Mechanisms of Coordination in Distributed Neural Circuits: Decoding and Integration of Coordinating Information

Abstract

We describe the synaptic connections through which information required to coordinate limb movements reaches the modular microcircuits that control individual limbs on different abdominal segments of the crayfish, Pacifastacus leniusculus. In each segmental ganglion, a local commissural interneuron, ComInt 1, integrates information about other limbs and transmits it to one microcircuit. Five types of nonspiking local interneurons are components of each microcircuit's pattern-generating kernel (Smarandache-Wellmann et al., 2013). We demonstrate here, using paired microelectrode recordings, that the pathway through which information reaches this kernel is an electrical synapse between ComInt 1 and one of these five types, an IRSh interneuron. Using single-electrode voltage clamp, we show that brief changes of ComInt 1's membrane potential affect the timing of its microcircuit's motor output. Changing ComInt 1's membrane potential also changes the phase, duration, and strengths of bursts of spikes in its microcircuit's motor neurons and corresponding changes in its efferent coordinating neurons that project to other ganglia. These effects on coordinating neurons cause changes in the phases of motor output from other microcircuits in those distant ganglia. ComInt 1s function as hub neurons in the intersegmental circuit that synchronizes distributed microcircuits. The synapse between each ComInt 1 and its microcircuit's IRSh neuron completes a five synapse pathway in which analog information is encoded as a digital signal by efference-copy neurons and decoded from digital to analog form by ComInt 1. The synaptic organization of this pathway provides a cellular explanation of this nervous system's key dynamic properties.