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.
Highlights
Biological sensory receptors have to constantly adapt to effectively represent the great variation of input intensities in their intrinsically limited output range
Simulated results from the current modelling framework can be compared against both experimental measurements and simulation results from previous models
We present here some scientific insights gained from simulating the stochastic adaptive sampling model for mechanosensitive channels (MSCs) in a mammalian muscle spindle
Summary
Biological sensory receptors have to constantly adapt to effectively represent the great variation of input intensities in their intrinsically limited output range (van Hateren & van der Schaaf, 1996). The significant differences in the input and output ranges impose common engineering objectives on all sensory systems: how to effectively represent. The vast input intensity changes within a limited output range so that faint signals are not buried in the noise, nor is the system completely saturated under intense stimuli (van Hateren & van der Schaaf, 1996; Rieke & Rudd, 2009). There are no commonly accepted explanations of how various steps work together to produce the temporal dynamics to even the simplest step-like stimuli (De Palo et al 2013), where adaptation could happen in multiple timescales (Wark et al 2009). Part of the reason is because transduction cascades in different sensory modalities have notable differences in the molecular components and their reaction mechanisms, which add to the complexities in comparing biophysical mechanisms associated with sensory adaptation
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