A Unifying Framework Underlying Mechanotransduction in the Somatosensory System

Abstract

Rodents use their whiskers to sense their surroundings. As most of the information available to the somatosensory system originates in whiskers' primary afferents, it is essential to understand the transformation of whisker motion into neuronal activity. Here, we combined in vivo recordings in anesthetized rats with mathematical modeling to ascertain the mechanical and electrical characteristics of mechanotransduction. We found that only two synergistic processes, which reflect the dynamic interactions between (1) receptor and whisker and (2) receptor and surrounding tissue, are needed to describe mechanotransduction during passive whiskers deflection. Interactions between these processes may account for stimulus-dependent changes in the magnitude and temporal pattern of tactile responses on multiple scales. Thus, we are able to explain complex electromechanical processes underlying sensory transduction using a simple model, which captures the responses of a wide range of mechanoreceptor types to diverse sensory stimuli. This compact and precise model allows for a ubiquitous description of how mechanoreceptors encode tactile stimulus.

Parallel coding schemes of whisker velocity in the rat's somatosensory system

“…Neuron classification into the three cell types was described in detail elsewhere (Lottem and Azouz 2011). Briefly, rapidly adapting (RA) neurons respond to step stimuli with a phasic response.…”

“…The two SA subtypes are similar, however, in that all SA neurons show directional selectivity, and both subtypes show a clear dependence of initial firing rates on whisker velocity. (For further distinguishing parameters between the cell types, see Lottem and Azouz 2011).…”

“…This, however, does not exclude the possibility that neurons may also represent tactile features by their spike timing. Substantial evidence from trigeminal ganglion (TG) neurons Jones et al 2004;Lottem and Azouz 2011;Shoykhet et al 2000;Stuttgen et al 2006), from the somatosensory thalamus (Deschenes et al 2003;Petersen et al 2008), and from primary somatosensory cortex neurons (Arabzadeh et al 2005Panzeri et al 2001;Petersen et al 2002b;Pinto et al 2000), have shown that neuronal responses in the somatosensory system are precise and reliable and can follow the fine temporal features of the stimulus (Deschenes et al 2003;Ewert et al 2008), suggesting that relevant tactile information may be represented in neuronal temporal patterns.…”

Tactile perception and working memory in rats and humans

“…Second, noisy vibrissal stimuli evoke a more robust cortical response (37,38), an advantage for future neurophysiological studies. Third, the structure of the noise stimulus is well suited to reverse correlation methods (39) and will provide rich data for studying the kinematic features extracted by sensory neurons (40,41).…”

Decoupling kinematics and mechanics reveals coding properties of trigeminal ganglion neurons in the rat vibrissal system

“…Accordingly, previous work has focused on quantifying the response of Vg neurons in terms of kinematic (geometric) variables of contact, including radial distance to an object, angular position, and angular velocity (Gibson and Welker, 1983a, 1983b; Jones et al, 2004a, 2004b; Leiser and Moxon, 2007; Lichtenstein et al, 1990; Lottem and Azouz, 2009, 2011; Lottem et al, 2015; Shoykhet et al, 2000, 2003; Szwed et al, 2003, 2006). …”