Rapid threat assessment in the Drosophila thermosensory system

Genevieve C. Jouandet, Michael H. Alpert, José Miguel Simões, Richard Suhendra, Dominic D. Frank, Joshua I. Levy, Alessia Para, William L. Kath and Marco Gallio ()
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Genevieve C. Jouandet: Northwestern University
Michael H. Alpert: Northwestern University
José Miguel Simões: Northwestern University
Richard Suhendra: Northwestern University
Dominic D. Frank: Northwestern University
Joshua I. Levy: Northwestern University
Alessia Para: Northwestern University
William L. Kath: Northwestern University
Marco Gallio: Northwestern University

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract Neurons that participate in sensory processing often display “ON” responses, i.e., fire transiently at the onset of a stimulus. ON transients are widespread, perhaps universal to sensory coding, yet their function is not always well-understood. Here, we show that ON responses in the Drosophila thermosensory system extrapolate the trajectory of temperature change, priming escape behavior if unsafe thermal conditions are imminent. First, we show that second-order thermosensory projection neurons (TPN-IIIs) and their Lateral Horn targets (TLHONs), display ON responses to thermal stimuli, independent of direction of change (heating or cooling) and of absolute temperature. Instead, they track the rate of temperature change, with TLHONs firing exclusively to rapid changes (>0.2 °C/s). Next, we use connectomics to track TLHONs’ output to descending neurons that control walking and escape, and modeling and genetic silencing to demonstrate how ON transients can flexibly amplify aversive responses to small thermal change. Our results suggest that, across sensory systems, ON transients may represent a general mechanism to systematically anticipate and respond to salient or dangerous conditions.

Date: 2023
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DOI: 10.1038/s41467-023-42864-5

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