Development of the Motor Periphery is the Rate-Limiting Step in the Ontogeny of the Vestibulo-ocular Reflex

Abstract

Sensory deprivation reshapes developing neural circuits, and sensory feedback adjusts the strength of reflexive behaviors throughout life. Sensory development might therefore limit the rate with which behaviors mature, but the complexity of most sensorimotor circuits preclude identifying this fundamental constraint. Here we compared the functional development of components of the vertebrate vestibulo-ocular reflex circuit that stabilizes gaze. We found that vestibular interneuron responses to body tilt sensation developed well before behavioral performance peaked, even without motor neuron-derived feedback. Motor neuron responses developed similarly. Instead, the ontogeny of behavior matched the rate of neuromuscular junction development. When sensation was delayed until after the neuromuscular junction developed, behavioral performance was immediately strong. The matching timecourse and ability to determine behavior establish the development of the neuromuscular junction, and not sensory-derived information, as the rate-limiting process for an ancient and evolutionarily-conserved neural circuit.