Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Abstract

Complex animal behaviors are built from dynamical relationships between sensory inputs, neuronal activity, and motor outputs in patterns with strategic value. Connecting these patterns illuminates how nervous systems compute behavior. Here, we study Drosophila larva navigation up temperature gradients toward preferred temperatures (positive thermotaxis). By tracking the movements of animals responding to fixed spatial temperature gradients or random temperature fluctuations, we calculate the sensitivity and dynamics of the conversion of thermosensory inputs into motor responses. We discover three thermosensory neurons in each dorsal organ ganglion (DOG) that are required for positive thermotaxis. Random optogenetic stimulation of the DOG thermosensory neurons evokes behavioral patterns that mimic the response to temperature variations. In vivo calcium and voltage imaging reveals that the DOG thermosensory neurons exhibit activity patterns with sensitivity and dynamics matched to the behavioral response. Temporal processing of temperature variations carried out by the DOG thermosensory neurons emerges in distinct motor responses during thermotaxis. N avigation toward environmental conditions that improve survival and fitness is of near-universal importance in motile biological organisms. Quantitative analysis of such animal behaviors to defined sensory inputs is a powerful approach to elucidate how behavior is encoded in underlying neurons and circuits. The advantage of studying navigation in small, optically transparent, genetically modifiable animals like Caenorhabditis elegans (1) or Drosophila larvae (2) is the opportunity to dissect sensory, neuronal, and behavioral dynamics in live animals by using optical neurophysiology and optogenetics throughout the nervous system.The Drosophila melanogaster larva navigates gradients of many sensory cues, including light, temperature, odors, and tastes, but with fewer neurons in its sensory periphery and brain than the adult. Moreover, the simpler body plan and crawling movements of the larva facilitate the precise quantification of behavioral dynamics. Poikilotherms like C. elegans or Drosophila use sensitive thermosensory mechanisms to navigate moderate temperature ranges, thereby enabling them to use their environments to regulate their own body temperatures (3, 4). Here, we study sensory and behavioral dynamics during positive thermotaxis (i.e., cool avoidance) by the Drosophila larva. Tracking the movements of Drosophila exploring temperature, olfactory, or gaseous gradients has shown that their navigation is generated by a sequence of two alternating motor programs: runs involving peristaltic forward movement that are interrupted by turns involving probing side-to-side head sweeps until the initiation of a new run (5-8). Larvae negotiating temperature gradients stochastically transition between runs and turns by strategies that cause runs pointed in favorable directions to be more frequent and longer than runs pointed in unfavorable directions. These transitions b...

Pan-neuronal imaging in roaming Caenorhabditis elegans

“…A custom-designed thermoelectric cooler was used to sinusoidally modulate the temperature of the stage over the course of an experiment to provide a defined thermosensory stimulus (Fig. 1B) (23). Individual young adult C. elegans were placed on a thin sheet of agar, covered with a large coverslip, and allowed to crawl between the agar and coverslip.…”

“…Because our system is capable of both 3D tracking and volumetric imaging, we asked whether it could meet the challenge of capturing calcium dynamics of neurons in the head of crawling Drosophila larva. We recently discovered three thermosensory neurons in the dorsal organ of Drosophila larva that are required for positive thermotaxis up temperature gradients (23). Like the AFD neuron in C. elegans, they can phase-lock calcium dynamics to an oscillating thermosensory input (32).…”

A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

“…Except for activity measurements of thermosensory neurons in the larval dorsal organ ganglion 32,33 , to our knowledge, no other device has been designed to enable precise and restricted application of stimuli such as chemicals or other cues to the larva or, in the case of tastants, even to the adult fly. Our system goes beyond previous approaches [32][33][34] by allowing for (i) precise chemical stimulation of restrained, semi-intact larvae, (ii) multiple stimulus sweeps interspersed with wash steps and (iii) stimulation of the same animal with different chemicals or combinations of chemicals.…”

“…Our system goes beyond previous approaches [32][33][34] by allowing for (i) precise chemical stimulation of restrained, semi-intact larvae, (ii) multiple stimulus sweeps interspersed with wash steps and (iii) stimulation of the same animal with different chemicals or combinations of chemicals.…”

The use of computational modeling to link sensory processing with behavior in Drosophila

“…A number of studies using Drosophila have examined the impact of visual, chemosensory, or thermal cues on navigational decisions (Gomez-Marin et al 2011;Clark et al 2011;Censi et al 2013;Klein et al 2014;Gepner et al 2015;Schulze et al 2015). In these studies, the detailed recording of fly movement parameters with a quantitative, model-supported analysis of the behavior revealed the navigational strategies with which Drosophila negotiates its environment to find food and avoid noxious chemical, heat, or light stimuli.…”