Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation

A conventional understanding of perception assigns sensory organs the role of capturing the environment. Better sensors result in more accurate encoding of stimuli, allowing for cognitive processing downstream. Here we show that plasticity in sensory neurons mediates a behavioral switch in C. elegans between attraction to NaCl in naive animals and avoidance of NaCl in preconditioned animals, called gustatory plasticity. Ca2+ imaging in ASE and ASH NaCl sensing neurons reveals multiple cell-autonomous and distributed circuit adaptation mechanisms. A computational model quantitatively accounts for observed behaviors and reveals roles for sensory neurons in the control and modulation of motor behaviors, decision making and navigational strategy. Sensory adaptation dynamically alters the encoding of the environment. Rather than encoding the stimulus directly, therefore, we propose that these C. elegans sensors dynamically encode a context-dependent value of the stimulus. Our results demonstrate how adaptive sensory computation can directly control an animal’s behavioral state. Martijn Dekkers and Felix Salfelder et al. combine experimental approaches and mathematical modeling to determine the contribution of the two main NaCl sensory neurons (termed ASEL and ASER) and the nociceptive neurons (termed ASH) in C. elegans to the context-dependent switching between NaCl attraction and avoidance. Their results show that regulated sensitivity of these sensory neurons to NaCl allows the animal to dynamically modulate its behavioral response and suggest a role for sensory modulation in balancing exploration and exploitation during foraging.