Neural Architecture of Hunger-Dependent Multisensory Decision Making in C. elegans

Abstract

SUMMARY Little is known about how animals integrate multiple sensory inputs in natural environments to balance avoidance of danger with approach to things of value. Furthermore, the mechanistic link between internal physiological state and threat-reward decision making remains poorly understood. Here we confronted C. elegans worms with the decision whether to cross a hyperosmotic barrier presenting the threat of desiccation to reach a source of food odor. We identified a specific interneuron that controls this decision via top-down extrasynaptic aminergic potentiation of the primary osmosensory neurons to increase their sensitivity to the barrier. We also establish that food deprivation increases the worm’s willingness to cross the dangerous barrier by suppressing this pathway. These studies reveal a potentially general neural circuit architecture for internal state control of threat-reward decision making.

Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans

“…Several computational models have been constructed to elucidate behavioral mechanisms underlying C. elegans taxis behavior (26)(27)(28). These models have been built using detailed observation of animals moving in gradients.…”

Multisensory integration in C. elegans

“…Behavioral paradigms used to investigate multisensory integration in C. elegans have been developed by taking advantage of the sensitivity of the worms to an array of sensory modalities. These paradigms include: 1) Expose the worms to two sensory cues of opposing valence and ask the animals to make a decision between the cues [22,23]; 2) Expose the worms to a single sensory stimulus that is paired with a contextual cue, such as ambient temperature or food availability [24–27]. Using these paradigms, it has been shown that integrated behavioral responses are regulated by several distinct, but overlapping neuronal and circuit mechanisms, which we will review as the following.…”

“…This high degree of convergence provides an anatomical basis for these interneurons to act as coincidence detectors to receive and process inputs from multiple sensory neurons that respond to simultaneously presented sensory cues of different modalities [22,23,48,62–65]. For example, when worms are simultaneously confronted with an attractive odorant diacetyl sensed by the chemosensory neurons AWA and an aversive stimulant Cu 2+ sensed by the polymodal sensory neurons ASH, they make a behavioral decision between approach and avoidance.…”

“…The ability of neuromodulators to facilitate interactions between neurons that have no anatomical connection not only allows neuromodulation to occur within a neuronal class, such as HEN-1 signaling between interneurons AIY and AIA, but also cross different neuronal types. For example, the biogenic amine tyramine that is secreted by inter/motor neuron RIM regulates the decision to cross a hyperosmotic barrier, sensed by the sensory neuron ASH, to reach a source of food odor by extrasynaptically modulating ASH activity [22]. This type of modulation can occur in a feedback loop [76,77].…”

“…The context can be external, such as the sensory environment of an animal, or internal, such as the state of a neural circuit. Integrating these contexts with sensorimotor response generates flexible behavioral outputs [22,25,26,48,57,58,62,63,65,66,73,75,78–86]. For example, in the above-mentioned study in which worms were confronted with a hyperosmotic barrier preventing it from reaching the food odor diacetyl, one hour of food deprivation significantly increases threat tolerance, promoting the decision to cross the osmotic barrier.…”