TY - JOUR

T1 - Broad frequency sensitivity and complex neural coding in the larval zebrafish auditory system

AU - Poulsen, Rebecca E.

AU - Scholz, Leandro A.

AU - Constantin, Lena

AU - Favre-Bulle, Itia

AU - Vanwalleghem, Gilles C.

AU - Scott, Ethan K.

N1 - Funding Information: We thank the University of Queensland’s Biological Resources aquatics team for animal care. We also thank Emmanuel Marquez-Legorreta for his intellectual expertise regarding telencephalic activity. We thank Germán Sumbre and Rowan Tweedale for suggestions on the manuscript. Support was provided by NHMRC project grants APP1066887 and APP1165173 , a Simons Foundation Pilot Award ( 399432 ), a Simons Foundation Research Award ( 625793 ), and two ARC Discovery Project Grants ( DP140102036 and DP110103612 ) to E.K.S. and the Australian National Fabrication Facility (ANFF), QLD node. The research reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award number R01NS118406 to E.K.S. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. G.C.V. was supported by an EMBO Long-term Fellowship, and R.E.P. and L.S. were supported by University of Queensland Postgraduate Awards. Publisher Copyright: © 2021 Elsevier Inc.

PY - 2021/5

Y1 - 2021/5

N2 - Most animals have complex auditory systems that identify salient features of the acoustic landscape to direct appropriate responses. In fish, these features include the volume, frequency, complexity, and temporal structure of acoustic stimuli transmitted through water. Larval fish have simple brains compared to adults but swim freely and depend on sophisticated sensory processing for survival.1–5 Zebrafish larvae, an important model for studying brain-wide neural networks, have thus far been found to possess a rudimentary auditory system, sensitive to a narrow range of frequencies and without evident sensitivity to acoustic features that are salient and ethologically important to adult fish.6,7 Here, we have combined a novel method for delivering water-borne sounds, a diverse assembly of acoustic stimuli, and whole-brain calcium imaging to describe the responses of individual auditory-responsive neurons across the brains of zebrafish larvae. Our results reveal responses to frequencies ranging from 100 Hz to 4 kHz, with evidence of frequency discrimination from 100 Hz to 2.5 kHz. Frequency-selective neurons are located in numerous regions of the brain, and neurons responsive to the same frequency are spatially grouped in some regions. Using functional clustering, we identified categories of neurons that are selective for a single pure-tone frequency, white noise, the sharp onset of acoustic stimuli, and stimuli involving a gradual crescendo. These results suggest a more nuanced auditory system than has previously been described in larval fish and provide insights into how a young animal's auditory system can both function acutely and serve as the scaffold for a more complex adult system.

AB - Most animals have complex auditory systems that identify salient features of the acoustic landscape to direct appropriate responses. In fish, these features include the volume, frequency, complexity, and temporal structure of acoustic stimuli transmitted through water. Larval fish have simple brains compared to adults but swim freely and depend on sophisticated sensory processing for survival.1–5 Zebrafish larvae, an important model for studying brain-wide neural networks, have thus far been found to possess a rudimentary auditory system, sensitive to a narrow range of frequencies and without evident sensitivity to acoustic features that are salient and ethologically important to adult fish.6,7 Here, we have combined a novel method for delivering water-borne sounds, a diverse assembly of acoustic stimuli, and whole-brain calcium imaging to describe the responses of individual auditory-responsive neurons across the brains of zebrafish larvae. Our results reveal responses to frequencies ranging from 100 Hz to 4 kHz, with evidence of frequency discrimination from 100 Hz to 2.5 kHz. Frequency-selective neurons are located in numerous regions of the brain, and neurons responsive to the same frequency are spatially grouped in some regions. Using functional clustering, we identified categories of neurons that are selective for a single pure-tone frequency, white noise, the sharp onset of acoustic stimuli, and stimuli involving a gradual crescendo. These results suggest a more nuanced auditory system than has previously been described in larval fish and provide insights into how a young animal's auditory system can both function acutely and serve as the scaffold for a more complex adult system.

KW - acoustics

KW - auditory processing

KW - calcium imaging

KW - frequency selectivity

KW - GCaMP

KW - hearing

KW - light-sheet microscopy

KW - sound encoding

KW - tonotopy

KW - zebrafish

UR - http://www.scopus.com/inward/record.url?scp=85105318041&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2021.01.103

DO - 10.1016/j.cub.2021.01.103

M3 - Journal article

C2 - 33657408

AN - SCOPUS:85105318041

VL - 31

SP - 1977-1987.e4

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 9

ER -