Abstract

Neuronal circuits are formed according to a genetically predetermined program and then reconstructed in an experience-dependent manner. While the existence of experience-dependent plasticity has been demonstrated for the visual and other sensory systems, it remains unknown whether this is also the case for motor systems. Here we examined the effects of eliminating sensory inputs on the development of peristaltic movements in Drosophila embryos and larvae. The peristalsis is initially slow and uncoordinated, but gradually develops into a mature pattern during late embryonic stages. We tested whether inhibiting the transmission of specific sensory neurons during this period would have lasting effects on the properties of the sensorimotor circuits. We applied Shibire-mediated inhibition for six hours during embryonic development (15–21 h after egg laying [AEL]) and studied its effects on peristalsis in the mature second- and third-instar larvae. We found that inhibition of chordotonal organs, but not multidendritic neurons, led to a lasting decrease in the speed of larval locomotion. To narrow down the sensitive period, we applied shorter inhibition at various embryonic and larval stages and found that two-hour inhibition during 16–20 h AEL, but not at earlier or later stages, was sufficient to cause the effect. These results suggest that neural activity mediated by specific sensory neurons is involved in the maturation of sensorimotor circuits in Drosophila and that there is a critical period for this plastic change. Consistent with a role of chordotonal neurons in sensory feedback, these neurons were activated during larval peristalsis and acute inhibition of their activity decreased the speed of larval locomotion.

Highlights

  • Neural control of almost all rhythmic behaviors, such as walking, chewing and swimming, are thought to be generated by neural circuits called central pattern generators (CPGs)

  • A previous study has shown that a maximum level of inhibition of md neurons can be achieved with 109(2)80-GAL4, suggesting that this GAL4 line drives expression in all or most of the md sensory feedback neurons

  • Modifications are mediated by sensory feedback about the current status of the locomotor organs and their interaction with the environment; this information is transmitted to the central nervous system

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Summary

Introduction

Neural control of almost all rhythmic behaviors, such as walking, chewing and swimming, are thought to be generated by neural circuits called central pattern generators (CPGs). CPGs are networks of neurons that produce rhythmic motor outputs without depending on sensory inputs [1,2]. From the beginning of the last century, CPGs have been found in many kinds of animals and are shown to play critical roles in motor generation. Sensory signals from muscles and other body regions often alter the pattern of CPG activity. Sensory feedback may help to generate a functional locomotive pattern by adapting an animal’s movements to its environmental demands. Sensory feedback is not necessary for generating the rhythms, it may play an important role in shaping the motor patterns

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