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

TL;DR

This study shows how proprioceptive feedback from limb retraction influences neural coordination and phase timing in segmentally-distributed microcircuits controlling crustacean swimmerets, revealing rapid, reversible modulation of motor patterns.

Contribution

It demonstrates that proprioceptive feedback modulates intersegmental coordination by altering efference copies and burst timing in a crustacean neural system, a novel insight into sensorimotor integration.

Findings

Retraction weakens Ps bursts and strengthens Rs bursts.

Efference copies change in strength and timing with limb movement.

Changes are quickly reversed upon limb release.

Abstract

The system of modular neural circuits that controls crustacean swimmerets drives a metachronal sequence of power-stroke and return-stroke 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 crayfish central nervous system of the crayfish, 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 coordinating axons. These changes in strength and timing of 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.