Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance

Startle responses triggered by aversive stimuli including predators are widespread across animals. These coordinated whole-body actions require the rapid and simultaneous activation of a large number of muscles. Here we study a startle response in a planktonic larva to understand the whole-body circ...

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Main Authors: Luis A Bezares-Calderón, Jürgen Berger, Sanja Jasek, Csaba Verasztó, Sara Mendes, Martin Gühmann, Rodrigo Almeda, Réza Shahidi, Gáspár Jékely
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/36262
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author Luis A Bezares-Calderón
Jürgen Berger
Sanja Jasek
Csaba Verasztó
Sara Mendes
Martin Gühmann
Rodrigo Almeda
Réza Shahidi
Gáspár Jékely
author_facet Luis A Bezares-Calderón
Jürgen Berger
Sanja Jasek
Csaba Verasztó
Sara Mendes
Martin Gühmann
Rodrigo Almeda
Réza Shahidi
Gáspár Jékely
author_sort Luis A Bezares-Calderón
collection DOAJ
description Startle responses triggered by aversive stimuli including predators are widespread across animals. These coordinated whole-body actions require the rapid and simultaneous activation of a large number of muscles. Here we study a startle response in a planktonic larva to understand the whole-body circuit implementation of the behaviour. Upon encountering water vibrations, larvae of the annelid Platynereis close their locomotor cilia and simultaneously raise the parapodia. The response is mediated by collar receptor neurons expressing the polycystins PKD1-1 and PKD2-1. CRISPR-generated PKD1-1 and PKD2-1 mutant larvae do not startle and fall prey to a copepod predator at a higher rate. Reconstruction of the whole-body connectome of the collar-receptor-cell circuitry revealed converging feedforward circuits to the ciliary bands and muscles. The wiring diagram suggests circuit mechanisms for the intersegmental and left-right coordination of the response. Our results reveal how polycystin-mediated mechanosensation can trigger a coordinated whole-body effector response involved in predator avoidance.
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spelling doaj.art-d778ac0dc98745ee8298c7d280fbba8d2022-12-22T04:29:20ZengeLife Sciences Publications LtdeLife2050-084X2018-12-01710.7554/eLife.36262Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidanceLuis A Bezares-Calderón0https://orcid.org/0000-0001-6678-6876Jürgen Berger1Sanja Jasek2Csaba Verasztó3https://orcid.org/0000-0001-6295-7148Sara Mendes4Martin Gühmann5https://orcid.org/0000-0002-4330-0754Rodrigo Almeda6Réza Shahidi7Gáspár Jékely8https://orcid.org/0000-0001-8496-9836Living Systems Institute, University of Exeter, Exeter, United Kingdom; Max Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyLiving Systems Institute, University of Exeter, Exeter, United Kingdom; Max Planck Institute for Developmental Biology, Tübingen, GermanyLiving Systems Institute, University of Exeter, Exeter, United Kingdom; Max Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyCentre for Ocean Life, Technical University of Denmark, Denmark, Kingdom of DenmarkLiving Systems Institute, University of Exeter, Exeter, United Kingdom; Max Planck Institute for Developmental Biology, Tübingen, GermanyLiving Systems Institute, University of Exeter, Exeter, United Kingdom; Max Planck Institute for Developmental Biology, Tübingen, GermanyStartle responses triggered by aversive stimuli including predators are widespread across animals. These coordinated whole-body actions require the rapid and simultaneous activation of a large number of muscles. Here we study a startle response in a planktonic larva to understand the whole-body circuit implementation of the behaviour. Upon encountering water vibrations, larvae of the annelid Platynereis close their locomotor cilia and simultaneously raise the parapodia. The response is mediated by collar receptor neurons expressing the polycystins PKD1-1 and PKD2-1. CRISPR-generated PKD1-1 and PKD2-1 mutant larvae do not startle and fall prey to a copepod predator at a higher rate. Reconstruction of the whole-body connectome of the collar-receptor-cell circuitry revealed converging feedforward circuits to the ciliary bands and muscles. The wiring diagram suggests circuit mechanisms for the intersegmental and left-right coordination of the response. Our results reveal how polycystin-mediated mechanosensation can trigger a coordinated whole-body effector response involved in predator avoidance.https://elifesciences.org/articles/36262connectomicspolycystinstartle responsezooplanktonneural circuitmechanosensation
spellingShingle Luis A Bezares-Calderón
Jürgen Berger
Sanja Jasek
Csaba Verasztó
Sara Mendes
Martin Gühmann
Rodrigo Almeda
Réza Shahidi
Gáspár Jékely
Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance
eLife
connectomics
polycystin
startle response
zooplankton
neural circuit
mechanosensation
title Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance
title_full Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance
title_fullStr Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance
title_full_unstemmed Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance
title_short Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance
title_sort neural circuitry of a polycystin mediated hydrodynamic startle response for predator avoidance
topic connectomics
polycystin
startle response
zooplankton
neural circuit
mechanosensation
url https://elifesciences.org/articles/36262
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AT jurgenberger neuralcircuitryofapolycystinmediatedhydrodynamicstartleresponseforpredatoravoidance
AT sanjajasek neuralcircuitryofapolycystinmediatedhydrodynamicstartleresponseforpredatoravoidance
AT csabaveraszto neuralcircuitryofapolycystinmediatedhydrodynamicstartleresponseforpredatoravoidance
AT saramendes neuralcircuitryofapolycystinmediatedhydrodynamicstartleresponseforpredatoravoidance
AT martinguhmann neuralcircuitryofapolycystinmediatedhydrodynamicstartleresponseforpredatoravoidance
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AT rezashahidi neuralcircuitryofapolycystinmediatedhydrodynamicstartleresponseforpredatoravoidance
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