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. We recorded extracellularly from the PS and RS nerves that innervated the attached limb and from coordinating axons that encode efference copies of the periodic bursts in PS and RS axons. Simultaneously, we recorded from homologous nerves in more anterior and posterior segments. Maintained retractions did not affect cycle period but promptly weakened PS bursts, strengthened RS bursts, and caused corresponding changes in the strength and timing of efference copies in the module's coordinating axons. Changes in these efference copies then caused changes in the phase and duration, but not the strength, of PS bursts in modules controlling neighboring swimmerets. These changes were promptly reversed when the limb was released. Each swimmeret is innervated by two nonspiking stretch receptors (NSSRs) that depolarize when the limb is retracted. Voltage clamp of an NSSR changed the durations and strengths of bursts in PS and RS axons innervating the same limb and caused corresponding changes in the efference copies of this motor output