Synchronous and opponent thermosensors use flexible cross-inhibition to orchestrate thermal homeostasis

Abstract

<jats:p>Animals often use sensory cells with opposing polarity that are separately tuned to detect increments or decrements of environmental stimuli. For example, cooling and warming cells detect temperature changes<jats:sup>1,2</jats:sup>; moist and dry cells detect humidity changes<jats:sup>3,4</jats:sup>; and ON-OFF retinal cells detect luminance changes<jats:sup>5,6</jats:sup>. How animals integrate the outputs of opponent cells to navigate towards favorable points along a sensory gradient from higher or lower points remains poorly understood. Here, we show how the outputs of warming cells (WCs) and cooling cells (CCs) in the <jats:italic>Drosophila</jats:italic> larva are combined to produce context-dependent thermotactic navigation. The newly discovered WCs and the previously described CCs<jats:sup>7</jats:sup> require distinct but overlapping sets of Ionotropic Receptors to sense temperature changes: Ir68a, Ir93a, and Ir25a for WCs; Ir21a, Ir93a, and Ir25a for CCs. WCs and CCs are bidirectional opponent sensors: WCs are activated by warming and inhibited by cooling, whereas CCs are activated by cooling and inhibited by warming. Both WCs and CCs are sensitive to temperature changes from high temperatures where the larva avoids warming to low temperatures where it avoids cooling. However, at all temperatures, optogenetically-imposed fictive warming of the WCs as well as fictive cooling of the CCs evoke avoidance responses, and fictive cooling of the WCs as well as fictive warming of the CCs inhibit avoidance responses. We reconcile these sensory properties and behavioral responses by showing that the larva uses flexible cross-inhibition of the output pathways of WCs and CCs when making perceptual choices during thermotaxis. Balanced cross-inhibition near preferred temperatures suppresses any directed movement on temperature gradients. Above preferred temperatures, WCs mediate avoidance to warming while cross-inhibiting avoidance to cooling. Below preferred temperatures, CCs mediate avoidance to cooling while cross-inhibiting avoidance to warming. Our results show how flexible cross-inhibition orchestrates a context-dependent perceptual choice during a navigational behavior.</jats:p>

Automated control of odor dynamics for neurophysiology and behavior

“…To understand how the brain transforms environmental cues into behavioral dynamics, it is crucial to be able to precisely control the temporal dynamics of sensory stimuli. The study of vision, audition, and other sensory modalities has benefited from experimental setups allowing precise temporal control of sensory stimuli to probe how circuits shape behavior (Clemens et al, 2018;Badwan et al, 2019;Klein et al, 2015;Hernandez-Nunez et al, 2020). The technical difficulty of controlling odor temporal dynamics for neurophysiology and behavior experiments has drastically constrained the study of the temporal structure of olfactory sensorimotor transformations.…”

“…The study of vision, audition, and other sensory modalities has benefited from experimental setups allowing precise temporal control of sensory stimuli to probe how circuits shape behavior(Clemens et al, 2018;Badwan et al, 2019;Klein et al, 2015;Hernandez-Nunez et al, 2020).…”

Bumblebees can detect floral humidity

“…Differences in floral temperature above a level that would induce a foraging response in bees (presumed to be a temperature difference between flowers of at least 2°C; Heran, 1952 ) may also conflate bee responses. Furthermore, temperature and humidity perception are linked in insects ( Budelli et al, 2019 ; Enjin, 2017 ; Enjin et al, 2016 ; Frank et al, 2017 ; Hernandez-Nunez et al, 2020 preprint). So, temperature differences may interact with humidity perception, influencing pollinator responses, perhaps leading to enhanced responses or contextual responses (e.g.…”

Continuous, long-term crawling behavior characterized by a robotic transport system

“…Larvae also perform robust behavioral responses to temperature changes, engaging in thermotaxis along thermal gradients, and modulating aspects of their locomotive behavior, in particular their turning rate, in order to reach optimal conditions ( Luo et al, 2010 , Klein et al, 2015 ). The recent availability of a connectome brain wiring diagram ( Huser et al, 2012 , Larderet et al, 2017 ) and numerous genetic tools have facilitated probing the neural circuits and molecular mechanisms that underlie these behaviors ( Hernandez-Nunez et al, 2020 , Kaun et al, 2012 , Gepner et al, 2015 , Sokolowski, 1980 , Tian et al, 2009 , Xie et al, 2018 , Inada et al, 2011 ). Here, we focus on directly observed free-moving exploratory search and navigation behavior and seek to continuously measure fly larva crawling over times scales of many hours.…”