On the High Frequency Transfer of Mechanical Stimuli from the Surface of the Head to the Macular Neuroepithelium of the Mouse

Timothy A. Jones, Choongheon Lee, G. Christopher Gaines, J. W.“Wally” Grant

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Vestibular macular sensors are activated by a shearing motion between the otoconial membrane and underlying receptor epithelium. Shearing motion and sensory activation in response to an externally induced head motion do not occur instantaneously. The mechanically reactive elastic and inertial properties of the intervening tissue introduce temporal constraints on the transfer of the stimulus to sensors. Treating the otoconial sensory apparatus as an overdamped second-order mechanical system, we measured the governing long time constant (ΤL) for stimulus transfer from the head surface to epithelium. This provided the basis to estimate the corresponding upper cutoff for the frequency response curve for mouse otoconial organs. A velocity step excitation was used as the forcing function. Hypothetically, the onset of the mechanical response to a step excitation follows an exponential rise having the form Velshear = U(1-e−t/TL), where U is the applied shearing velocity step amplitude. The response time of the otoconial apparatus was estimated based on the activation threshold of macular neural responses to step stimuli having durations between 0.1 and 2.0 ms. Twenty adult C57BL/6 J mice were evaluated. Animals were anesthetized. The head was secured to a shaker platform using a non-invasive head clip or implanted skull screws. The shaker was driven to produce a theoretical forcing step velocity excitation at the otoconial organ. Vestibular sensory evoked potentials (VsEPs) were recorded to measure the threshold for macular neural activation. The duration of the applied step motion was reduced systematically from 2 to 0.1 ms and response threshold determined for each duration (nine durations). Hypothetically, the threshold of activation will increase according to the decrease in velocity transfer occurring at shorter step durations. The relationship between neural threshold and stimulus step duration was characterized. Activation threshold increased exponentially as velocity step duration decreased below 1.0 ms. The time constants associated with the exponential curve were ΤL = 0.50 ms for the head clip coupling and TL = 0.79 ms for skull screw preparation. These corresponded to upper −3 dB frequency cutoff points of approximately 318 and 201 Hz, respectively. TL ranged from 224 to 379 across individual animals using the head clip coupling. The findings were consistent with a second-order mass-spring mechanical system. Threshold data were also fitted to underdamped models post hoc. The underdamped fits suggested natural resonance frequencies on the order of 278 to 448 Hz as well as the idea that macular systems in mammals are less damped than generally acknowledged. Although estimated indirectly, it is argued that these time constants reflect largely if not entirely the mechanics of transfer to the sensory apparatus. The estimated governing time constant of 0.50 ms for composite data predicts high frequency cutoffs of at least 318 Hz for the intact otoconial apparatus of the mouse.

Original languageEnglish (US)
Pages (from-to)189-204
Number of pages16
JournalJARO - Journal of the Association for Research in Otolaryngology
Volume16
Issue number2
DOIs
StatePublished - Apr 1 2015

Fingerprint

Head
Surgical Instruments
Skull
Epithelium
Mechanics
Inbred C57BL Mouse
Evoked Potentials
Reaction Time
Mammals
Membranes

Keywords

  • frequency cutoff
  • mammal
  • mouse
  • otoconial organs
  • stimulus transfer
  • vestibular

ASJC Scopus subject areas

  • Otorhinolaryngology
  • Sensory Systems

Cite this

On the High Frequency Transfer of Mechanical Stimuli from the Surface of the Head to the Macular Neuroepithelium of the Mouse. / Jones, Timothy A.; Lee, Choongheon; Gaines, G. Christopher; Grant, J. W.“Wally”.

In: JARO - Journal of the Association for Research in Otolaryngology, Vol. 16, No. 2, 01.04.2015, p. 189-204.

