Chemosensory neurons extract information about chemical cues from the environment. How is the activity in these sensory neurons transformed into behavior? Using Caenorhabditis elegans, we map a novel sensory neuron circuit motif that encodes odor concentration. Primary neurons, AWCON and AWA, directly detect the food odor benzaldehyde (BZ) and release insulin-like peptides and acetylcholine, respectively, which are required for odor-evoked responses in secondary neurons, ASEL and AWB. Consistently, both primary and secondary neurons are required for BZ attraction. Unexpectedly, this combinatorial code is altered in aged animals: odor-evoked activity in secondary, but not primary, olfactory neurons is reduced. Moreover, experimental manipulations increasing neurotransmission from primary neurons rescues aging-associated neuronal deficits. Finally, we correlate the odor responsiveness of aged animals with their lifespan. Together, these results show how odors are encoded by primary and secondary neurons and suggest reduced neurotransmission as a novel mechanism driving aging-associated sensory neural activity and behavioral declines.DOI: http://dx.doi.org/10.7554/eLife.10181.001

Summary 7While much is known about how external cues affect neural circuits, less is known about how 1 8 internal states modify their function. We acutely food-deprived C. elegans and analyzed its 1 9 responses in integrating attractant and repellent signals. We show that food deprivation leads to a 2 0 reversible decline in repellent sensitivity; with no effect on appetitive behavior allowing animals 2 1 to engage in higher risk behavior. Multiple tissues including the intestine and body wall muscles released peptide signals modifying their stimulus-evoked adaptation rate. We suggest that altering ASI neuronal dynamics affects its function and modifies behavior. Together, these 2 7 studies show how internal state signals modify sensory perception and risk assessment to 2 8 generate flexible behaviors.

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