Abstract

Rhythmic locomotor behaviour in animals requires exact timing of muscle activation within the locomotor cycle. In rapidly oscillating motor systems, conventional control strategies may be affected by neural delays, making these strategies inappropriate for precise timing control. In flies, wing control thus requires sensory processing within the peripheral nervous system, circumventing the central brain. The underlying mechanism, with which flies integrate graded depolarization of visual interneurons and spiking proprioceptive feedback for precise muscle activation, is under debate. Based on physiological parameters, we developed a numerical model of spike initiation in flight muscles of a blowfly. The simulated Hodgkin–Huxley neuron reproduces multiple experimental findings and explains on the cellular level how vision might control wing kinematics. Sensory processing by single motoneurons appears to be sufficient for control of muscle power during flight in flies and potentially other flying insects, reducing computational load on the central brain during body posture reflexes and manoeuvring flight.

Highlights

  • Rhythmic locomotor behaviour in animals results from periodic production of muscle mechanical power

  • Several problems for phase control in locomotor systems are associated with synaptic delays and the time needed for spike propagation from sensors to the central brain and locomotor muscles [6,7]

  • This study investigates sensory processing and motor control in an insect that flaps its wings at approximately 150 Hz stroke frequency

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Summary

Introduction

Rhythmic locomotor behaviour in animals results from periodic production of muscle mechanical power. Muscle power typically depends on neural activation frequency, and strongly on the muscle’s spike phase, i.e. the timing of electrical muscle activation within the locomotor cycle [1,2,3]. The latter mechanism provides the nervous system with an additional opportunity to influence motor control and locomotor efficacy. Conventional neural strategies for phase control, may fail in locomotor systems with high oscillatory frequencies of up to approximately 800 Hz [5]. This study investigates sensory processing and motor control in an insect that flaps its wings at approximately 150 Hz stroke frequency

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