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.

Phase response properties of half-center oscillators

“…We note, however, that the second order PRCs of the detailed model closely resemble the first order PRCs, indicating there are minimal higher order effects, as is the case in our Morris-Lecar-based model. Nadim et al (2011) measured a PRC for the central pattern generator (CPG) of the crustacean pyloric circuit, and Smarandache et al (2009) measured the CPG underlying a segment of the crayfish swimmeret system. Both of these circuits are composed, at least partially, of HCO structures.…”

“…PRCs for individual neurons and neuronal networks can be obtained directly by applying brief current pulses at many different times in the oscillator's cycle and measuring the subsequent change in timing of the next spike (e.g., Mancilla et al 2007;Smarandache et al 2009;Netoff et al 2012). PRCs for mathematical models can also be computed by solving the adjoint equations for the full model equations linearized around the system's T-periodic limit cycle.…”

The Swimmeret System of Crayfish: A Practical Guide for the Dissection of the Nerve Cord and Extracellular Recordings of the Motor Pattern

“…In this system the neuronal components [8][9][10] of the local microcircuits are identified and additionally the coordinating network is known in cellular detail 11,14,15 . The results drawn from the experiments performed with extracellular recordings, allow already predictions for mathematical models and for roboticists.…”

“…In the swimmeret system such coordination is established by the coordinating microcircuit which ensures that limbs are active at correct times. This microcircuit is built by three identified neurons in each segment [11][12][13][14][15] . This protocol provides for the first time a step-by-step dissection guide to isolate the chain of ganglia (T4 to A6, Figure 1).…”

Nitric oxide modulates a swimmeret beating rhythm in the crayfish

“…Rhythmic bursts of motor neurone spikes are generated by chains of serially repeated pairs of CPGs, one in each hemiganglion, that are interconnected both bilaterally across the midline and across abdominal segments Wiersma and Ikeda, 1964). The local pattern-generating circuits, including nonspiking local interneurones, and the pathways for intersegmental coordination have been well characterized by the detailed studies of Mulloney and colleagues (Mulloney and Hall, 2000;Mulloney and Hall, 2003;Mulloney and Hall, 2007;Mulloney et al, 2006;Paul and Mulloney, 1985;Smarandache et al, 2009;SmarandacheWellmann et al, 2013;Smarandache-Wellmann et al, 2014; for a review, see Mulloney and Smarandache, 2010;Mulloney and Smarandache-Wellmann, 2012). There is, however, almost no evidence that the rhythmic beating activity of the swimmeret motor neurones is affected by NO.…”