Review
Exploratory decisions of the Caenorhabditis elegans male: A conflict of two drives

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Highlights

Abstract

The ability to generate behavioral plasticity according to ever-changing physiological demands and environmental conditions is a universal feature of decision-making circuits in all animals. Decision-making requires complex integration of internal states with sensory context. As a mate searching strategy, the Caenorhabditis elegans male modifies his exploratory behavior in relation to a source of food according to recent sensory experience with mates. Information about the reproductive and nutritional status of the male is also incorporated in his choice of exploratory behavior. The study of mate searching in the C. elegans male, a genetic model organism with a nervous system of only 383 neurons, provides the opportunity to elucidate the molecular and cellular mechanisms of state-dependent control of behavior and sensory integration. Here I review our progress in understanding the physiological and environmental regulation of the male's exploratory choices – to explore in search of mates or to exploit a source of food – and the neural circuits and neuromodulator pathways underlying this decision.

Introduction

The biggest challenge facing all animals is to choose what to do when. The prioritization of one behavior over another when the two compete for expression is the foundation of decision-making. Optimal decision-making requires the integration and resolution of conflicting inputs within neural networks as well as modulation of behavioral output by physiological states [1], [2]. These are universal features of the neural circuits that drive behavioral choice in all organisms, from nematodes to humans [3].

Decision-making relies on the operational plasticity of neural networks, i.e. the ability of one network to generate more than one behavioral output. The study of small circuits in invertebrate systems has contributed greatly to our understanding of how neural networks produce distinct behavioral outputs. Work on central pattern generators that drive swimming in Tritonia and the leech, biting in Aplysia and gastric mill movements in crustaceans have revealed the mechanisms by which cellular, synaptic and connectivity properties of neural networks can change to provide output diversity [4]. However, when animals execute behavioral choices that involve the whole organism, such as feeding versus mating or source exploitation versus exploration, the choice is shaped by the physiological demands of the organism. For these decisions, network plasticity needs to incorporate internal drive states that may sometimes be in conflict.

The study of behavioral prioritization in animals with small nervous systems, such as Caenorhabditis elegans (only 383 neurons in the male), provides the opportunity to elucidate the cellular and molecular mechanisms by which a whole organismal neural network encodes behavioral decisions according to sensory experience and physiological demands. In this system, one can address with precision and relative ease how neural circuits are modulated by the endocrine system, how previous experience and physiological state regulate the acquisition and processing of environmental stimuli and how behavioral state transitions are generated and terminated at the cellular and molecular level.

The C. elegans male needs to explore his environment in search of both food and mates. In the wild, these resources are often available in discrete patches at distant locations. The mate-searching strategy of the C. elegans male consists of an exploratory behavior that will take him away from a food source if mates are absent and will keep him at a source of food where he has recently experienced mates. The food-leaving assay exploits the C. elegans male's tendency to explore his environment and readiness to leave a plentiful source of food depleted of mates as a measure of the male's drive and motivation to reproduce [5]. Consistent with the idea that male food-leaving behavior is a mate-searching strategy, exploration away from a plentiful source of food only occurs in sexually mature males, not self-fertilizing hermaphrodites or males at larval stages [5]. Furthermore, recent experience with a mate inhibits exploration away from food [5], [6].

Food leaving as a mate-searching strategy imposes behavioral prioritization on the male to satisfy competing needs: to explore in search of mates over exploiting a source of food. This exploratory decision is executed through the regulation of specific patterns of locomotion. What need the male prioritizes and what choice he executes depends on his internal nutritional, reproductive and neuromodulatory state and on previous sensory experience of mates. This information needs to be integrated within the neural network for exploration and converge onto the pre-motor interneurons controlling locomotion.

In this review I will present our current knowledge of the mechanisms regulating the male's decision to leave or to stay on food (Fig. 1). I will first provide an overview of the internal physiological signals (reproductive, nutritional and neuromodulatory states) that regulate male exploration. Then I will explain how environmental signals -recent mate experience and food- alter the male's patterns of locomotion to produce exploratory decisions. Finally I will describe the main cellular components of the male's neural network for exploration and how they regulate locomotion based on sensory experience and internal modulatory state.

Section snippets

Reproductive status

C. elegans is an hermaphroditic species with two genders: males and self-fertilising hermaphrodites, which may also serve as mates for the males. Both males and hermaphrodites explore their environment in search of favorable conditions. Patterns of exploration are sexually dimorphic and are regulated differently in males and hermaphrodites according to their specific needs (reviewed in [7]). One such sexually dimorphic need is associated with their different systems of reproduction. Males, who

Sensing a mate on food

As an efficient mate-searching strategy, food leaving is suppressed when mates are found on a food patch [5], [6]. Experiencing a mate on food produces a durable change (1 h) in the state of the male and a consequent change in his behavioral responses to food [6], [26]. These changes in state and behavior result in exploration being confined to the limits of the food patch [6]. Copulation is not required for this change in male exploratory behavior. Instead, mate experience involves the male

A distributed neural network for male exploratory behavior

In order for the male to produce the appropriate exploratory decision, the internal physiological signals and environmental cues described heretofore need to be processed and effectively integrated within the male's neural network for locomotion. The main neuronal components that convey food, mate and PDF neuromodulation inputs to the network as well as the pre-motor interneurons executing distinct locomotion outputs have been identified.

Outlook and outstanding questions

The paradigm of food leaving as a mate-searching strategy of the C. elegans male provides a powerful system to elucidate the molecular and cellular mechanisms of decision-making under conflicting drives. Although substantial progress has been made toward elucidating main cellular and molecular components of the male's network for exploration and its outputs, as revealed by the present review, there is still considerable knowledge to be gained on the operational logic of this network. A deeper

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