Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs

Loranzie S. Rogers; Jacey C. Van Wert; Allen F. Mensinger

doi:10.1152/jn.00483.2021

Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs

Loranzie S. Rogers, Jacey C. Van Wert, Allen F. Mensinger

Research output: Contribution to journal › Article › peer-review

2 Scopus citations

Abstract

The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish (Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0–12.5 cm/s; acceleration: 0.2–2.6 cm/s²) and while fish freely swam (velocity: 3.5–18.6 cm/s; acceleration: 0.8–29.8 cm/s²). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming.

Original language	English (US)
Pages (from-to)	364-377
Number of pages	14
Journal	Journal of neurophysiology
Volume	128
Issue number	2
DOIs	https://doi.org/10.1152/jn.00483.2021
State	Published - Aug 2022
Externally published	Yes

Bibliographical note

Funding Information:
The authors acknowledge the Marine Resources Center staff at the Marine Biological Laboratory for providing toadfish care. The authors also acknowledge Dr. Joseph Sisneros for helpful comments on the manuscript, Dr. Geoffrey Boynton for statistical consultation, and Dr. Steve Zottoli for providing the image of the toadfish brain and inner ear used in Fig. 1B. Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 & 1659604 (to A. F. Mensinger) and by the National Science Foundation Graduate Research Fellowship Program DGE 1762114 (to L. S. Rogers). All experimental procedures conformed to NIH guidelines for animal care and use of animals and were approved by the Marine Biological Laboratories Institutional Animal Care and Use Committee.

Funding Information:
Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 & 1659604 (to A. F. Mensinger) and by the National Science Foundation Graduate Research Fellowship Program DGE 1762114 (to L. S. Rogers). All experimental procedures conformed to NIH guidelines for animal care and use of animals and were approved by the Marine Biological Laboratories Institutional Animal Care and Use Committee.

Publisher Copyright:
© 2022 American Physiological Society. All rights reserved.

Keywords

auditory
fish hearing
swimming
utricle
vestibular

PubMed: MeSH publication types

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Access

10.1152/jn.00483.2021

OpenUrl availability

Full text

Cite this

@article{b48ccb4883ea446280405f573c957d8e,

title = "Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs",

abstract = "The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish (Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0–12.5 cm/s; acceleration: 0.2–2.6 cm/s2) and while fish freely swam (velocity: 3.5–18.6 cm/s; acceleration: 0.8–29.8 cm/s2). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming.",

keywords = "auditory, fish hearing, swimming, utricle, vestibular",

author = "Rogers, {Loranzie S.} and {Van Wert}, {Jacey C.} and Mensinger, {Allen F.}",

note = "Funding Information: The authors acknowledge the Marine Resources Center staff at the Marine Biological Laboratory for providing toadfish care. The authors also acknowledge Dr. Joseph Sisneros for helpful comments on the manuscript, Dr. Geoffrey Boynton for statistical consultation, and Dr. Steve Zottoli for providing the image of the toadfish brain and inner ear used in Fig. 1B. Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 & 1659604 (to A. F. Mensinger) and by the National Science Foundation Graduate Research Fellowship Program DGE 1762114 (to L. S. Rogers). All experimental procedures conformed to NIH guidelines for animal care and use of animals and were approved by the Marine Biological Laboratories Institutional Animal Care and Use Committee. Funding Information: Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 & 1659604 (to A. F. Mensinger) and by the National Science Foundation Graduate Research Fellowship Program DGE 1762114 (to L. S. Rogers). All experimental procedures conformed to NIH guidelines for animal care and use of animals and were approved by the Marine Biological Laboratories Institutional Animal Care and Use Committee. Publisher Copyright: {\textcopyright} 2022 American Physiological Society. All rights reserved.",

year = "2022",

month = aug,

doi = "10.1152/jn.00483.2021",

language = "English (US)",

volume = "128",

pages = "364--377",

journal = "Journal of neurophysiology",

issn = "0022-3077",

publisher = "American Physiological Society",

number = "2",

}

TY - JOUR

T1 - Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs

AU - Rogers, Loranzie S.

AU - Van Wert, Jacey C.

AU - Mensinger, Allen F.

N1 - Funding Information: The authors acknowledge the Marine Resources Center staff at the Marine Biological Laboratory for providing toadfish care. The authors also acknowledge Dr. Joseph Sisneros for helpful comments on the manuscript, Dr. Geoffrey Boynton for statistical consultation, and Dr. Steve Zottoli for providing the image of the toadfish brain and inner ear used in Fig. 1B. Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 & 1659604 (to A. F. Mensinger) and by the National Science Foundation Graduate Research Fellowship Program DGE 1762114 (to L. S. Rogers). All experimental procedures conformed to NIH guidelines for animal care and use of animals and were approved by the Marine Biological Laboratories Institutional Animal Care and Use Committee. Funding Information: Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 & 1659604 (to A. F. Mensinger) and by the National Science Foundation Graduate Research Fellowship Program DGE 1762114 (to L. S. Rogers). All experimental procedures conformed to NIH guidelines for animal care and use of animals and were approved by the Marine Biological Laboratories Institutional Animal Care and Use Committee. Publisher Copyright: © 2022 American Physiological Society. All rights reserved.

PY - 2022/8

Y1 - 2022/8

N2 - The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish (Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0–12.5 cm/s; acceleration: 0.2–2.6 cm/s2) and while fish freely swam (velocity: 3.5–18.6 cm/s; acceleration: 0.8–29.8 cm/s2). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming.

AB - The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish (Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0–12.5 cm/s; acceleration: 0.2–2.6 cm/s2) and while fish freely swam (velocity: 3.5–18.6 cm/s; acceleration: 0.8–29.8 cm/s2). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming.

KW - auditory

KW - fish hearing

KW - swimming

KW - utricle

KW - vestibular

UR - http://www.scopus.com/inward/record.url?scp=85135596194&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85135596194&partnerID=8YFLogxK

U2 - 10.1152/jn.00483.2021

DO - 10.1152/jn.00483.2021

M3 - Article

C2 - 35830608

AN - SCOPUS:85135596194

SN - 0022-3077

VL - 128

SP - 364

EP - 377

JO - Journal of neurophysiology

JF - Journal of neurophysiology

IS - 2

ER -

Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this