Reliability of an interneuron response depends on an integrated sensory state

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Abstract

The central nervous system transforms sensory information into representations that are salient to the animal. Here we define the logic of this transformation in a Caenorhabditis elegans integrating interneuron. AIA interneurons receive input from multiple chemosensory neurons that detect attractive odors. We show that reliable AIA responses require the coincidence of two sensory inputs: activation of AWA olfactory neurons that are activated by attractive odors, and inhibition of one or more chemosensory neurons that are inhibited by attractive odors. AWA activates AIA through an electrical synapse, while the disinhibitory pathway acts through glutamatergic chemical synapses. AIA interneurons have bistable electrophysiological properties consistent with their calcium dynamics, suggesting that AIA activation is a stereotyped response to an integrated stimulus. Our results indicate that AIA interneurons combine sensory information using AND-gate logic, requiring coordinated activity from multiple chemosensory neurons. We propose that AIA encodes positive valence based on an integrated sensory state.

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All data generated or analyzed during this study, including source data, are included in the manuscript and supporting files.

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May Dobosiewicz

Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Qiang Liu

Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Cornelia I Bargmann

Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, United States

For correspondence
cori@rockefeller.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8484-0618

Funding

Chan Zuckerberg Initiative

May Dobosiewicz
Qiang Liu
Cornelia I Bargmann

Howard Hughes Medical Institute

May Dobosiewicz
Qiang Liu
Cornelia I Bargmann

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.