The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors

Abstract

Touch sensation is critical for our social and environmental interactions. In mammals, most discriminative light touch sensation is mediated by the Aβ low-threshold mechanoreceptors. Cell bodies of Aβ low-threshold mechanoreceptors are located in the dorsal root ganglia and trigeminal ganglia, which extend a central projection innervating the spinal cord and brain stem and a peripheral projection innervating the specialized mechanosensory end organs. These specialized mechanosensory end organs include Meissner’s corpuscles, Pacinian corpuscles, lanceolate endings, Merkel cells, and Ruffini corpuscles. The morphologies and physiological properties of these mechanosensory end organs and their innervating neurons have been investigated for over a century. In addition, recent advances in mouse genetics have enabled the identification of molecular mechanisms underlying the development of Aβ low-threshold mechanoreceptors, which highlight the crucial roles of neurotrophic factor signaling and transcription factor activity in this process. Here, we will review the anatomy, physiological properties, and development of mammalian low-threshold Aβ mechanoreceptors.

Keywords

mechanoreceptor / Meissner’s corpuscle / Pacinian corpuscle / lanceolate ending / Merkel cell / Ruffini corpuscle / dorsal root ganglion

References

[1] Abdo H, Li L, Lallemend F, Bachy I, Xu X J, Rice F L, Ernfors P (2011). Dependence on the transcription factor Shox2 for specification of sensory neurons conveying discriminative touch. Eur J Neurosci, 34(10): 1529–1541

[2] Airaksinen M S, Koltzenburg M, Lewin G R, Masu Y, Helbig C, Wolf E, Brem G, Toyka K V, Thoenen H, Meyer M (1996). Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron, 16(2): 287–295

[3] Albrecht F L R P J (2008). Cutaneous Mechanisms of Tactile Perception: Morphological and Chemical Organization of the Innervation to the Skin. The Senses: A Comprehensive Reference. San Diego, Academic Press. 6: 1-32.

[4] Bell J, Bolanowski S, Holmes M H (1994). The structure and function of Pacinian corpuscles: a review. Prog Neurobiol, 42(1): 79–128

[5] Bentivoglio M, Pacini P (1995). Filippo Pacini: a determined observer. Brain Res Bull, 38(2): 161–165

[6] Biemesderfer D, Munger B L, Binck J, Dubner R (1978). The pilo-Ruffini complex: a non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin. Brain Res, 142(2): 197–222

[7] Boulais N, Misery L (2007). Merkel cells. J Am Acad Dermatol, 57(1): 147–165

[8] Bourane S, Garces A, Venteo S, Pattyn A, Hubert T, Fichard A, Puech S, Boukhaddaoui H, Baudet C, Takahashi S, Valmier J, Carroll P (2009). Low-threshold mechanoreceptor subtypes selectively express MafA and are specified by Ret signaling. Neuron, 64(6): 857–870

[9] Brisben A J, Hsiao S S, Johnson K O (1999). Detection of vibration transmitted through an object grasped in the hand. J Neurophysiol, 81(4): 1548–1558

[10] Brown A G (1981). Organization in the spinal cord: the anatomy and physiology of identified neurones. Berlin; New York, Springer-Verlag

[11] Brown A G, Fyffe R E, Noble R (1980). Projections from Pacinian corpuscles and rapidly adapting mechanoreceptors of glabrous skin to the cat’s spinal cord. J Physiol, 307: 385–400

[12] Burgess P R P E.R. (1973). Cutaneious mechanoreceptors and nociceptors. Handbook of Sensory Physiology. A. Iggo. Berlin, Springer. 11:29–78

[13] Byers M R (1985). Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffini-like mechanoreceptors and free nerve endings. J Comp Neurol, 231(4): 500–518

[14] Calavia M G, Feito J, López-Iglesias L, de Carlos F, García-Suarez O, Pérez-Piñera P, Cobo J, Vega J A (2010). The lamellar cells in human Meissner corpuscles express TrkB. Neurosci Lett, 468(2): 106–109

