Memory of recent oxygen experience switches pheromone valence in Caenorhabditis elegans

Abstract

Animals adjust their behavioral priorities according to momentary needs and prior experience. We show that Caenorhabditis elegans changes how it processes sensory information according to the oxygen environment it experienced recently. C. elegans acclimated to 7% O 2 are aroused by CO 2 and repelled by pheromones that attract animals acclimated to 21% O 2 . This behavioral plasticity arises from prolonged activity differences in a circuit that continuously signals O 2 levels. A sustained change in the activity of O 2 -sensing neurons reprograms the properties of their postsynaptic partners, the RMG hub interneurons. RMG is gap-junctionally coupled to the ASK and ADL pheromone sensors that respectively drive pheromone attraction and repulsion. Prior O 2 experience has opposite effects on the pheromone responsiveness of these neurons. These circuit changes provide a physiological correlate of altered pheromone valence. Our results suggest C. elegans stores a memory of recent O 2 experience in the RMG circuit and illustrate how a circuit is flexibly sculpted to guide behavioral decisions in a context-dependent manner.neural circuit | experience-dependent plasticity | tonic circuit | oxygen sensing | acclimation T he body comprises multiple highly integrated subsystems working together to sustain life from moment to moment and over long time scales (1). Much of this coordination involves dynamically interacting neural circuits that optimize responses to current circumstances by taking into account sensory input, organismal state, and previous experience (2-8). Circuit cross-talk enables animals to adjust their behavioral priorities to changing environments, e.g., variation in temperature, humidity, day length, or oxygen (O 2 ) levels (9-13). Whereas some behavioral adjustments can be rapid (14, 15), others develop over time, as animals adapt to changed conditions. How animals store information about their recent environment, and use this information to modify behavioral choices, is poorly understood.The compact nervous system of Caenorhabditis elegans, which comprises only 302 uniquely identifiable neurons (wormwiring.org) (16), provides an opportunity to study the links between prior environmental experience, circuit plasticity, and behavioral change. This nematode is adapted to a life feeding on bacteria in rotting fruit (17). It has sensory receptors for odors, tastants, pheromones, and respiratory gases, as well as temperature, mechanical, and noxious cues (18-21). Despite this simplicity, the mechanisms by which its nervous system marshals information about past and present sensory experience to shape behavioral priorities remain largely mysterious. The anatomical connectome, while valuable (22), is insufficient to explain or predict neuronal network function (23, 24), partly because neuromodulators can dynamically reconfigure and specify functional circuits (25-27).When ambient O 2 approaches 21%, C. elegans wild isolates become persistently aroused and burrow to escape the surface (28)(29)(30). This state swi...

Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior

“…An overlapping set of ascarosides causes sex-specific behavioral responses. In particular, ascr#2, ascr#3, ascr#4, and ascr#8 elicit strong (and highly concentration-dependent) attraction in males, and can generate repulsion responses in hermaphrodites (Srinivasan et al 2008;Macosko et al 2009;Pungaliya et al 2009;Jang et al 2012;Fenk and de Bono 2017). Some of these, particularly ascr#3, are preferentially produced by hermaphrodites (Izrayelit et al 2012).…”

A chemosensory switch couples genetic sex to behavioral valence

“…The degree to which the function of the other 56 shared, ciliated sensory neurons in C. elegans is also modulated by sex is unknown, but it could be much deeper than has been appreciated. Notably, many other aspects of C. elegans internal state regulate chemosensory neuron function [24,37,[80][81][82][83][84][85][86][87][88][89][90], suggesting that such plasticity provides a specific, flexible, and economical means for the compact C. elegans nervous system to implement state-dependent behaviors. Regulated chemosensation is also emerging as an important mechanism in many other systems, including insects, rodents, and humans [84,88,[91][92][93][94][95][96].…”

“…The most well-characterized of these are members of the ascaroside family [20], several of which elicit concentration-dependent, sexually dimorphic behavioral responses alone and in combination [17,18,21,22]. In particular, specific concentrations of ascr#3 (also known as C9 and asc-∆C9) trigger attractive responses in males and, depending on neuromodulatory state, aversion in hermaphrodites [17,21,23,24].…”

Transcriptional Control Of Calmodulin By CAMTA Regulates Neural Excitability

“…We identified mutations in camt-1, the sole C. elegans CAMTA, in a forward genetic screen for mutations that disrupt C. elegans aggregation behavior 19 . This behavior, where animals form groups (Extended Data Fig.…”