Abstract

A central model that describes how behavioral sequences are produced features a neural architecture that readies different movements simultaneously, and a mechanism where prioritized suppression between the movements determines their sequential performance. We previously described a model whereby suppression drives a Drosophila grooming sequence that is induced by simultaneous activation of different sensory pathways that each elicit a distinct movement (Seeds et al., 2014). Here, we confirm this model using transgenic expression to identify and optogenetically activate sensory neurons that elicit specific grooming movements. Simultaneous activation of different sensory pathways elicits a grooming sequence that resembles the naturally induced sequence. Moreover, the sequence proceeds after the sensory excitation is terminated, indicating that a persistent trace of this excitation induces the next grooming movement once the previous one is performed. This reveals a mechanism whereby parallel sensory inputs can be integrated and stored to elicit a delayed and sequential grooming response.

Highlights

  • A major question about nervous system function is how different movements are assembled to form behavioral sequences

  • Our initial goal was to identify GAL4 transgenic lines expressing in sensory neurons across the body, to directly test whether simultaneous activation of these neurons leads to a prioritized grooming response

  • We identified a spGAL4 combination (R31H10-activation domain (AD) ∩ R34E03-DNA binding domain (DBD)) that expressed both in the eye bristle mechanosensory neurons and the same three categories of sensory neurons on the wings and halteres that were expressed in the R30B01-AD ∩ R31H10-DBD combination (Figure 5B)

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Summary

Introduction

A major question about nervous system function is how different movements are assembled to form behavioral sequences. Behavioral competition arises in situations where different mutually exclusive behaviors are appropriate, but they must be performed one at a time (Houghton and Hartley 1995; Redgrave, Prescott, and Gurney 1999) These conflicts can be resolved through the suppression of all but the highest priority behavior, as mollusks do to suppress their mating behavior while feeding Completion of the highest priority movement lifts suppression on movements of lower priority that are subsequently performed according to a new round of competition and suppression This parallel model could drive behaviors across a range of complexity, from the sequential typing of letters on a keyboard in humans to the selection of which behavior to perform first in mollusks (Houghton and Hartley 1995). The identification of examples of simple parallel neural architectures that drive a prioritized selection of movements may inform a broad spectrum of sequential behaviors (Kristan 2014; Jovanic et al 2016)

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