Asymmetric adaptation reveals functional lateralization for graded versus discrete stimuli

Abstract

150 words 9Animal navigation strategies depend on the nature of the environmental cues used. In the 10 nematode Caenorhabditis elegans, navigation has been studied in the context of gradients of 11 attractive or repellent stimuli as well is in response to acute aversive stimuli. We wanted to 12 better understand how sensory responses to the same stimulus vary between graded and acute 13 stimuli, and how this variation relates to behavioral responses. C. elegans has two salt-sensing 14 neurons, ASEL and ASER, that show opposite responses to stepped changes in stimulus levels, 15 however only ASER has been shown to play a prominent role in salt chemotaxis. We used pre-16 exposure to natural stimuli to manipulate the responsiveness of these neurons and tested their 17 separate contributions to behavior. Our results suggest ASEL is specialized for responses to 18 acute stimulus changes. We also found that ASER remains responsive to graded stimuli under 19 conditions where it is unresponsive to large steps. 20 21 22 attractant my change over orders of magnitude. At the same time, animals must remain 33 sensitive to abrupt changes in stimuli that may require acute behavioral responses. 34 In Caenorhabditis elegans, salt chemotaxis has been used to dissect navigation strategies 35 used at the genetic, cellular, circuit, and behavioral levels . The primary salt sensing neurons in 36 C. elegans, ASEL and ASER, exhibit opposite responses to stepped changes in salt 37 concentration: ASEL is activated by cations and responds to up-steps in salt concentration, 38 while ASER detects anions and responds to down-steps (Pierce-Shimomura et al., 2001; 39 Suzuki et al., 2008). Under most conditions, gradient chemotaxis in the nematode 40 Caenorhabditis elegans can be described as a biased random walk, a strategy identical to that 41 used by single-celled organisms like bacteria, multicellular growth processes observed in plant 42 roots, and even subcellular structures like axonal growth cones (Berg and Brown, 1972; Pierce-43 Shimomura et al., 1999). While C. elegans does respond to salt up-steps and down-steps (Miller 44 et al., 2005), most behavioral analysis is done in the context of gradient navigation. However, 45 the physiological properties of ASEL and ASER are less well-explored in the context of graded 46 stimuli. ASER shows complex calcium responses to gradients that depend both on the direction 47 of salt change and whether salt levels are above or below a memorized cultivation 48 concentration (Luo et al., 2014). While ASEL contributes to forward locomotion during 49 exposure to attractive salt concentrations (Suzuki et al., 2008), ASEL has been found to be 50 largely dispensable for both positive and negative salt gradient chemotaxis (Kunitomo et al., 51 2013; Luo et al., 2014), though recently it was shown that optogenetic stimulation of ASEL can 52 drive fictive positive chemotaxis under specific conditions (Wang et al., 2017). 53We were interested in attempting to reconcile calcium imaging experiments, usually 54 per...

A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli

“…Interestingly, the activation dynamics in individual animals considerably varied, even in response to identical highly reproducible optogenetic activations (Fig 5 ). This variability is in line with previous reports demonstrating significant differences between individual worms in neural activity patterns and behavioral outputs (Luo et al , 2014 ; Gordus et al , 2015 ; Stern et al , 2017 ; preprint: Desrochers et al , 2018 ; Itskovits et al , 2018 ; preprint: Pritz et al , 2020 ). Notably, the assayed worms were isogenic and were grown in the exact same conditions.…”

“…In multicellular organisms, equipped with a neural network, one may assume that similar features may be attributed to dynamics within defined neural circuits. Interestingly, however, individual sensory neurons may also implement such computations in a cell‐autonomous manner (Tanimoto et al , 2017 ; preprint: Desrochers et al , 2018 ). For example, the nervous system of Caenorhabditis elegans nematodes consists of 302 neurons (White et al , 1986 ; Cook et al , 2019 ).…”