[15] Carroll P, Lewin G R, Koltzenburg M, Toyka K V, Thoenen H (1998). A role for BDNF in mechanosensation. Nat Neurosci, 1(1): 42–46

[16] Cauna N (1956). Nerve supply and nerve endings in Meissner’s corpuscles. Am J Anat, 99(2): 315–350

[17] Cauna N, Mannan G (1958). The structure of human digital pacinian corpuscles (corpus cula lamellosa) and its functional significance. J Anat, 92(1): 1–20

[18] Cauna N, Ross L L (1960). The fine structure of Meissner’s touch corpuscles of human fingers. J Biophys Biochem Cytol, 8(2): 467–482

[19] Chambers M R, Andres K H, von Duering M, Iggo A (1972). The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q J Exp Physiol Cogn Med Sci, 57(4): 417–445

[20] Cronk K M, Wilkinson G A, Grimes R, Wheeler E F, Jhaveri S, Fundin B T, Silos-Santiago I, Tessarollo L, Reichardt L F, Rice F L (2002). Diverse dependencies of developing Merkel innervation on the trkA and both full-length and truncated isoforms of trkC. Development, 129(15): 3739–3750

[21] Diamond J, Mills L R, Mearow K M (1988). Evidence that the Merkel cell is not the transducer in the mechanosensory Merkel cell-neurite complex. Prog Brain Res, 74: 51–56

[22] English K B, Burgess P R, Kavka-Van Norman D (1980). Development of rat Merkel cells. J Comp Neurol, 194(2): 475–496

[23] Fagan B M, Cahusac P M (2001). Evidence for glutamate receptor mediated transmission at mechanoreceptors in the skin. Neuroreport, 12(2): 341–347

[24] Fundin B T, Silos-Santiago I, Ernfors P, Fagan A M, Aldskogius H, DeChiara T M, Phillips H S, Barbacid M, Yancopoulos G D, Rice F L (1997). Differential dependency of cutaneous mechanoreceptors on neurotrophins, trk receptors, and P75 LNGFR. Dev Biol, 190(1): 94–116

[25] Gardner E P, Palmer C I (1990). Simulation of motion on the skin. III. Mechanisms used by rapidly adapting cutaneous mechanoreceptors in the primate hand for spatiotemporal resolution and two-point discrimination. J Neurophysiol, 63(4): 841–859

[26] González-Martínez T, Fariñas I, Del Valle M E, Feito J, Germanà G, Cobo J, Vega J A (2005). BDNF, but not NT-4, is necessary for normal development of Meissner corpuscles. Neurosci Lett, 377(1): 12–15

[27] González-Martínez T, Germanà G P, Monjil D F, Silos-Santiago I, de Carlos F, Germanà G, Cobo J, Vega J A (2004). Absence of Meissner corpuscles in the digital pads of mice lacking functional TrkB. Brain Res, 1002(1-2): 120–128

[28] Gottschaldt K M, Iggo A, Young D W (1973). Functional characteristics of mechanoreceptors in sinus hair follicles of the cat. J Physiol, 235(2): 287–315

[29] Gottschaldt K M, Vahle-Hinz C (1981). Merkel cell receptors: structure and transducer function. Science, 214(4517): 183–186

[30] Grim M, Halata Z (2000). Developmental origin of avian Merkel cells. Anat Embryol (Berl), 202(5): 401–410

[31] Haeberle H, Fujiwara M, Chuang J, Medina M M, Panditrao M V, Bechstedt S, Howard J, Lumpkin E A (2004). Molecular profiling reveals synaptic release machinery in Merkel cells. Proc Natl Acad Sci USA, 101(40): 14503–14508

[32] Halata Z (1977). The ultrastructure of the sensory nerve endings in the articular capsule of the knee joint of the domestic cat (Ruffini corpuscles and Pacinian corpuscles). J Anat, 124(Pt 3): 717–729

