Deflection of a vibrissa leads to a gradient of strain across mechanoreceptors in a mystacial follicle

Journal of Neurophysiology

Volumn 114, Issue 1, 2015, Pages 138-145

  Whiteley, Samuel J ^a,b   Knutsen, Per M ^b   Matthews, David W ^b   Kleinfeld, David ^b,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEUROBIOLOGY SECTION   (United States)

Author keywords

Biomechanics; Displacement; Merkel cells; Ringwulst; Somatosensation; Whisker

Indexed keywords

ION CHANNEL;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL TRACKING; LASER MICROSCOPY; MECHANORECEPTOR; MECHANOTRANSDUCTION; MERKEL CELL; MOUSE; NERVE ENDING; NONHUMAN; PARTICLE IMAGE VELOCIMETRY; PRIORITY JOURNAL; VIBRISSA; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; FACE; HAIR FOLLICLE; INNERVATION; PHYSICAL STIMULATION; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE; TOUCH; TRANSGENIC MOUSE;

ANIMALS; FACE; HAIR FOLLICLE; MECHANORECEPTORS; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PHYSICAL STIMULATION; TISSUE CULTURE TECHNIQUES; TOUCH; VIBRISSAE;

EID: 84939789380     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00179.2015     Document Type: Article

References (35)

1. Abraira VE, Ginty DD. The sensory neurons of touch. Neuron 79: 618-639, 2013.
2. Bagdasarian K, Szwed M, Knutsen PM, Deutsch D, Derdikman D, Pietr M, Simony E, Ahissar E. Pre-neuronal morphological processing of object location by individual whiskers. Nat Neurosci 16: 622-631, 2013.
3. Coste B, Mathur J, Schmidt M, Earley T. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330: 55-60, 2010.
4. da Silva S, Hasegawa H, Scott A, Zhou X, Wagner AK, Han BX, Wang F. Proper formation of whisker barrelettes requires periphery-derived Smad4- dependent TGF-beta signaling. Proc Natl Acad Sci USA 22: 3395-3400, 2011.
5. Ebara S, Kumamoto K, Matsuura T, Mazurkiewicz JE, Rice FL. Similarities and differences in the innervation of mystacial vibrissal follicle-sinus complexes in the rat and cat: a confocal microscopic study. J Comp Neurol 449: 103-119, 2002.
6. Fassihi A, Akrami A, Esmaeili V, Diamond ME. Tactile perception and working memory in rats and humans. Proc Natl Acad Sci USA 111: 2331-2336, 2014.
7. Gibson JM, Welker WI. Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 1. Receptive field properties and threshold distributions. Somatosens Res 1: 51-67, 1983.
8. Hill DN, Bermejo R, Zeigler HP, Kleinfeld D. Biomechanics of the vibrissa motor plant in rat: Rhythmic whisking consists of triphasic neuromuscular activity. J Neurosci 28: 3438-3455, 2008.
9. Hires SA, Pammer L, Svoboda K, Golomb D. Tapered whiskers are required for active tactile sensation. Elife 2: e01350, 2013.
10. Ikeda R, Cha M, Ling J, Jia Z, Coyle D, Gu JG. Merkel cells transduce and encode tactile stimuli to drive Aβ-afferent impulses. Cell 157: 664-675, 2014.
11. Ikeda R, Gu JG. Piezo2 channel conductance and localization domains in Merkel cells of rat whisker hair follicles. Neurosci Lett 583: 210-215, 2014.
12. Johnson KO. The roles and functions of cutaneous mechanoreceptors. Curr Opin Neurobiol 11: 455-461, 2001.
13. Jones LM, Depireux DA, Simons DJ, Keller A. Robust temporal coding in the trigeminal system. Science 204: 1986-1989, 2004.
14. Kleinfeld D, Delaney KR. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage sensitive dyes. J Comp Neurol 375: 89-108, 1996.
15. Krupa DJ, Matell MS, Brisben AJ, Oliveira LM, Nicolelis MA. Behavioral properties of the trigeminal somatosensory system in rats performing whisker- dependent tactile discriminations. J Neurosci 21: 5752-5763, 2001.
16. Landau LD, Lifshitz EM. Theory of Elasticity. New York: Plenum, 1959.
17. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L, Gong S, Jankowski MP, Luo W, Heintz N, Koerber HR, Woodbury CJ, Ginty DD. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147: 1615-1627, 2011.
18. Lichtenstein SH, Carvell GE, Simons DJ. Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosens Mot Res 7: 47-65, 1990.
19. Lou S, Duan B, Vong L, Lowell BB, Ma Q. Runx1 controls terminal morphology and mechanosensitivity of VGLUT3-expressing C-mechanoreceptors. J Neurosci 33: 870-882, 2013.
20. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala, HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140, 2010.
21. Maksimovic S, Nakatani M, Baba Y, Nelson AM, Marshall KL, Wellnitz S, Firozi P, Woo SH, Ranade S, Patapoutian A, EL. Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509: 617-621, 2014.
22. Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A, Bonhoeffer T, Hübener M, Griesbeck O. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5: 805-811, 2008.
23. Mitchinson B, Arabzadeh E, Diamond ME, Prescott TJ. Spike-timing in primary sensory neurons: a model of somatosensory transduction in the rat. Biol Cybern 98: 185-194, 2008.
24. Mitchinson B, Gurney KN, Redgrave P, Melhuish C, Pipe AG, Pearson M, Gilhespy I, Prescott TJ. Empirically inspired simulated electro-mechanical model of the rat mystacial follicle-sinus complex. Proc Biol Sci 271: 2509-2516, 2004.
25. O'Connor DH, Clack NG, Huber D, Komiyama T, Myers EW, Svoboda K. Vibrissa-based object localization in head-fixed mice. J Neurosci 30: 1947-1967, 2010.
26. Poole K, Herget R, Lapatsina L, Ngo HD, Lewin GR. Tuning Piezo ion channels to detect molecular-scale movements relevant for fine touch. Nat Commun 5: 3520, 2014.
27. Quist BW, Hartmann MJ. Mechanical signals at the base of a rat vibrissa: the effect of intrinsic vibrissa curvature and implications for tactile exploration. J Neurophysiol 107: 2298-2312, 2012.
28. Rice FL, Mance A, Munger BL. A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle-sinus complexes. J Comp Neurol 252: 154-174, 1986.
29. Rice FL, Munger BL. A comparative light microscopic analysis of the sensory innervation of the mystacial pad. II. The common fur between the vibrissae. J Comp Neurol 252: 186-205, 1986.
30. Sakurai K, Akiyama M, Cai B, Scott A, Han BX, Takatoh J, Sigrist M, Arber S, Wang F. The organization of submodality-specific touch afferent inputs in the vibrissa column. Cell Rep 5: 87-98, 2013.
31. Shoykhet M, Doherty D, Simons DJ. Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing. Somatosens Mot Res 17: 171-180, 2000.
32. Stüttgen MC, Rüter J, Schwarz C. Two psychophysical channels of whisker deflection in rats align with two neuronal classes of primary afferents. J Neurosci 26: 7933-7941, 2006.
33. Szwed M, Bagdasarian K, Ahissar E. Coding of vibrissal active touch. Neuron 40: 621-630, 2003.
34. Woodbury C, Koerber H. Central and peripheral anatomy of slowly adapting type I low-threshold mechanoreceptors innervating trunk skin of neonatal mice. J Comp Neurol 561: 547-561, 2007.
35. Wrobel K. Bau und Bedeutung der Blutsinus in den Vibrissen von Tupaia glis. Zentralblatt für Veterinärmedizin Reihe A 12: 888-899, 1965.