Modelling the mechanoreceptor’s dynamic behaviour

Zhuoyi Song, Robert W. Banks, Guy S. Bewick

Research output: Contribution to journalArticle

4 Citations (Scopus)
5 Downloads (Pure)

Abstract

All sensory receptors adapt, i.e. they constantly adjust their sensitivity to external stimuli to match the current demands of the natural environment. Electrophysiological responses of sensory receptors from widely different modalities seem to exhibit common features related to adaptation, and these features can be used to examine the underlying sensory transduction mechanisms. Among the principal senses, mechanosensation remains the least understood at the cellular level. To gain greater insights into mechanosensory signalling, we investigated if mechanosensation displayed adaptive dynamics that could be explained by similar biophysical mechanisms in other sensory modalities. To do this, we adapted a fly photoreceptor model to describe the primary transduction process for a stretch-sensitive mechanoreceptor, taking into account the viscoelastic properties of the accessory muscle fibres and the biophysical properties of known mechanosensitive channels (MSCs). The model's output is in remarkable agreement with the electrical properties of a primary ending in an isolated decapsulated spindle; ramp-and-hold stretch evokes a characteristic pattern of potential change, consisting of a large dynamic depolarization during the ramp phase and a smaller static depolarization during the hold phase. The initial dynamic component is likely to be caused by a combination of the mechanical properties of the muscle fibres and a refractory state in the MSCs. Consistent with the literature, the current model predicts that the dynamic component is due to a rapid stress increase during the ramp. More novel predictions from the model are the mechanisms to explain the initial peak in the dynamic component. At the onset of the ramp, all MSCs are sensitive to external stimuli, but as they become refractory (inactivated), fewer MSCs are able to respond to the continuous stretch, causing a sharp decrease after the peak response. The same mechanism could contribute a faster component in the ‘sensory habituation’ of mechanoreceptors, in which a receptor responds more strongly to the first stimulus episode during repetitive stimulation.
Original languageEnglish
Pages (from-to)243-254
Number of pages12
JournalJournal of Anatomy
Volume227
Issue number2
Early online date25 Jun 2015
DOIs
Publication statusPublished - Aug 2015

Fingerprint

mechanoreceptors
Architectural Accessibility
Mechanoreceptors
sensory receptors
Sensory Receptor Cells
muscle fibers
modeling
muscle
habituation
electrical properties
Muscles
electrical property
photoreceptors
Diptera
dynamic models
mechanical properties
mechanical property
receptors
prediction
fibre

Keywords

  • biophysical model
  • fly photoreceptor
  • refractory period
  • sensory adaptation
  • sensory habituation
  • stochastic adaptive sampling
  • stretch-sensitive mechanoreceptor

Cite this

Modelling the mechanoreceptor’s dynamic behaviour. / Song, Zhuoyi; Banks, Robert W.; Bewick, Guy S.

In: Journal of Anatomy, Vol. 227, No. 2, 08.2015, p. 243-254.

Research output: Contribution to journalArticle

Song, Zhuoyi ; Banks, Robert W. ; Bewick, Guy S. / Modelling the mechanoreceptor’s dynamic behaviour. In: Journal of Anatomy. 2015 ; Vol. 227, No. 2. pp. 243-254.
@article{f2927e9781e548fd9170c02b7ca0c7ac,
title = "Modelling the mechanoreceptor’s dynamic behaviour",
abstract = "All sensory receptors adapt, i.e. they constantly adjust their sensitivity to external stimuli to match the current demands of the natural environment. Electrophysiological responses of sensory receptors from widely different modalities seem to exhibit common features related to adaptation, and these features can be used to examine the underlying sensory transduction mechanisms. Among the principal senses, mechanosensation remains the least understood at the cellular level. To gain greater insights into mechanosensory signalling, we investigated if mechanosensation displayed adaptive dynamics that could be explained by similar biophysical mechanisms in other sensory modalities. To do this, we adapted a fly photoreceptor model to describe the primary transduction process for a stretch-sensitive mechanoreceptor, taking into account the viscoelastic properties of the accessory muscle fibres and the biophysical properties of known mechanosensitive channels (MSCs). The model's output is in remarkable agreement with the electrical properties of a primary ending in an isolated decapsulated spindle; ramp-and-hold stretch evokes a characteristic pattern of potential change, consisting of a large dynamic depolarization during the ramp phase and a smaller static depolarization during the hold phase. The initial dynamic component is likely to be caused by a combination of the mechanical properties of the muscle fibres and a refractory state in the MSCs. Consistent with the literature, the current model predicts that the dynamic component is due to a rapid stress increase during the ramp. More novel predictions from the model are the mechanisms to explain the initial peak in the dynamic component. At the onset of the ramp, all MSCs are sensitive to external stimuli, but as they become refractory (inactivated), fewer MSCs are able to respond to the continuous stretch, causing a sharp decrease after the peak response. The same mechanism could contribute a faster component in the ‘sensory habituation’ of mechanoreceptors, in which a receptor responds more strongly to the first stimulus episode during repetitive stimulation.",
keywords = "biophysical model, fly photoreceptor, refractory period, sensory adaptation, sensory habituation, stochastic adaptive sampling, stretch-sensitive mechanoreceptor",
author = "Zhuoyi Song and Banks, {Robert W.} and Bewick, {Guy S.}",
note = "Acknowledgements This study was funded by an EPSRC-funded 2020 Science Fellowship (EP/I017909/1). Z.S would like to thank the organisers for the invitation to present at the symposium ‘A Mechano-reception to Celebrate Bob Banks’ Career in Stretching the Imagination’. This paper summarizes the contents of the talk given at the symposium.",
year = "2015",
month = "8",
doi = "10.1111/joa.12328",
language = "English",
volume = "227",
pages = "243--254",
journal = "Journal of Anatomy",
issn = "0021-8782",
publisher = "Wiley-Blackwell",
number = "2",

