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

Abstract

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 naïve 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.

A Multiscale Sensorimotor Model of Experience-Dependent Behavior in a Minimal Organism

“…5. This simplification has already been used in other models of C. elegans navigation 23 , for the same parsimonious reasons as ours. The parameters of Eqs.…”

“…We note that the changes in ASER activity in response to salt steps need to be transient, to prevent the worm from being stuck in the same direction of motion for long periods of time. Experiments show that the timescale of these activity changes is of the order of seconds 13,22,23 .…”

“…The instantaneous excess glutamate, ΔGlu, is assumed in turn to increase linearly with the intracellular Ca 2+ levels of ASER. It is worth mentioning that Glu basal and ΔGlu have different timescales, corresponding to those of their activating factors: Glu basal , regulated by DAG, has a characteristic time ~ 10 minutes 14 , whereas ΔGlu operates in time scales on the order of ~ 10 seconds, corresponding to the Ca 2+ dynamics of ASER 13,22,23 .…”

Ultrastructure of Rat Rostral Nucleus of the Solitary Tract Terminals in the Parabrachial Nucleus and Medullary Reticular Formation

“…Dendritic spines undergo activity-dependent plasticity with respect to their profile diameter, number, and the size of their postsynaptic densities, all resulting in changes in the strength of the synaptic transmission ( Harms and Dunaevsky, 2007 ; Baczynska et al, 2021 ). Many studies have shown that synaptic plasticity is common in the brain regions involved in gustatory perception ( Hill, 2004 ; Dekkers et al, 2021 ; Martin et al, 2021 ). rNST afferent terminals established synaptic contacts with dendritic spines much more frequently in the PBN than in the RF, and the number of dendritic spines receiving synaptic contact from an rNST afferent terminal was six times higher in the PBN than in the RF.…”

The Conscious Nematode: Exploring Hallmarks of Minimal Phenomenal Consciousness in Caenorhabditis Elegans

“…Ardiel & Rankin, 2010;Ghosh et al, 2017;Guillermin et al, 2017;Dekkers et al, 2021;Merritt et al, 2019 Embodiment and self Perhaps. There is an efferent copy of motor commands.…”