Identifying neural substrates of competitive interactions and sequence transitions during mechanosensory responses in Drosophila.

Jean-Baptiste Masson,Marta Zlatic,Tihana Jovanic,François Laurent,Albert Cardona,Nicolas Skatchkovsky,Chloé Barré,Aravinthan Samuel

doi:10.1371/journal.pgen.1008589

Abstract

Nervous systems have the ability to select appropriate actions and action sequences in response to sensory cues. The circuit mechanisms by which nervous systems achieve choice, stability and transitions between behaviors are still incompletely understood. To identify neurons and brain areas involved in controlling these processes, we combined a large-scale neuronal inactivation screen with automated action detection in response to a mechanosensory cue in Drosophila larva. We analyzed behaviors from 2.9x105 larvae and identified 66 candidate lines for mechanosensory responses out of which 25 for competitive interactions between actions. We further characterize in detail the neurons in these lines and analyzed their connectivity using electron microscopy. We found the neurons in the mechanosensory network are located in different regions of the nervous system consistent with a distributed model of sensorimotor decision-making. These findings provide the basis for understanding how selection and transition between behaviors are controlled by the nervous system.

Highlights

In response to a sensory cue, animals can perform different behaviors
We have previously identified a circuit for behavioral choice and a two-element sequence in response to an airpuff at the earliest stage sensory processing site which supports a model in which competitive interactions are distributed across the nervous system [3,10]
In addition to new sensory lines, we identified candidate GAL4 lines that target central neurons required for behavioral responses to mechanosensory stimuli

Summary

Introduction

In response to a sensory cue, animals can perform different behaviors. The transformation of the sensory information into appropriate motor outputs involves different parts of the nervous system from sensory processing areas to motor control areas. In order to enable reliable and coherent responses of organisms to sensory cues, the choice of one action must be accompanied by a full suppression of all competing physically mutually exclusive actions, areas of the nervous system that ensure proper selection of behavior will be involved. In response to a single stimulus, different individuals may perform different actions and the same individual can respond to the repetition of the stimulus differently.

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