}

TY - JOUR

T1 - Modelling the mechanoreceptor’s dynamic behaviour

AU - Song, Zhuoyi

AU - Banks, Robert W.

AU - Bewick, Guy S.

N1 - Acknowledgements This study was funded by an EPSRC-funded 2020 Science Fellowship (EP/I017909/1). Z.S would like to thank the organisers for the invitation to present at the symposium ‘A Mechano-reception to Celebrate Bob Banks’ Career in Stretching the Imagination’. This paper summarizes the contents of the talk given at the symposium.

PY - 2015/8

Y1 - 2015/8

N2 - All sensory receptors adapt, i.e. they constantly adjust their sensitivity to external stimuli to match the current demands of the natural environment. Electrophysiological responses of sensory receptors from widely different modalities seem to exhibit common features related to adaptation, and these features can be used to examine the underlying sensory transduction mechanisms. Among the principal senses, mechanosensation remains the least understood at the cellular level. To gain greater insights into mechanosensory signalling, we investigated if mechanosensation displayed adaptive dynamics that could be explained by similar biophysical mechanisms in other sensory modalities. To do this, we adapted a fly photoreceptor model to describe the primary transduction process for a stretch-sensitive mechanoreceptor, taking into account the viscoelastic properties of the accessory muscle fibres and the biophysical properties of known mechanosensitive channels (MSCs). The model's output is in remarkable agreement with the electrical properties of a primary ending in an isolated decapsulated spindle; ramp-and-hold stretch evokes a characteristic pattern of potential change, consisting of a large dynamic depolarization during the ramp phase and a smaller static depolarization during the hold phase. The initial dynamic component is likely to be caused by a combination of the mechanical properties of the muscle fibres and a refractory state in the MSCs. Consistent with the literature, the current model predicts that the dynamic component is due to a rapid stress increase during the ramp. More novel predictions from the model are the mechanisms to explain the initial peak in the dynamic component. At the onset of the ramp, all MSCs are sensitive to external stimuli, but as they become refractory (inactivated), fewer MSCs are able to respond to the continuous stretch, causing a sharp decrease after the peak response. The same mechanism could contribute a faster component in the ‘sensory habituation’ of mechanoreceptors, in which a receptor responds more strongly to the first stimulus episode during repetitive stimulation.

AB - All sensory receptors adapt, i.e. they constantly adjust their sensitivity to external stimuli to match the current demands of the natural environment. Electrophysiological responses of sensory receptors from widely different modalities seem to exhibit common features related to adaptation, and these features can be used to examine the underlying sensory transduction mechanisms. Among the principal senses, mechanosensation remains the least understood at the cellular level. To gain greater insights into mechanosensory signalling, we investigated if mechanosensation displayed adaptive dynamics that could be explained by similar biophysical mechanisms in other sensory modalities. To do this, we adapted a fly photoreceptor model to describe the primary transduction process for a stretch-sensitive mechanoreceptor, taking into account the viscoelastic properties of the accessory muscle fibres and the biophysical properties of known mechanosensitive channels (MSCs). The model's output is in remarkable agreement with the electrical properties of a primary ending in an isolated decapsulated spindle; ramp-and-hold stretch evokes a characteristic pattern of potential change, consisting of a large dynamic depolarization during the ramp phase and a smaller static depolarization during the hold phase. The initial dynamic component is likely to be caused by a combination of the mechanical properties of the muscle fibres and a refractory state in the MSCs. Consistent with the literature, the current model predicts that the dynamic component is due to a rapid stress increase during the ramp. More novel predictions from the model are the mechanisms to explain the initial peak in the dynamic component. At the onset of the ramp, all MSCs are sensitive to external stimuli, but as they become refractory (inactivated), fewer MSCs are able to respond to the continuous stretch, causing a sharp decrease after the peak response. The same mechanism could contribute a faster component in the ‘sensory habituation’ of mechanoreceptors, in which a receptor responds more strongly to the first stimulus episode during repetitive stimulation.

KW - biophysical model

KW - fly photoreceptor

KW - refractory period

KW - sensory adaptation

KW - sensory habituation

KW - stochastic adaptive sampling

KW - stretch-sensitive mechanoreceptor

U2 - 10.1111/joa.12328

DO - 10.1111/joa.12328

M3 - Article

VL - 227

SP - 243

EP - 254

JO - Journal of Anatomy

JF - Journal of Anatomy

SN - 0021-8782

IS - 2

ER -