TY - JOUR

T1 - Brain-wide mapping of water flow perception in zebrafish

AU - Vanwalleghem, Gilles

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

UR - http://www.scopus.com/inward/record.url?scp=85085263688&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0049-20.2020

DO - 10.1523/JNEUROSCI.0049-20.2020

M3 - Journal article

C2 - 32277044

AN - SCOPUS:85085263688

VL - 40

SP - 4130

EP - 4144

JO - The Journal of neuroscience : the official journal of the Society for Neuroscience

JF - The Journal of neuroscience : the official journal of the Society for Neuroscience

SN - 0270-6474

IS - 21

ER -