Abstract
All organisms react to noxious and mechanical stimuli but we still lack a complete understanding of cellular and molecular mechanisms by which somatosensory information is transformed into appropriate motor outputs. The small number of neurons and excellent genetic tools make Drosophila larva an especially tractable model system in which to address this problem. We developed high throughput assays with which we can simultaneously expose more than 1,000 larvae per man-hour to precisely timed noxious heat, vibration, air current, or optogenetic stimuli. Using this hardware in combination with custom software we characterized larval reactions to somatosensory stimuli in far greater detail than possible previously. Each stimulus evoked a distinctive escape strategy that consisted of multiple actions. The escape strategy was context-dependent. Using our system we confirmed that the nociceptive class IV multidendritic neurons were involved in the reactions to noxious heat. Chordotonal (ch) neurons were necessary for normal modulation of head casting, crawling and hunching, in response to mechanical stimuli. Consistent with this we observed increases in calcium transients in response to vibration in ch neurons. Optogenetic activation of ch neurons was sufficient to evoke head casting and crawling. These studies significantly increase our understanding of the functional roles of larval ch neurons. More generally, our system and the detailed description of wild type reactions to somatosensory stimuli provide a basis for systematic identification of neurons and genes underlying these behaviors.
Highlights
Understanding sensory-motor transformations at the level of genes, neurons and circuits has important implications for neurobiology and medicine
We showed for the first time that optogenetic activation of ch neurons increased the probability of head casting and increased crawling speed, reactions that were evoked by vibration
We developed methods that provide more than a hundredfold increase in the speed with which larval reactions to noxious, mechanical and optogenetic stimuli can be quantified compared to previously available single animal methods [26,48]
Summary
Understanding sensory-motor transformations at the level of genes, neurons and circuits has important implications for neurobiology and medicine. The somatosensory system of Drosophila larva is an especially tractable model system for tackling this problem, due to the small number of neurons Drosophila larvae respond to somatosensory stimuli with stereotyped behaviors. Noxious mechanical and thermal stimuli can evoke sideways rolling, a stereotyped escape response [9]. The nociceptive sensory neurons mediate, in part, larval avoidance of strong light [18]. Several ion channels essential for mechanical and thermal nociception and numerous other genes involved in the function and development of somatosensory neurons have been identified over the years [9,19,20,21,22]
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