An inter-species computational analysis of vibrotactile sensitivity in Pacinian and Herbst corpuscles

Vibration sensing is ubiquitous among vertebrates, with the sensory end organ generally being a multilayered ellipsoidal structure. There is, however, a wide range of sizes and structural arrangements across species. In this work, we applied our earlier computational model of the Pacinian corpuscle to predict the sensory response of different species to various stimulus frequencies, and based on the results, we identified the optimal frequency for vibration sensing and the bandwidth over which frequencies should be most detectable. We found that although the size and layering of the corpuscles were very different, almost all of the 19 species studied showed very similar sensitivity ranges. The human and goose were the notable exceptions, with their corpuscle tuned to higher frequencies (130–170 versus 40–50 Hz). We observed no correlation between animal size and any measure of corpuscle geometry in our model. Based on the results generated by our computational model, we hypothesize that lamellar corpuscles across different species may use different sizes and structures to achieve similar frequency detection bands.

[1]  K. Catania Born Knowing: Tentacled Snakes Innately Predict Future Prey Behavior , 2010, PloS one.

[2]  T. Quilliam Unit Design and Array Patterns in Receptor Organs , 2008 .

[3]  J. Soley,et al.  General morphology of the oral cavity of the Nile crocodile, Crocodylus niloticus (Laurenti, 1768). II. The tongue. , 2004, The Onderstepoort journal of veterinary research.

[4]  S. Ebara,et al.  Distribution of pacinian corpuscles in the hand of the monkey, Macaca fuscata. , 1993, Journal of anatomy.

[5]  Mandayam A. Srinivasan,et al.  Multiscale Layered Biomechanical Model of the Pacinian Corpuscle , 2015, IEEE Transactions on Haptics.

[6]  M. Risling,et al.  Distribution of Human Pacinian Corpuscles in the Hand , 1998, Journal of hand surgery.

[7]  Julia C. Quindlen,et al.  Computational Parametric Analysis of the Mechanical Response of Structurally Varying Pacinian Corpuscles. , 2017, Journal of biomechanical engineering.

[8]  A. Deane,et al.  Mechanoreceptivity of Prehensile Tail Skin Varies Between Ateline and Cebine Primates , 2011, Anatomical record.

[9]  J. Vega,et al.  Development of Meissner‐like and Pacinian sensory corpuscles in the mouse demonstrated with specific markers for corpuscular constituents , 2000, The Anatomical record.

[10]  R. Saxod Ontogeny of the cutaneous sensory organs , 1996, Microscopy research and technique.

[11]  Jizhe Hao,et al.  Multiple Desensitization Mechanisms of Mechanotransducer Channels Shape Firing of Mechanosensory Neurons , 2010, The Journal of Neuroscience.

[12]  S J Bolanowski,et al.  Intensity and frequency characteristics of pacinian corpuscles. III. Effects of tetrodotoxin on transduction process. , 1984, Journal of neurophysiology.

[13]  T. Fujita,et al.  Oral sensory papillae, chemo- and mechano-receptors, in the snake, Elaphe quadrivirgata. A light and electron microscopic study. , 2000, Archives of histology and cytology.

[14]  R. T. Verrillo,et al.  Investigation of Some Parameters of the Cutaneous Threshold for Vibration , 1962 .

[15]  S. Huggenberger,et al.  Histological and ultrastructural aspects of the nasal complex in the harbour porpoise, Phocoena phocoena , 2009, Journal of morphology.

[16]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[17]  T. Hildebrandt,et al.  The distribution, density and three‐dimensional histomorphology of Pacinian corpuscles in the foot of the Asian elephant (Elephas maximus) and their potential role in seismic communication , 2007, Journal of anatomy.

[18]  K. Gottschaldt,et al.  Thermosensitivity and its possible fine‐structural basis in mechanoreceptors in the beak skin of geese , 1982, The Journal of comparative neurology.

[19]  M. Düring,et al.  The fine structure of lamellated receptors in the skin of Rana Esculenta , 2004, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[20]  Matthew D. Johnson,et al.  A multiphysics model of the Pacinian corpuscle. , 2016, Integrative biology : quantitative biosciences from nano to macro.

[21]  Sarah S. Kienle,et al.  Eye, Nose, Hair, and Throat: External Anatomy of the Head of a Neonate Gray Whale (Cetacea, Mysticeti, Eschrichtiidae) , 2015, Anatomical record.

