Dopamine signaling tunes spatial pattern selectivity in C. elegans

Animals with complex brains can discriminate the spatial arrangement of physical features in the environment. It is unknown whether such sensitivity to spatial patterns can be accomplished in simpler nervous systems that lack long-range sensory modalities such as vision and hearing. Here we show tha...

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Main Authors: Bicheng Han, Yongming Dong, Lin Zhang, Yan Liu, Ithai Rabinowitch, Jihong Bai
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/22896
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author Bicheng Han
Yongming Dong
Lin Zhang
Yan Liu
Ithai Rabinowitch
Jihong Bai
author_facet Bicheng Han
Yongming Dong
Lin Zhang
Yan Liu
Ithai Rabinowitch
Jihong Bai
author_sort Bicheng Han
collection DOAJ
description Animals with complex brains can discriminate the spatial arrangement of physical features in the environment. It is unknown whether such sensitivity to spatial patterns can be accomplished in simpler nervous systems that lack long-range sensory modalities such as vision and hearing. Here we show that the nematode Caenorhabditis elegans can discriminate spatial patterns in its surroundings, despite having a nervous system of only 302 neurons. This spatial pattern selectivity requires touch-dependent dopamine signaling, including the mechanosensory TRP-4 channel in dopaminergic neurons and the D2-like dopamine receptor DOP-3. We find that spatial pattern selectivity varies significantly among C. elegans wild isolates. Electrophysiological recordings show that natural variations in TRP-4 reduce the mechanosensitivity of dopaminergic neurons. Polymorphic substitutions in either TRP-4 or DOP-3 alter the selectivity of spatial patterns. Together, these results demonstrate an ancestral role for dopamine signaling in tuning spatial pattern preferences in a simple nervous system.
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spelling doaj.art-9e635cdbdfc14c74bdd7b4264f63aa202022-12-22T02:05:29ZengeLife Sciences Publications LtdeLife2050-084X2017-03-01610.7554/eLife.22896Dopamine signaling tunes spatial pattern selectivity in C. elegansBicheng Han0Yongming Dong1https://orcid.org/0000-0002-6510-0913Lin Zhang2https://orcid.org/0000-0002-9065-4168Yan Liu3https://orcid.org/0000-0002-5631-7272Ithai Rabinowitch4https://orcid.org/0000-0003-0361-9055Jihong Bai5https://orcid.org/0000-0001-6773-2175Basic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesBasic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesBasic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesBasic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesBasic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesBasic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesAnimals with complex brains can discriminate the spatial arrangement of physical features in the environment. It is unknown whether such sensitivity to spatial patterns can be accomplished in simpler nervous systems that lack long-range sensory modalities such as vision and hearing. Here we show that the nematode Caenorhabditis elegans can discriminate spatial patterns in its surroundings, despite having a nervous system of only 302 neurons. This spatial pattern selectivity requires touch-dependent dopamine signaling, including the mechanosensory TRP-4 channel in dopaminergic neurons and the D2-like dopamine receptor DOP-3. We find that spatial pattern selectivity varies significantly among C. elegans wild isolates. Electrophysiological recordings show that natural variations in TRP-4 reduce the mechanosensitivity of dopaminergic neurons. Polymorphic substitutions in either TRP-4 or DOP-3 alter the selectivity of spatial patterns. Together, these results demonstrate an ancestral role for dopamine signaling in tuning spatial pattern preferences in a simple nervous system.https://elifesciences.org/articles/22896spatial pattern selectiondopaminenatural variationTRP channel
spellingShingle Bicheng Han
Yongming Dong
Lin Zhang
Yan Liu
Ithai Rabinowitch
Jihong Bai
Dopamine signaling tunes spatial pattern selectivity in C. elegans
eLife
spatial pattern selection
dopamine
natural variation
TRP channel
title Dopamine signaling tunes spatial pattern selectivity in C. elegans
title_full Dopamine signaling tunes spatial pattern selectivity in C. elegans
title_fullStr Dopamine signaling tunes spatial pattern selectivity in C. elegans
title_full_unstemmed Dopamine signaling tunes spatial pattern selectivity in C. elegans
title_short Dopamine signaling tunes spatial pattern selectivity in C. elegans
title_sort dopamine signaling tunes spatial pattern selectivity in c elegans
topic spatial pattern selection
dopamine
natural variation
TRP channel
url https://elifesciences.org/articles/22896
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