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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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2017-03-01
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Series: | eLife |
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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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format | Article |
id | doaj.art-9e635cdbdfc14c74bdd7b4264f63aa20 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-14T07:41:34Z |
publishDate | 2017-03-01 |
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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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