

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.