Research output: Contribution to journalArticle

@article{4d71289964264d0180bb62ab9d4d421a,
title = "On the High Frequency Transfer of Mechanical Stimuli from the Surface of the Head to the Macular Neuroepithelium of the Mouse",
abstract = "Vestibular macular sensors are activated by a shearing motion between the otoconial membrane and underlying receptor epithelium. Shearing motion and sensory activation in response to an externally induced head motion do not occur instantaneously. The mechanically reactive elastic and inertial properties of the intervening tissue introduce temporal constraints on the transfer of the stimulus to sensors. Treating the otoconial sensory apparatus as an overdamped second-order mechanical system, we measured the governing long time constant (ΤL) for stimulus transfer from the head surface to epithelium. This provided the basis to estimate the corresponding upper cutoff for the frequency response curve for mouse otoconial organs. A velocity step excitation was used as the forcing function. Hypothetically, the onset of the mechanical response to a step excitation follows an exponential rise having the form Velshear = U(1-e−t/TL), where U is the applied shearing velocity step amplitude. The response time of the otoconial apparatus was estimated based on the activation threshold of macular neural responses to step stimuli having durations between 0.1 and 2.0 ms. Twenty adult C57BL/6 J mice were evaluated. Animals were anesthetized. The head was secured to a shaker platform using a non-invasive head clip or implanted skull screws. The shaker was driven to produce a theoretical forcing step velocity excitation at the otoconial organ. Vestibular sensory evoked potentials (VsEPs) were recorded to measure the threshold for macular neural activation. The duration of the applied step motion was reduced systematically from 2 to 0.1 ms and response threshold determined for each duration (nine durations). Hypothetically, the threshold of activation will increase according to the decrease in velocity transfer occurring at shorter step durations. The relationship between neural threshold and stimulus step duration was characterized. Activation threshold increased exponentially as velocity step duration decreased below 1.0 ms. The time constants associated with the exponential curve were ΤL = 0.50 ms for the head clip coupling and TL = 0.79 ms for skull screw preparation. These corresponded to upper −3 dB frequency cutoff points of approximately 318 and 201 Hz, respectively. TL ranged from 224 to 379 across individual animals using the head clip coupling. The findings were consistent with a second-order mass-spring mechanical system. Threshold data were also fitted to underdamped models post hoc. The underdamped fits suggested natural resonance frequencies on the order of 278 to 448 Hz as well as the idea that macular systems in mammals are less damped than generally acknowledged. Although estimated indirectly, it is argued that these time constants reflect largely if not entirely the mechanics of transfer to the sensory apparatus. The estimated governing time constant of 0.50 ms for composite data predicts high frequency cutoffs of at least 318 Hz for the intact otoconial apparatus of the mouse.",
keywords = "frequency cutoff, mammal, mouse, otoconial organs, stimulus transfer, vestibular",
author = "Jones, {Timothy A.} and Choongheon Lee and Gaines, {G. Christopher} and Grant, {J. W.“Wally”}",
year = "2015",
month = "4",
day = "1",
doi = "10.1007/s10162-014-0501-9",
language = "English (US)",
volume = "16",
pages = "189--204",
journal = "JARO - Journal of the Association for Research in Otolaryngology",
issn = "1525-3961",
publisher = "Springer New York",
number = "2",

}

TY - JOUR

T1 - On the High Frequency Transfer of Mechanical Stimuli from the Surface of the Head to the Macular Neuroepithelium of the Mouse

AU - Jones, Timothy A.

AU - Lee, Choongheon

AU - Gaines, G. Christopher

AU - Grant, J. W.“Wally”

PY - 2015/4/1

Y1 - 2015/4/1

N2 - Vestibular macular sensors are activated by a shearing motion between the otoconial membrane and underlying receptor epithelium. Shearing motion and sensory activation in response to an externally induced head motion do not occur instantaneously. The mechanically reactive elastic and inertial properties of the intervening tissue introduce temporal constraints on the transfer of the stimulus to sensors. Treating the otoconial sensory apparatus as an overdamped second-order mechanical system, we measured the governing long time constant (ΤL) for stimulus transfer from the head surface to epithelium. This provided the basis to estimate the corresponding upper cutoff for the frequency response curve for mouse otoconial organs. A velocity step excitation was used as the forcing function. Hypothetically, the onset of the mechanical response to a step excitation follows an exponential rise having the form Velshear = U(1-e−t/TL), where U is the applied shearing velocity step amplitude. The response time of the otoconial apparatus was estimated based on the activation threshold of macular neural responses to step stimuli having durations between 0.1 and 2.0 ms. Twenty adult C57BL/6 J mice were evaluated. Animals were anesthetized. The head was secured to a shaker platform using a non-invasive head clip or implanted skull screws. The shaker was driven to produce a theoretical forcing step velocity excitation at the otoconial organ. Vestibular sensory evoked potentials (VsEPs) were recorded to measure the threshold for macular neural activation. The duration of the applied step motion was reduced systematically from 2 to 0.1 ms and response threshold determined for each duration (nine durations). Hypothetically, the threshold of activation will increase according to the decrease in velocity transfer occurring at shorter step durations. The relationship between neural threshold and stimulus step duration was characterized. Activation threshold increased exponentially as velocity step duration decreased below 1.0 ms. The time constants associated with the exponential curve were ΤL = 0.50 ms for the head clip coupling and TL = 0.79 ms for skull screw preparation. These corresponded to upper −3 dB frequency cutoff points of approximately 318 and 201 Hz, respectively. TL ranged from 224 to 379 across individual animals using the head clip coupling. The findings were consistent with a second-order mass-spring mechanical system. Threshold data were also fitted to underdamped models post hoc. The underdamped fits suggested natural resonance frequencies on the order of 278 to 448 Hz as well as the idea that macular systems in mammals are less damped than generally acknowledged. Although estimated indirectly, it is argued that these time constants reflect largely if not entirely the mechanics of transfer to the sensory apparatus. The estimated governing time constant of 0.50 ms for composite data predicts high frequency cutoffs of at least 318 Hz for the intact otoconial apparatus of the mouse.