[22]  J. F. Dammann,et al.  The Effect of Surface Wave Propagation on Neural Responses to Vibration in Primate Glabrous Skin , 2012, PloS one.

[23]  Ellen T. Bloom,et al.  Micropipette aspiration of the Pacinian corpuscle. , 2017, Journal of biomechanics.

[24]  S J Bolanowski,et al.  Immunocytochemical identification of proteins within the Pacinian corpuscle. , 2000, Somatosensory & motor research.

[25]  B. Munger,et al.  A re-evaluation of the cytology of cat Pacinian corpuscles , 1988, Cell and Tissue Research.

[26]  K. Andres,et al.  Morphology of cutaneous receptors. , 1982, Annual review of neuroscience.

[27]  J. Bell,et al.  The structure and function of pacinian corpuscles: A review , 1994, Progress in Neurobiology.

[28]  J J Zwislocki,et al.  Intensity and frequency characteristics of pacinian corpuscles. I. Action potentials. , 1984, Journal of neurophysiology.

[29]  A. Feldman,et al.  Length–mass allometry in snakes , 2013 .

[30]  Julia C. Quindlen-Hotek,et al.  Computational and Psychophysical Experiments on the Pacinian Corpuscle's Ability to Discriminate Complex Stimuli , 2019, IEEE Transactions on Haptics.

[31]  H. Berkhoudt The Morphology and Distribution of Cutaneous Mechanoreceptors (Herbst and Grandry Corpuscles) in Bill and Tongue of the Mallard (Anas Platyrhynchos L.) , 1979 .

[32]  E. K. Sawyer,et al.  Organization of the spinal trigeminal nucleus in star‐nosed moles , 2014, The Journal of comparative neurology.

[33]  D. Pease,et al.  ELECTRON MICROSCOPY OF THE PACINIAN CORPUSCLE , 1957, The Journal of biophysical and biochemical cytology.

[34]  Werner R. Loewenstein,et al.  THE SITES FOR MECHANO-ELECTRIC CONVERSION IN A PACINIAN CORPUSCLE , 1958, The Journal of general physiology.

[35]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[36]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[37]  Kerstin Pingel,et al.  50 Years of Image Analysis , 2012 .

[38]  R. Winkelmann,et al.  The histochemistry and morphology of the cutaneous sensory end‐organs of the chicken , 1961, The Journal of comparative neurology.

[39]  J. Gregory An electrophysiological investigation of the receptor apparatus of the duck's bill , 1973, The Journal of physiology.

[40]  A re-evaluation of the cytology of cat Pacinian corpuscles , 1988, Cell and Tissue Research.

[41]  M. Hasegawa,et al.  A time‐calibrated phylogenetic approach to assessing the phylogeography, colonization history and phenotypic evolution of snakes in the Japanese Izu Islands , 2011 .

[42]  E. R. Schneider,et al.  Evolutionary Specialization of Tactile Perception in Vertebrates. , 2016, Physiology.

[43]  P. Marasco,et al.  Fine structure of Eimer's organ in the coast mole (Scapanus orarius) , 2007, Anatomical record.

[44]  Julia C. Quindlen-Hotek,et al.  A finite-element model of mechanosensation by a Pacinian corpuscle cluster in human skin , 2018, Biomechanics and modeling in mechanobiology.

[45]  R. Skalak,et al.  Mechanical transmission in a Pacinian corpuscle. An analysis and a theory , 1966, The Journal of physiology.

[46]  K. Gottschaldt,et al.  Mechanoreceptors and their properties in the beak skin of geese (Anser anser). , 1974, Brain research.

[47]  A. Mcintyre,et al.  Vibration-evoked responses from lamellated corpuscles in the legs of kangaroos , 2004, Experimental Brain Research.

[48]  J. Kaas,et al.  Somatosensory fovea in the star‐nosed mole: Behavioral use of the star in relation to innervation patterns and cortical representation , 1997, The Journal of comparative neurology.

[49]  U Schumacher,et al.  Lectin and Proteoglycan Histochemistry of Feline Pacinian Corpuscles , 2001, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[50]  M. Potter,et al.  Remote touch prey-detection by Madagascar crested ibises Lophotibis cristata urschi , 2010 .

[51]  J. Soley,et al.  Morphological Features of Herbst Corpuscles in the Oropharynx of the Ostrich (Struthio camelus) and Emu (Dromaius novaehollandiae) , 2015, Anatomical record.