[33] Halata Z, Grim M, Bauman K I (2003). Friedrich Sigmund Merkel and his “Merkel cell”, morphology, development, and physiology: review and new results. Anat Rec A Discov Mol Cell Evol Biol, 271(1): 225–239

[34] Halata Z, Munger B L (1980). The sensory innervation of primate eyelid. Anat Rec, 198(4): 657–670

[35] Halata Z, Munger B L (1980). Sensory nerve endings in rhesus monkey sinus hairs. J Comp Neurol, 192(4): 645–663

[36] Heidenreich M, Lechner S G, Vardanyan V, Wetzel C, Cremers C W, De Leenheer E M, Aránguez G, Moreno-Pelayo M Á, Jentsch T J, Lewin G R (2012). KCNQ4 K(+) channels tune mechanoreceptors for normal touch sensation in mouse and man. Nat Neurosci, 15(1): 138–145

[37] Hoggan G, Hoggan F E (1893). Forked Nerve Endings on Hairs. J Anat Physiol, 27(Pt 2): 224–231

[38] Honma Y, Kawano M, Kohsaka S, Ogawa M (2010). Axonal projections of mechanoreceptive dorsal root ganglion neurons depend on Ret. Development, 137(14): 2319–2328

[39] Hoshino N, Harada F, Alkhamrah B A, Aita M, Kawano Y, Hanada K, Maeda T (2003). Involvement of brain-derived neurotrophic factor (BDNF) in the development of periodontal Ruffini endings. Anat Rec A Discov Mol Cell Evol Biol, 274(1): 807–816

[40] Hu J, Huang T, Li T, Guo Z, Cheng L (2012). c-Maf is required for the development of dorsal horn laminae III/IV neurons and mechanoreceptive DRG axon projections. J Neurosci, 32(16): 5362–5373

[41] Hubbard S J (1958). A study of rapid mechanical events in a mechanoreceptor. J Physiol, 141(2): 198–218

[42] Hunt C C (1961). On the nature of vibration receptors in the hind limb of the cat. J Physiol, 155: 175–186

[43] Iggo A (1985). Sensory receptors in the skin of mammals and their sensory functions. Rev Neurol (Paris), 141(10): 599–613

[44] Iggo A, Andres K H (1982). Morphology of cutaneous receptors. Annu Rev Neurosci, 5(1): 1–31

[45] Iggo A, Muir A R (1969). The structure and function of a slowly adapting touch corpuscle in hairy skin. J Physiol, 200(3): 763–796

[46] Iggo A, Ogawa H (1977). Correlative physiological and morphological studies of rapidly adapting mechanoreceptors in cat’s glabrous skin. J Physiol, 266(2): 275–296

[47] Ikeda I, Yamashita Y, Ono T, Ogawa H (1994). Selective phototoxic destruction of rat Merkel cells abolishes responses of slowly adapting type I mechanoreceptor units. J Physiol, 479(Pt 2): 247–256

[48] Johansson R S, Vallbo A B (1979). Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol, 286: 283–300

[49] Johnson K O (2001). The roles and functions of cutaneous mechanoreceptors. Curr Opin Neurobiol, 11(4): 455–461

[50] Johnson K O, Yoshioka T, Vega-Bermudez F (2000). Tactile functions of mechanoreceptive afferents innervating the hand. J Clin Neurophysiol, 17(6): 539–558

[51] Kinkelin I, Stucky C L, Koltzenburg M (1999). Postnatal loss of Merkel cells, but not of slowly adapting mechanoreceptors in mice lacking the neurotrophin receptor p75. Eur J Neurosci, 11(11): 3963–3969

[52] Knibestöl M (1973). Stimulus-response functions of rapidly adapting mechanoreceptors in human glabrous skin area. J Physiol, 232(3): 427–452

[53] Kramer I, Sigrist M, de Nooij J C, Taniuchi I, Jessell T M, Arber S (2006). A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron, 49(3): 379–393

