Skin relaxation predicts neural firing rate adaptation in SAI touch receptors

Abstract

In response to ramp-and-hold indentation, the slowly-adapting type I (SAI) afferent exhibits an exponential decrease in its firing frequency during the hold phase. Such adaptation may be tied to skin relaxation but is neither well understood nor has it been quantitatively modeled. The specific hypothesis of this work is that skin relaxation is a primary contributor to observed changes in firing rate. Double exponential functions were fit to 21 responses from a mouse SAI afferent for both instantaneous firing rate and indenter tip force over time. The model was then generalized by using a linear transformation between fit parameters for force and firing rate data, allowing prediction of firing rates from force. The results show that the generalized model matches the recorded firing rate (R2 = 0.65) equally well as fitting a double-exponential function directly to firing rate (R2 = 0.67) for a second dataset. When the procedure was repeated with two D-hair fibers, the generalized model matched the recorded firing rate (R2 = 0.47) much more poorly compared to the fitted double-exponential function (R2 = 0.89). Thus, firing rate adaptation in SAI responses can be predicted by skin relaxation, whereas this factor alone did not adequately describe adaptation in the D-hair.

Force sensor in simulated skin and neural model mimic tactile SAI afferent spiking response to ramp and hold stimuli

“…As the magnitude of indentation increased from 1.2 mm (indentation type III ), 1.3 mm ( IV ), to 1.4 mm ( V ) the spiking-sensor model predicted a trend of increased spike firing, evident from decreasing average ISI s (98.81, 54.51, 41.11 ms respectively) within the static hold phase (Figure 8b). These predictions fit favorably (mean stat_FSS  = 0.925) to those observed average static ISI s (93.31, 36.28, 29.89 ms respectively) and agree with works by Mountcastle et al [33] and Ge and Khalsa [29]. Mountcastle et al [33] demonstrated a roughly positive and linear relationship between stimulus displacement magnitude and firing rate reported by SAI afferents in the macaque monkey.…”

“…The cylindrical tip’s dimensions were 14 mm height by 20 mm diameter. The use of this particular tip size and shape ensured that an equal state of normal stress was applied over the entire sensing area surface of the embedded sensor and minimized the out-of-plane shear stress [29]. These conditions thereby matched those for the mouse SAI afferent.…”

Active Touch and Self-Motion Encoding by Merkel Cell-Associated Afferents

“…We therefore hypothesized that sensitivity to both M 0 and $M_0^{\prime }$ arose from tissue viscoelasticity (cf. (Fraser et al, 2006; Williams et al., 2010)).…”

“…The excellent fit between data and model suggests that filtering of contact stresses by tissue viscoelasticity underlies spike rate adaptation, and thus plays a central role in determining the activity of Merkel and SA afferents (Williams et al, 2010). …”

Impact of Skin Hyper- and Visco-elastic Properties on Neural Mechanotransduction of the Slowly Adapting Type I Afferent

“…As interstitial fluid plays an important role in skin's viscoelasticity, the change of its amount and how the fluid is distributed within the tissue causes different relaxation behaviors. The increase of instantaneous modulus observed as the rate of loading increases may tend to agree, as well, with electrophysiological recordings from tactile mechanoreceptors where increased probe velocity yields higher firing rates from slowly adapting type I afferents [31], [32], though the neuron itself may play a role apart from the skin's response. This result may suggest a need to control loading velocity in electrophysiological experiments.…”