Literature DB >> 32277044

Brain-Wide Mapping of Water Flow Perception in Zebrafish.

Gilles Vanwalleghem1, Kevin Schuster2, Michael A Taylor3, Itia A Favre-Bulle4,5, Ethan K Scott1.   

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.SIGNIFICANCE STATEMENT In aquatic animals, the lateral line is important for detecting water flow stimuli, but the brain networks that interpret this information remain mysterious. Here, we have imaged the activity of individual neurons across the entire brains of larval zebrafish, revealing all response types and their brain locations as water flow processing occurs. We find neurons that respond to the simple presence of water flow, and others attuned to the direction, speed, and duration of flow, or the accumulated displacement of water that has passed during the stimulus. With this information, we modeled the underlying network, describing a system that is nuanced in its processing of water flow simulating head-to-tail motion but rudimentary in processing flow in the tail-to-head direction.
Copyright © 2020 the authors.

Entities:  

Keywords:  calcium imaging; lateral line; light sheet microscopy; microfluidic; sensory; zebrafish

Year:  2020        PMID: 32277044      PMCID: PMC7244201          DOI: 10.1523/JNEUROSCI.0049-20.2020

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  54 in total

1.  The functioning and significance of the lateral-line organs.

Authors:  S DIJKGRAAF
Journal:  Biol Rev Camb Philos Soc       Date:  1963-02

Review 2.  Development of the zebrafish lateral line.

Authors:  Alain Ghysen; Christine Dambly-Chaudière
Journal:  Curr Opin Neurobiol       Date:  2004-02       Impact factor: 6.627

3.  Complex network measures of brain connectivity: uses and interpretations.

Authors:  Mikail Rubinov; Olaf Sporns
Journal:  Neuroimage       Date:  2009-10-09       Impact factor: 6.556

4.  A profile of auditory-responsive neurons in the larval zebrafish brain.

Authors:  Gilles Vanwalleghem; Lucy A Heap; Ethan K Scott
Journal:  J Comp Neurol       Date:  2017-06-23       Impact factor: 3.215

5.  Afferent and motoneuron activity in response to single neuromast stimulation in the posterior lateral line of larval zebrafish.

Authors:  Melanie Haehnel-Taguchi; Otar Akanyeti; James C Liao
Journal:  J Neurophysiol       Date:  2014-06-25       Impact factor: 2.714

6.  Larval zebrafish rapidly sense the water flow of a predator's strike.

Authors:  M J McHenry; K E Feitl; J A Strother; W J Van Trump
Journal:  Biol Lett       Date:  2009-03-25       Impact factor: 3.703

7.  Connections of octaval and lateral line nuclei of the medulla in the goldfish, including the cytoarchitecture of the secondary octaval population in goldfish and catfish.

Authors:  C A McCormick; D V Hernandez
Journal:  Brain Behav Evol       Date:  1996       Impact factor: 1.808

8.  Neural circuits for evidence accumulation and decision making in larval zebrafish.

Authors:  Armin Bahl; Florian Engert
Journal:  Nat Neurosci       Date:  2019-12-02       Impact factor: 24.884

9.  Zebrafish larvae exhibit rheotaxis and can escape a continuous suction source using their lateral line.

Authors:  Julia Olszewski; Melanie Haehnel; Masashige Taguchi; James C Liao
Journal:  PLoS One       Date:  2012-05-03       Impact factor: 3.240

10.  Motor Behavior Selectively Inhibits Hair Cells Activated by Forward Motion in the Lateral Line of Zebrafish.

Authors:  Paul Pichler; Leon Lagnado
Journal:  Curr Biol       Date:  2019-12-19       Impact factor: 10.834

View more
  16 in total

1.  Fast whole-brain imaging of seizures in zebrafish larvae by two-photon light-sheet microscopy.

Authors:  Giuseppe de Vito; Lapo Turrini; Caroline Müllenbroich; Pietro Ricci; Giuseppe Sancataldo; Giacomo Mazzamuto; Natascia Tiso; Leonardo Sacconi; Duccio Fanelli; Ludovico Silvestri; Francesco Vanzi; Francesco Saverio Pavone
Journal:  Biomed Opt Express       Date:  2022-02-16       Impact factor: 3.732

2.  Broad frequency sensitivity and complex neural coding in the larval zebrafish auditory system.

Authors:  Rebecca E Poulsen; Leandro A Scholz; Lena Constantin; Itia Favre-Bulle; Gilles C Vanwalleghem; Ethan K Scott
Journal:  Curr Biol       Date:  2021-03-02       Impact factor: 10.834

3.  A neuronal blueprint for directional mechanosensation in larval zebrafish.

Authors:  Gema Valera; Daniil A Markov; Kayvan Bijari; Owen Randlett; Amir Asgharsharghi; Jean-Pierre Baudoin; Giorgio A Ascoli; Ruben Portugues; Hernán López-Schier
Journal:  Curr Biol       Date:  2021-02-04       Impact factor: 10.834

Review 4.  How Zebrafish Can Drive the Future of Genetic-based Hearing and Balance Research.

Authors:  Lavinia Sheets; Melanie Holmgren; Katie S Kindt
Journal:  J Assoc Res Otolaryngol       Date:  2021-04-28

5.  Calcium Imaging and the Curse of Negativity.

Authors:  Gilles Vanwalleghem; Lena Constantin; Ethan K Scott
Journal:  Front Neural Circuits       Date:  2021-01-06       Impact factor: 3.492

Review 6.  Optical Tweezers Exploring Neuroscience.

Authors:  Isaac C D Lenton; Ethan K Scott; Halina Rubinsztein-Dunlop; Itia A Favre-Bulle
Journal:  Front Bioeng Biotechnol       Date:  2020-11-27

7.  Sound generation in zebrafish with Bio-Opto-Acoustics.

Authors:  Itia A Favre-Bulle; Michael A Taylor; Emmanuel Marquez-Legorreta; Gilles Vanwalleghem; Rebecca E Poulsen; Halina Rubinsztein-Dunlop; Ethan K Scott
Journal:  Nat Commun       Date:  2020-11-30       Impact factor: 14.919

8.  Altered brain-wide auditory networks in a zebrafish model of fragile X syndrome.

Authors:  Lena Constantin; Rebecca E Poulsen; Leandro A Scholz; Itia A Favre-Bulle; Michael A Taylor; Biao Sun; Geoffrey J Goodhill; Gilles C Vanwalleghem; Ethan K Scott
Journal:  BMC Biol       Date:  2020-09-16       Impact factor: 7.431

9.  Sensory adaptation at ribbon synapses in the zebrafish lateral line.

Authors:  Francesca De Faveri; Walter Marcotti; Federico Ceriani
Journal:  J Physiol       Date:  2021-07-09       Impact factor: 6.228

Review 10.  Neuronal Graphs: A Graph Theory Primer for Microscopic, Functional Networks of Neurons Recorded by Calcium Imaging.

Authors:  Carl J Nelson; Stephen Bonner
Journal:  Front Neural Circuits       Date:  2021-06-10       Impact factor: 3.492

View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.