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Elife. 2015 Sep 22;4:e10181. doi: 10.7554/eLife.10181.

Circuit mechanisms encoding odors and driving aging-associated behavioral declines in Caenorhabditis elegans.

Author information

1
Neurosciences Graduate Program, University of California, San Diego, La Jolla, United States.
2
Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United States.
3
Department of Mechanical Engineering, University of Michigan, Ann Arbor, United States.
4
Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, United States.

Abstract

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, AWC(ON) 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.

KEYWORDS:

C. elegans; aging; neural circuits; neuroscience; neurotransmission; olfaction; sensory neurons

PMID:
26394000
PMCID:
PMC4577979
DOI:
10.7554/eLife.10181
[Indexed for MEDLINE]
Free PMC Article

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