Neurophysiology of Tactile Perception : A Tribute to Steven Hsiao Computational modeling indicates that surface pressure can be reliably conveyed to tactile receptors even amidst changes in skin mechanics

Distinct patterns in neuronal firing are observed between classes of cutaneous afferents. Such differences may be attributed to end-organ morphology, distinct ion-channel complements, and skin microstructure, among other factors. Even for just the slowly adapting type I afferent, the skin's mechanics for a particular specimen might impact the afferent's firing properties, especially given the thickness and elasticity of skin can change dramatically over just days. Here, we show computationally that the skin can reliably convey indentation magnitude, rate, and spatial geometry to the locations of tactile receptors even amid changes in skin's structure. Using finite element analysis and neural dynamics models, we considered the skin properties of six mice that span a representative cohort. Modeling the propagation of the surface stimulus to the interior of the skin demonstrated that there can be large variance in stresses and strains near the locations of tactile receptors, which can lead to large variance in static firing rate. However, variance is significantly reduced when the stimulus tip is controlled by surface pressure and compressive stress is measured near the end organs. This particular transformation affords the least variability in predicted firing rates compared with others derived from displacement, force, strain energy density, or compressive strain. Amid changing skin mechanics, stimulus control by surface pressure may be more naturalistic and optimal and underlie how animals actively explore the tactile environment.

[1]  V. Mountcastle,et al.  NEURAL ACTIVITY IN MECHANORECEPTIVE CUTANEOUS AFFERENTS: STIMULUS-RESPONSE RELATIONS, WEBER FUNCTIONS, AND INFORMATION TRANSMISSION. , 1965, Journal of neurophysiology.

[2]  W. Smutz,et al.  A structural fingertip model for simulating of the biomechanics of tactile sensation. , 2004, Medical engineering & physics.

[3]  Gregory J. Gerling,et al.  Validating a Population Model of Tactile Mechanotransduction of Slowly Adapting Type I Afferents at Levels of Skin Mechanics, Single-Unit Response and Psychophysics , 2014, IEEE Transactions on Haptics.

[4]  J. Lévêque,et al.  Age-related mechanical properties of human skin: an in vivo study. , 1989, The Journal of investigative dermatology.

[5]  Gregory J. Gerling,et al.  Hyperelastic Material Properties of Mouse Skin under Compression , 2013, PloS one.

[6]  C H Daly,et al.  Age-related changes in the mechanical properties of human skin. , 1979, The Journal of investigative dermatology.

[7]  B H Pubols Factors affecting cutaneous mechanoreceptor response. I. Constant-force versus constant-displacement stimulation. , 1982, Journal of neurophysiology.

[8]  G. J. Gerling,et al.  Predicting SA-I mechanoreceptor spike times with a skin-neuron model. , 2009, Mathematical biosciences.

[9]  Carl T. Bergstrom,et al.  Theory, models and biology , 2015, eLife.

[10]  Alessandro Sanzeni,et al.  Tissue mechanics govern the rapidly adapting and symmetrical response to touch , 2015, Proceedings of the National Academy of Sciences.

[11]  K. O. Johnson,et al.  Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. , 1981, Journal of neurophysiology.

[12]  David J. Anderson,et al.  Ventromedial hypothalamic neurons control a defensive emotion state , 2015, eLife.

[13]  Sophia Mã ¶ ller,et al.  Biomechanics — Mechanical properties of living tissue , 1982 .

[14]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[15]  A. Goodwin,et al.  Representation of curved surfaces in responses of mechanoreceptive afferent fibers innervating the monkey's fingerpad , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  S. Cowin,et al.  Biomechanics: Mechanical Properties of Living Tissues, 2nd ed. , 1994 .

[17]  Mandayam A Srinivasan,et al.  Viscoelastic characterization of the primate finger pad in vivo by microstep indentation and three-dimensional finite element models for tactile sensation studies. , 2015, Journal of biomechanical engineering.

