Post-embryonic maturation of the C. elegans motor circuit

Abstract

During development, animals can maintain behavioral output even as the underlying circuits structurally remodel. After hatching, C. elegans undergoes substantial motor neuron expansion and synapse re-wiring while the animal continuously moves with an undulatory pattern. To understand how the circuit transitions from its juvenile to mature configuration without disrupting functional output, we reconstructed the C. elegans motor circuit by electron microscopy across larval development. We observed: 1) Embryonic motor neurons transiently interact with the developing post-embryonic motor neurons prior to remodeling of their juvenile wiring; 2) Post-embryonic neurons initiate synapse development with their future partners as their neurites navigate through the juvenile nerve cords; 3) Embryonic and post-embryonic neurons sequentially build structural machinery needed for the adult circuit before the embryonic neurons relinquish their roles to post-embryonic neurons; 4) This transition is repeated region by region along the body in an anterior to posterior sequence, following the birth order of post-embryonic neurons. Through this orchestrated, programmed and gradual rewiring, the motor circuit transforms from asymmetric to symmetric wiring. These maturation strategies support the continuous maintenance of motor patterns as the juvenile circuit develops into the adult configuration. HighlightsO_LIPost-embryonic motor circuit maturation was reconstructed by synapse-resolution serial EM. C_LIO_LIMotor patterns are maintained as the circuit matures from asymmetric to symmetric configuration. C_LIO_LIProgrammed rewiring gradually and sequentially transforms the circuit structure. C_LIO_LIPreparatory and communicative wiring-rewiring allows maturation without functional disruption. C_LI