Editors' ChoiceNeuroscience

A Salty Switch

Science Signaling  08 Oct 2013:
Vol. 6, Issue 296, pp. ec243
DOI: 10.1126/scisignal.2004789

Specialized sensory neurons guide attraction or repulsion behavior (taxis) in animals. In Caenorhabditis elegans, chemosensory circuits are mediated by ASE neurons in response to salt or AWC neurons in response to odors. Leinwand and Chalasani found that the chemotaxis in response to low concentrations of salt required both ASE and AWC neurons. Neural activity in response to different concentrations of salt was assessed in a microfluidic chamber by calcium imaging of worms expressing the calcium indicator GCaMP. The left ASE neuron (ASEL) and the interneuron AIA, which is stimulated by ASEL, were both activated by either low or high concentrations of salt, and, unexpectedly, one of the AWC neurons, AWCON, also responded to high-salt stimuli. Although the response to low-salt stimuli was normal, worms lacking AWCON neurons or AWCON-specific UNC-31 (an essential component of synaptic vesicle release machinery) mutants failed to show AIA activation and chemotaxis in response to high-salt stimuli. In hypomorphic osm-6–mutant worms, which lack functional sensory cilia, restoration of OSM-6 selectively in ASEL neurons rescued the calcium signaling in response to low- and high-salt stimuli. Although restoration selectively in AWCON neurons rescued the response to odorants, these worms failed to respond to changes in salt concentration, indicating that AWCON neurons did not sense salt autonomously. Furthermore, low-salt stimuli weakly activated AWCON in worms with an ASEL-specific deletion in tom-1, which encodes a syntaxin-interaction protein and results in increased synaptic vesicle exocytosis, suggesting that high-salt stimuli may trigger greater synaptic activity than low-salt stimuli, which could allow diffusible signals to mediate communication between these two neurons nonsynaptically. Worms lacking the insulin-like peptide globally (ins-6 null) or specifically in ASEL neurons showed decreased activation of AWCON neurons and chemotaxis in response to high-salt stimuli. The high-salt response also required the expression of daf-2 (encoding the C. elegans homolog of the insulin and insulin-like growth factor receptor tyrosine kinase) and age-1 (encoding phosphatidylinositol 3-kinase) in AWCON neurons. The findings indicated that nonsynaptic signaling occurred from the ASEL to the AWCON and that AWCON neurons can functionally switch from a sensory neuron to an interneuron in a context-specific manner.

S. G. Leinwand, S. H. Chalasani, Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans. Nat. Neurosci. 16, 1461–1467 (2013). [PubMed]