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.
Highlights
Animals have evolved specialized sensory systems to detect relevant information in their environment
We found that mutations in the vesicular acetylcholine transporter (VAChT), unc-17, which packs acetylcholine into synaptic vesicles (Alfonso et al, 1994), reduced AWB odor responses (Figure 4E)
We found that knocking down the C. elegans choline acetyltransferase (ChaT), cha-1, which is required for the biosynthesis of acetylcholine (Rand and Russell, 1984; Alfonso et al, 1994), in the AWA neurons significantly reduced AWB neuron responses to BZ (Figure 4F)
Summary
Animals have evolved specialized sensory systems to detect relevant information in their environment. Activity in an individual olfactory sensory neuron represents the molecular receptive field of its odor receptors (Araneda et al, 2000), and gating by feedback circuits (Gomez et al, 2005; Wachowiak et al, 2009) and modulation by sniffing behavior in mammals (Wesson et al, 2009). Information from these sensory neurons is further processed and relayed to other brain regions
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