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Molecular tuning of electroreception in sharks and skates

Ancient cartilaginous vertebrates, such as sharks, skates, and rays, possess specialized electrosensory organs that detect weak electric fields and relay this information to the central nervous system(1–4). Sharks exploit this sensory modality for predation, whereas skates may also use it to detect...

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Autores principales: Bellono, Nicholas W., Leitch, Duncan B., Julius, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6101975/
https://www.ncbi.nlm.nih.gov/pubmed/29849147
http://dx.doi.org/10.1038/s41586-018-0160-9
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author Bellono, Nicholas W.
Leitch, Duncan B.
Julius, David
author_facet Bellono, Nicholas W.
Leitch, Duncan B.
Julius, David
author_sort Bellono, Nicholas W.
collection PubMed
description Ancient cartilaginous vertebrates, such as sharks, skates, and rays, possess specialized electrosensory organs that detect weak electric fields and relay this information to the central nervous system(1–4). Sharks exploit this sensory modality for predation, whereas skates may also use it to detect signals from conspecifics(5). Here we analyze shark and skate electrosensory cells to ask if discrete physiological properties could contribute to behaviorally-relevant sensory tuning. We show that sharks and skates use a similar low threshold voltage-gated calcium channel to initiate cellular activity but employ distinct potassium channels to modulate this activity. Electrosensory cells from sharks express specially adapted voltage-gated potassium channels that support large, repetitive membrane voltage spikes capable of driving near-maximal vesicular release from elaborate ribbon synapses. In contrast, skates use a calcium-activated potassium channel to produce small, tunable membrane voltage oscillations that elicit stimulus-dependent vesicular release. We propose that these sensory adaptations support amplified indiscriminate signal detection in sharks versus selective frequency detection in skates, potentially reflecting the electroreceptive requirements of these elasmobranch species. Our findings demonstrate how sensory systems adapt to suit an animal’s lifestyle or environmental niche through discrete molecular and biophysical modifications.
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spelling pubmed-61019752018-11-30 Molecular tuning of electroreception in sharks and skates Bellono, Nicholas W. Leitch, Duncan B. Julius, David Nature Article Ancient cartilaginous vertebrates, such as sharks, skates, and rays, possess specialized electrosensory organs that detect weak electric fields and relay this information to the central nervous system(1–4). Sharks exploit this sensory modality for predation, whereas skates may also use it to detect signals from conspecifics(5). Here we analyze shark and skate electrosensory cells to ask if discrete physiological properties could contribute to behaviorally-relevant sensory tuning. We show that sharks and skates use a similar low threshold voltage-gated calcium channel to initiate cellular activity but employ distinct potassium channels to modulate this activity. Electrosensory cells from sharks express specially adapted voltage-gated potassium channels that support large, repetitive membrane voltage spikes capable of driving near-maximal vesicular release from elaborate ribbon synapses. In contrast, skates use a calcium-activated potassium channel to produce small, tunable membrane voltage oscillations that elicit stimulus-dependent vesicular release. We propose that these sensory adaptations support amplified indiscriminate signal detection in sharks versus selective frequency detection in skates, potentially reflecting the electroreceptive requirements of these elasmobranch species. Our findings demonstrate how sensory systems adapt to suit an animal’s lifestyle or environmental niche through discrete molecular and biophysical modifications. 2018-05-30 2018-06 /pmc/articles/PMC6101975/ /pubmed/29849147 http://dx.doi.org/10.1038/s41586-018-0160-9 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Bellono, Nicholas W.
Leitch, Duncan B.
Julius, David
Molecular tuning of electroreception in sharks and skates
title Molecular tuning of electroreception in sharks and skates
title_full Molecular tuning of electroreception in sharks and skates
title_fullStr Molecular tuning of electroreception in sharks and skates
title_full_unstemmed Molecular tuning of electroreception in sharks and skates
title_short Molecular tuning of electroreception in sharks and skates
title_sort molecular tuning of electroreception in sharks and skates
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6101975/
https://www.ncbi.nlm.nih.gov/pubmed/29849147
http://dx.doi.org/10.1038/s41586-018-0160-9
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