Sensory Coding and Olfactory Integration in Caenorhabditis Elegans
Animals must sense their external environments to guide meaningful behavior. The nematode Caenorhabditis elegans, for example, uses volatile cues to navigate toward food from a distance. How does an animal integrate the olfactory information from its environment? Here, I ask how multiple sensory neurons drive and shape one interneuron's activity. C. elegans senses several odors, including the bacterial metabolite diacetyl, using the AWA sensory neurons. AWA forms chemical and electrical synapses onto several interconnected interneurons, which contribute to chemotaxis toward attractive odors like diacetyl. One AWA target is the interneuron AIA, which is connected to AWA via a putative electrical synapse. Both AWA and AIA are robustly activated by diacetyl, but the reliability of their responses decreases at low concentrations. AIA relies on AWA for its reliable response to diacetyl. However, directly activating AWA is not sufficient to evoke reliable AIA responses. Instead, AIA responses to optogenetic AWA stimulation had high and variable latencies and low probabilities. AIA responses, when they did occur, had stereotyped on-dynamics to all concentrations of diacetyl tested, to AWA optogenetic stimulation, and to several additional attractive odors, suggesting all-or-none AIA activation to sensory input. In animals lacking chemical synaptic transmission, AIA responses to direct AWA optogenetic stimulation were fast and reliable, resembling those evoked by diacetyl. AWA-to-AIA communication is thus regulated by inhibitory synaptic input from surrounding neurons. This inhibition comes from a small set of glutamatergic sensory neurons that work together to gate AIA responses to AWA activation. Consistently, two of these glutamatergic sensory neurons directly sense and are inhibited by diacetyl. Their responses are less reliable, or even non-existent, at low concentrations of diacetyl. The difference in the reliability of AIA responses to different diacetyl concentrations may be explained by differences in the composition of the upstream sensory responses. Reliable AIA responses appear to require both activation from AWA through an electrical synapse and the release of inhibition from glutamatergic sensory neurons through chemical synapses. AIA acts as a coincidence detector, and its activity represents a readout of global sensory state, providing insight into how AIA represents "food" signals that are sensed by multiple sensory neurons.
olfaction, C. elegans, sensory integration, AWA-AIA communication, chemotaxis, glutamatergic inhibition, Life Sciences
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