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Reliability of an interneuron response depends on an integrated sensory state

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...

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Autores principales: Dobosiewicz, May, Liu, Qiang, Bargmann, Cornelia I
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894930/
https://www.ncbi.nlm.nih.gov/pubmed/31718773
http://dx.doi.org/10.7554/eLife.50566
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author Dobosiewicz, May
Liu, Qiang
Bargmann, Cornelia I
author_facet Dobosiewicz, May
Liu, Qiang
Bargmann, Cornelia I
author_sort Dobosiewicz, May
collection PubMed
description 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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spelling pubmed-68949302019-12-06 Reliability of an interneuron response depends on an integrated sensory state Dobosiewicz, May Liu, Qiang Bargmann, Cornelia I eLife Neuroscience 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. eLife Sciences Publications, Ltd 2019-11-13 /pmc/articles/PMC6894930/ /pubmed/31718773 http://dx.doi.org/10.7554/eLife.50566 Text en © 2019, Dobosiewicz et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Dobosiewicz, May
Liu, Qiang
Bargmann, Cornelia I
Reliability of an interneuron response depends on an integrated sensory state
title Reliability of an interneuron response depends on an integrated sensory state
title_full Reliability of an interneuron response depends on an integrated sensory state
title_fullStr Reliability of an interneuron response depends on an integrated sensory state
title_full_unstemmed Reliability of an interneuron response depends on an integrated sensory state
title_short Reliability of an interneuron response depends on an integrated sensory state
title_sort reliability of an interneuron response depends on an integrated sensory state
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894930/
https://www.ncbi.nlm.nih.gov/pubmed/31718773
http://dx.doi.org/10.7554/eLife.50566
work_keys_str_mv AT dobosiewiczmay reliabilityofaninterneuronresponsedependsonanintegratedsensorystate
AT liuqiang reliabilityofaninterneuronresponsedependsonanintegratedsensorystate
AT bargmanncorneliai reliabilityofaninterneuronresponsedependsonanintegratedsensorystate