Context-dependent plasticity in a sensory circuit

Animals sense the world around them using specialized sensory neurons that are wired into circuits that process sensory information and use it to guide behavior. Such sensory circuits are plastic, with their sensitivity and even constituent neurons changing in regard to context. On page 1461 of this issue, Leinwand and Chalasani take advantage of the relatively simple nervous system of C. elegans, with its 302 identified neurons, to show how a chemosensory circuit changes its composition depending on context.

C. elegans can sense many chemical stimuli in their environment, leading to either attraction or repulsion. Cell ablation experiments have shown that ASE sensory neurons are required for attraction to salts, whereas the AWC sensory neurons are required for attraction to odors. ASE neurons are further subdivided into the ASEL and ASER neurons, and AWC neurons have ON and OFF subtypes. The authors used calcium imaging to show that, although the ASEL neuron (red) responds to low concentrations of NaCl, the AWC^ON neuron (green) responds to high concentrations of NaCl. Similarly, although ASE neurons are required for behavioral attraction to low salt concentrations, AWC neurons are also necessary for attraction to higher salt concentrations. Both ASE and AWC neurons project to the AIA interneuron, which also responds to NaCl. The authors found that AIA responses to high salt concentration depend on the AWC^ON neuron.

These results suggest that the AWC^ON neuron, which is not normally part of the salt-sensing circuit, is recruited into a new circuit at high salt concentrations. The role of the AWC^ON neuron in this circuit is different from its known role in sensing odorants, as its sensory cilia were not required for its response to high salt concentrations. The recruitment of the AWC^ON neuron into the circuit required the release of the insulin-like peptide INS-6 from the ASEL neuron in response to high salt concentrations. INS-6 signals through the insulin receptor DAF-2 to switch the AWC^ON sensory neuron into an interneuron in the salt-sensing circuit. Disrupting insulin signaling also blocked behavioral responses to high salt concentrations. The authors' findings describe a neuropeptide-mediated mechanism in which a sensory circuit can adapt to environmental context to drive context-appropriate behaviors.