Proprioceptive feedback modulates coordinating information in a system of segmentally distributed microcircuits.

The system of modular neural circuits that controls crustacean swimmerets drives a metachronal sequence of power-stroke (PS, retraction) and return-stroke (RS, protraction) movements that propels the animal forward efficiently. These neural modules are synchronized by an intersegmental coordinating circuit that imposes characteristic phase differences between these modules. Using a semi-intact preparation that left one swimmeret attached to an otherwise isolated central nervous system (CNS) of the crayfish, Pacifastacus leniusculus, we investigated how the rhythmic activity of this system responded to imposed movements.

Coordination of rhythmic motor activity by gradients of synaptic strength in a neural circuit that couples modular neural oscillators.

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).

Local and intersegmental interactions of coordinating neurons and local circuits in the swimmeret system.

During forward swimming, periodic movements of swimmerets on different segments of the crayfish abdomen progress from back to front with the same period. Information encoded as bursts of spikes by coordinating neurons in each segmental ganglion is necessary for this coherent organization. This information is conducted to targets in other ganglia.

Not by spikes alone: responses of coordinating neurons and the swimmeret system to local differences in excitation.

Swimmeret coordinating neurons in the crayfish CNS collectively encode a detailed cycle-by-cycle report on features of the motor output to each swimmeret. This information coordinates the motor output that drives swimmeret movements. To see how coordinating neurons responded to forced changes in intersegmental phase, we used a split-bath, repeated-measures experimental design to expose different regions of isolated abdominal nerve cords to different levels of excitation.

Bursts of information: coordinating interneurons encode multiple parameters of a periodic motor pattern.

The limbs on different segments of the crayfish abdomen that drive forward swimming are directly controlled by modular pattern-generating circuits. These circuits are linked together by axons of identified coordinating interneurons. We described the distributions of these neurons in each abdominal ganglion and monitored their firing during expression of the swimming motor pattern.

Local commissural interneurons integrate information from intersegmental coordinating interneurons.

The information that coordinates movements of swimmerets on different segments of the crayfish abdomen is conducted by interneurons that originate in each abdominal ganglion. These interneurons project axons to neighboring ganglia and beyond. To discover the anatomy of these axons in their target ganglia, we used Neurobiotin and dextran-Texas Red microelectrodes to fill them near their targets.

Architectonics of crayfish ganglia.

The central nervous system of crayfish consists of a chain of segmental ganglia that are linked by cables of intersegmental axons. Each ganglion contains a highly-ordered core of longitudinal tracts, vertical tracts, commissures, and synaptic neuropils. We review from a technical perspective the history of the description of these ganglia, and recognize four episodes of progress.