AB - Vestibular macular sensors are activated by a shearing motion between the otoconial membrane and underlying receptor epithelium. Shearing motion and sensory activation in response to an externally induced head motion do not occur instantaneously. The mechanically reactive elastic and inertial properties of the intervening tissue introduce temporal constraints on the transfer of the stimulus to sensors. Treating the otoconial sensory apparatus as an overdamped second-order mechanical system, we measured the governing long time constant (ΤL) for stimulus transfer from the head surface to epithelium. This provided the basis to estimate the corresponding upper cutoff for the frequency response curve for mouse otoconial organs. A velocity step excitation was used as the forcing function. Hypothetically, the onset of the mechanical response to a step excitation follows an exponential rise having the form Velshear = U(1-e−t/TL), where U is the applied shearing velocity step amplitude. The response time of the otoconial apparatus was estimated based on the activation threshold of macular neural responses to step stimuli having durations between 0.1 and 2.0 ms. Twenty adult C57BL/6 J mice were evaluated. Animals were anesthetized. The head was secured to a shaker platform using a non-invasive head clip or implanted skull screws. The shaker was driven to produce a theoretical forcing step velocity excitation at the otoconial organ. Vestibular sensory evoked potentials (VsEPs) were recorded to measure the threshold for macular neural activation. The duration of the applied step motion was reduced systematically from 2 to 0.1 ms and response threshold determined for each duration (nine durations). Hypothetically, the threshold of activation will increase according to the decrease in velocity transfer occurring at shorter step durations. The relationship between neural threshold and stimulus step duration was characterized. Activation threshold increased exponentially as velocity step duration decreased below 1.0 ms. The time constants associated with the exponential curve were ΤL = 0.50 ms for the head clip coupling and TL = 0.79 ms for skull screw preparation. These corresponded to upper −3 dB frequency cutoff points of approximately 318 and 201 Hz, respectively. TL ranged from 224 to 379 across individual animals using the head clip coupling. The findings were consistent with a second-order mass-spring mechanical system. Threshold data were also fitted to underdamped models post hoc. The underdamped fits suggested natural resonance frequencies on the order of 278 to 448 Hz as well as the idea that macular systems in mammals are less damped than generally acknowledged. Although estimated indirectly, it is argued that these time constants reflect largely if not entirely the mechanics of transfer to the sensory apparatus. The estimated governing time constant of 0.50 ms for composite data predicts high frequency cutoffs of at least 318 Hz for the intact otoconial apparatus of the mouse.

KW - frequency cutoff

KW - mammal

KW - mouse

KW - otoconial organs

KW - stimulus transfer

KW - vestibular

UR - http://www.scopus.com/inward/record.url?scp=84939993815&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84939993815&partnerID=8YFLogxK

U2 - 10.1007/s10162-014-0501-9

DO - 10.1007/s10162-014-0501-9

M3 - Article

C2 - 25648882

AN - SCOPUS:84939993815

VL - 16

SP - 189

EP - 204

JO - JARO - Journal of the Association for Research in Otolaryngology

JF - JARO - Journal of the Association for Research in Otolaryngology

SN - 1525-3961

IS - 2

ER -