[18]  Ingvars Birznieks,et al.  Effects of changing skin mechanics on the differential sensitivity to surface compliance by tactile afferents in the human finger pad. , 2015, Journal of neurophysiology.

[19]  Lukas Kaim,et al.  Exploratory Strategies in Haptic Softness Discrimination Are Tuned to Achieve High Levels of Task Performance , 2011, IEEE Transactions on Haptics.

[20]  Yoshichika Baba,et al.  Epidermal Merkel Cells are Mechanosensory Cells that Tune Mammalian Touch Receptors , 2014, Nature.

[21]  G. J. Gerling,et al.  Fingerprint lines may not directly affect SA-I mechanoreceptor response , 2008, Somatosensory & motor research.

[22]  A. Bretag,et al.  Synthetic interstitial fluid for isolated mammalian tissue. , 1969, Life sciences.

[23]  A. Goodwin,et al.  Encoding of object curvature by tactile afferents from human fingers. , 1997, Journal of neurophysiology.

[24]  Yoshichika Baba,et al.  Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors , 2014, eLife.

[25]  Randall B Widelitz,et al.  Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. , 2009, The International journal of developmental biology.

[26]  R H LaMotte,et al.  Tensile and compressive responses of nociceptors in rat hairy skin. , 1997, Journal of neurophysiology.

[27]  Balasundar I Raju,et al.  3-D finite-element models of human and monkey fingertips to investigate the mechanics of tactile sense. , 2003, Journal of biomechanical engineering.

[28]  P. Khalsa,et al.  Encoding of compressive stress during indentation by slowly adapting type I mechanoreceptors in rat hairy skin. , 2002, Journal of neurophysiology.

[29]  R. Sivamani,et al.  Tribometrology of Skin , 2004 .

[30]  Ruth E. Baker,et al.  Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration , 2008, Nature.

[31]  Kenneth O. Johnson,et al.  A continuum mechanical model of mechanoreceptive afferent responses to indented spatial patterns. , 2006, Journal of neurophysiology.

[32]  A. W. Schopper,et al.  Nonlinear and viscoelastic characteristics of skin under compression: experiment and analysis. , 2003, Bio-medical materials and engineering.

[33]  R. Johansson,et al.  Factors influencing the force control during precision grip , 2004, Experimental Brain Research.

[34]  Y Lanir,et al.  Two-dimensional mechanical properties of rabbit skin. I. Experimental system. , 1974, Journal of biomechanics.

[35]  K. O. Johnson,et al.  Tactile spatial resolution. III. A continuum mechanics model of skin predicting mechanoreceptor responses to bars, edges, and gratings. , 1981, Journal of neurophysiology.

[36]  G. J. Gerling,et al.  The regularity of sustained firing reveals two populations of slowly adapting touch receptors in mouse hairy skin. , 2010, Journal of neurophysiology.

[37]  A. R. Muir,et al.  The structure and function of a slowly adapting touch corpuscle in hairy skin , 1969, The Journal of physiology.

[38]  K. O. Johnson,et al.  Human tactile pattern recognition: active versus passive touch, velocity effects, and patterns of confusion. , 1991, Journal of neurophysiology.

[39]  Cheng-Ming Chuong,et al.  Complex hair cycle domain patterns and regenerative hair waves in living rodents. , 2008, The Journal of investigative dermatology.

[40]  P. Gill,et al.  Sequential Quadratic Programming Methods , 2012 .

[41]  A W Goodwin,et al.  Effects of Nonuniform Fiber Sensitivity, Innervation Geometry, and Noise on Information Relayed by a Population of Slowly Adapting Type I Primary Afferents from the Fingerpad , 1999, The Journal of Neuroscience.

[42]  Gregory J. Gerling,et al.  Compressive Viscoelasticity of Freshly Excised Mouse Skin Is Dependent on Specimen Thickness, Strain Level and Rate , 2015, PloS one.