Brain-wide mapping of water flow perception in zebrafish

Gilles Vanwalleghem; Kevin Schuster; Michael A. Taylor; Itia A. Favre-Bulle; Ethan K. Scott

doi:10.1523/JNEUROSCI.0049-20.2020

Brain-wide mapping of water flow perception in zebrafish

Gilles Vanwalleghem^*, Kevin Schuster, Michael A. Taylor, Itia A. Favre-Bulle, Ethan K. Scott

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

36 Citationer (Scopus)

Abstract

Information about water flow, detected by lateral line organs, is critical to the behavior and survival of fish and amphibians. While certain aspects of water flow processing have been revealed through electrophysiology, we lack a comprehensive description of the neurons that respond to water flow and the network that they form. Here, we use brain-wide calcium imaging in combination with microfluidic stimulation to map out, at cellular resolution, neuronal responses involved in perceiving and processing water flow information in larval zebrafish. We find a diverse array of neurons responding to head-to-tail (h-t) flow, tail-to-head (t-h) flow, or both. Early in this pathway, in the lateral line ganglia, neurons respond almost exclusively to the simple presence of h-t or t-h flow, but later processing includes neurons responding specifically to flow onset, representing the accumulated displacement of flow during a stimulus, or encoding the speed of the flow. The neurons reporting on these more nuanced details are located across numerous brain regions, including some not previously implicated in water flow processing. A graph theory-based analysis of the brain-wide water flow network shows that a majority of this processing is dedicated to h-t flow detection, and this is reinforced by our finding that details like flow velocity and the total accumulated flow are only encoded for the h-t direction. The results represent the first brain-wide description of processing for this important modality, and provide a departure point for more detailed studies of the flow of information through this network.

Originalsprog	Engelsk
Tidsskrift	Journal of Neuroscience
Vol/bind	40
Nummer	21
Sider (fra-til)	4130-4144
Antal sider	15
ISSN	0270-6474
DOI	https://doi.org/10.1523/JNEUROSCI.0049-20.2020
Status	Udgivet - 20 maj 2020
Udgivet eksternt	Ja

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10.1523/JNEUROSCI.0049-20.2020

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title = "Brain-wide mapping of water flow perception in zebrafish",

abstract = "Information about water flow, detected by lateral line organs, is critical to the behavior and survival of fish and amphibians. While certain aspects of water flow processing have been revealed through electrophysiology, we lack a comprehensive description of the neurons that respond to water flow and the network that they form. Here, we use brain-wide calcium imaging in combination with microfluidic stimulation to map out, at cellular resolution, neuronal responses involved in perceiving and processing water flow information in larval zebrafish. We find a diverse array of neurons responding to head-to-tail (h-t) flow, tail-to-head (t-h) flow, or both. Early in this pathway, in the lateral line ganglia, neurons respond almost exclusively to the simple presence of h-t or t-h flow, but later processing includes neurons responding specifically to flow onset, representing the accumulated displacement of flow during a stimulus, or encoding the speed of the flow. The neurons reporting on these more nuanced details are located across numerous brain regions, including some not previously implicated in water flow processing. A graph theory-based analysis of the brain-wide water flow network shows that a majority of this processing is dedicated to h-t flow detection, and this is reinforced by our finding that details like flow velocity and the total accumulated flow are only encoded for the h-t direction. The results represent the first brain-wide description of processing for this important modality, and provide a departure point for more detailed studies of the flow of information through this network.",

keywords = "Calcium imaging, Lateral line, Light sheet microscopy, Microfluidic, Sensory, Zebrafish",

author = "Gilles Vanwalleghem and Kevin Schuster and Taylor, {Michael A.} and Favre-Bulle, {Itia A.} and Scott, {Ethan K.}",

note = "Funding Information: Support for this research was provided by an National Health and Medical Research Council Project Grant (APP1066887) and three Australia Research Council Discovery Project Grants (DP140102036, DP110103612, and DP190103430) to E.K.S., and an EMBO Long-Term Fellowship to G.V.; and a Fellowship from the Human Frontier Science Program to M.A.T. Support was also provided by the Australian National Fabrication Facility, QLD node. We thank the Biological Resources Aquatics Team at the University of Queensland for animal care. Publisher Copyright: Copyright {\textcopyright} 2020 the authors",

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doi = "10.1523/JNEUROSCI.0049-20.2020",

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AU - Schuster, Kevin

AU - Taylor, Michael A.

