Concentration memory-dependent synaptic plasticity of a taste circuit regulates salt concentration chemotaxis in Caenorhabditis elegans

Abstract

It is poorly understood how sensory systems memorize the intensity of sensory stimulus, compare it with a newly sensed stimulus, and regulate the orientation behaviour based on the memory. Here we report that Caenorhabditis elegans memorizes the environmental salt concentration during cultivation and exhibits a strong behavioural preference for this concentration. The right-sided amphid gustatory neuron known as ASER, senses decreases in salt concentration, and this information is transmitted to the postsynaptic AIB interneurons only in the salt concentration range lower than the cultivation concentration. In this range, animals migrate towards higher concentration by promoting turning behaviour upon decreases in salt concentration. These observations provide a mechanism for adjusting the orientation behaviour based on the memory of sensory stimulus using a simple neural circuit. A ll living animals are endowed with the capacity to seek optimal ambient conditions. Such behaviour requires memorizing the intensity of sensory stimulus associated with favourable conditions, recognizing the spatio-temporal changes of the stimulus intensity under current conditions, comparing it with the memorized stimulus intensity and regulating the motor output to generate a movement towards a preferred direction. However, in most sensory systems how stimulus intensity is memorized and how distinct orientation behaviours are generated depending on the memory have been poorly explored.Sodium chloride was identified as a chemoattractant for C. elegans 1 . Based on this view the mechanisms of salt chemotaxis has been examined for decades. Amphid taste neurons ASE, which consist of two morphologically symmetric neurons on the left (ASEL) and the right (ASER), have a predominant role in chemotaxis to NaCl and other inorganic salts 2-4 . Calcium imaging experiments showed that these neurons are functionally asymmetric: ASER is depolarized by decreases in salt concentration, while ASEL responds to increases 5 . As activation of ASER and ASEL promotes redirecting turns and forward locomotion, respectively, it was suggested that the right and the left neurons have distinct roles but act in concert for migrating up salt gradient 5 . Through another line of studies on the migration behaviours, two distinct behavioural mechanisms that drive animals towards higher salt concentration have been characterized so far (see below) 6,7 . Despite these sets of knowledge, the physiological and mechanistic properties of the information flow for salt chemotaxis downstream of the sensory neurons have not been obvious, as ASEL and ASER form synapses onto overlapping targets (Fig. 1a).Meanwhile, we have previously shown that pairing starvation with exposure to NaCl causes salt avoidance learning in C. elegans 8 . The insulin signalling pathway components, DAF-2 insulin receptor, AGE-1 phosphoinositide 3-kinase and AKT-1 AKT kinase, are required in ASER for this learning 9 . Activation of the Gq/DAG/PKC signalling pathway consisting of EGL-30 Gq, diacylglycer...

A Single Set of Interneurons Drives Opposite Behaviors in C. elegans

“…Thus, cultivating animals at high CO 2 results in a drive toward higher CO 2 levels rather than a preference for their previous cultivation condition. This is in contrast to other sensory behaviors in C. elegans , including salt chemotaxis and thermotaxis, where animals are attracted to their prior cultivation condition [17, 18]. Animals raised at high CO 2 were not attracted to 40% CO 2 in the 2.5%−40% CO 2 gradient (Figure S1D), suggesting that they retain the ability to avoid toxic levels of CO 2 [19].…”

An Evolutionarily Conserved PLC-PKD-TFEB Pathway for Host Defense

“…PKD activation is required for TFEB nuclear translocation, and downstream transcription of host defense genes. Recent evidence supports a role for PLC-1 downstream of EGL-30 for salt chemotaxis as well (Kunitomo et al, 2013). We observed a complex phenotype for knockdown of plc-1 .…”

Illuminating neural circuits and behaviour in Caenorhabditis elegans with optogenetics

“…Using this approach, it was shown that ASH photoactivation triggers withdrawal behaviours mimicking the endogenous response [50,59]. The strength of the optogenetic activation of the ASH neurons directly correlated with the magnitude of the behavioural response [50,60].…”