AU - Favre-Bulle, Itia A.

AU - Scott, Ethan K.

N1 - Funding Information: Support for this research was provided by an National Health and Medical Research Council Project Grant (APP1066887) and three Australia Research Council Discovery Project Grants (DP140102036, DP110103612, and DP190103430) to E.K.S., and an EMBO Long-Term Fellowship to G.V.; and a Fellowship from the Human Frontier Science Program to M.A.T. Support was also provided by the Australian National Fabrication Facility, QLD node. We thank the Biological Resources Aquatics Team at the University of Queensland for animal care. Publisher Copyright: Copyright © 2020 the authors

PY - 2020/5/20

Y1 - 2020/5/20

N2 - Information about water flow, detected by lateral line organs, is critical to the behavior and survival of fish and amphibians. While certain aspects of water flow processing have been revealed through electrophysiology, we lack a comprehensive description of the neurons that respond to water flow and the network that they form. Here, we use brain-wide calcium imaging in combination with microfluidic stimulation to map out, at cellular resolution, neuronal responses involved in perceiving and processing water flow information in larval zebrafish. We find a diverse array of neurons responding to head-to-tail (h-t) flow, tail-to-head (t-h) flow, or both. Early in this pathway, in the lateral line ganglia, neurons respond almost exclusively to the simple presence of h-t or t-h flow, but later processing includes neurons responding specifically to flow onset, representing the accumulated displacement of flow during a stimulus, or encoding the speed of the flow. The neurons reporting on these more nuanced details are located across numerous brain regions, including some not previously implicated in water flow processing. A graph theory-based analysis of the brain-wide water flow network shows that a majority of this processing is dedicated to h-t flow detection, and this is reinforced by our finding that details like flow velocity and the total accumulated flow are only encoded for the h-t direction. The results represent the first brain-wide description of processing for this important modality, and provide a departure point for more detailed studies of the flow of information through this network.

AB - Information about water flow, detected by lateral line organs, is critical to the behavior and survival of fish and amphibians. While certain aspects of water flow processing have been revealed through electrophysiology, we lack a comprehensive description of the neurons that respond to water flow and the network that they form. Here, we use brain-wide calcium imaging in combination with microfluidic stimulation to map out, at cellular resolution, neuronal responses involved in perceiving and processing water flow information in larval zebrafish. We find a diverse array of neurons responding to head-to-tail (h-t) flow, tail-to-head (t-h) flow, or both. Early in this pathway, in the lateral line ganglia, neurons respond almost exclusively to the simple presence of h-t or t-h flow, but later processing includes neurons responding specifically to flow onset, representing the accumulated displacement of flow during a stimulus, or encoding the speed of the flow. The neurons reporting on these more nuanced details are located across numerous brain regions, including some not previously implicated in water flow processing. A graph theory-based analysis of the brain-wide water flow network shows that a majority of this processing is dedicated to h-t flow detection, and this is reinforced by our finding that details like flow velocity and the total accumulated flow are only encoded for the h-t direction. The results represent the first brain-wide description of processing for this important modality, and provide a departure point for more detailed studies of the flow of information through this network.

KW - Calcium imaging

KW - Lateral line

KW - Light sheet microscopy

KW - Microfluidic

KW - Sensory

KW - Zebrafish

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DO - 10.1523/JNEUROSCI.0049-20.2020

M3 - Journal article

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AN - SCOPUS:85085263688

SN - 0270-6474

VL - 40

SP - 4130

EP - 4144

JO - Journal of Neuroscience

JF - Journal of Neuroscience

IS - 21

ER -

Brain-wide mapping of water flow perception in zebrafish

Abstract

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