[54] Krimm R F, Davis B M, Noel T, Albers K M (2006). Overexpression of neurotrophin 4 in skin enhances myelinated sensory endings but does not influence sensory neuron number. J Comp Neurol, 498(4): 455–465

[55] LeMaster A M, Krimm R F, Davis B M, Noel T, Forbes M E, Johnson J E, Albers K M (1999). Overexpression of brain-derived neurotrophic factor enhances sensory innervation and selectively increases neuron number. J Neurosci, 19(14): 5919–5931

[56] Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R, Bernstein Y, Goldenberg D, Xiao C, Fliegauf M, Kremer E, Otto F, Brenner O, Lev-Tov A, Groner Y (2002). The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J, 21(13): 3454–3463

[57] Li L, Rutlin M, Abraira V E, Cassidy C, Kus L, Gong S, Jankowski M P, Luo W, Heintz N, Koerber H R, Woodbury C J, Ginty D D (2011). The functional organization of cutaneous low-threshold mechanosensory neurons. Cell, 147(7): 1615–1627

[58] Loewenstein W R, Mendelson M (1965). Components of Receptor Adaptation in a Pacinian Corpuscle. J Physiol, 177: 377–397

[59] Lou S, Duan B, Vong L, Lovell B B, Ma Q (2013). Runx1 controls terminal morphology and mechanosensitivity of VGLUT3-expressing C-mechanoreceptors. J Neurosci, 33(3): 870–882

[60] Lucarz A, Brand G (2007). Current considerations about Merkel cells. Eur J Cell Biol, 86(5): 243–251

[61] Luo W, Enomoto H, Rice F L, Milbrandt J, Ginty D D (2009). Molecular identification of rapidly adapting mechanoreceptors and their developmental dependence on ret signaling. Neuron, 64(6): 841–856

[62] Maklad A, Conway M, Hodges C, Hansen L A (2010). Development of innervation to maxillary whiskers in mice. Anat Rec (Hoboken), 293(9): 1553–1567

[63] Maksimovic S, Baba Y, Lumpkin E A (2013). Neurotransmitters and synaptic components in the Merkel cell-neurite complex, a gentle-touch receptor. Ann N Y Acad Sci, 1279(1): 13–21

[64] Maricich S M, Morrison K M, Mathes E L, Brewer B M (2012). Rodents rely on Merkel cells for texture discrimination tasks. J Neurosci, 32(10): 3296–3300

[65] Maricich S M, Wellnitz S A, Nelson A M, Lesniak D R, Gerling G J, Lumpkin E A, Zoghbi H Y (2009). Merkel cells are essential for light-touch responses. Science, 324(5934): 1580–1582

[66] Maruyama Y, Harada F, Jabbar S, Saito I, Aita M, Kawano Y, Suzuki A, Nozawa-Inoue K, Maeda T (2005). Neurotrophin-4/5-depletion induces a delay in maturation of the periodontal Ruffini endings in mice. Arch Histol Cytol, 68(4): 267–288

[67] Matsuo S, Ichikawa H, Silos-Santiago I, Kiyomiya K, Kurebe M, Arends J J, Jacquin M F (2002). Ruffini endings are absent from the periodontal ligament of trkB knockout mice. Somatosens Mot Res, 19(3): 213–217

[68] Mendelson M, Lowenstein W R (1964). Mechanisms of Receptor Adaptation. Science, 144(3618): 554–555

[69] Merkel F (1875). Tastzellen and Tastkoerperchen bei den Hausthieren und beim Menschen. Arch Mikrosc Anat, 11(S1): 636–652

[70] Montaño J A, Pérez-Piñera P, García-Suárez O, Cobo J, Vega J A (2010). Development and neuronal dependence of cutaneous sensory nerve formations: Lessons from neurotrophins. Microsc Res Tech, 73(5): 513–529

[71] Morrison K M, Miesegaes G R, Lumpkin E A, Maricich S M (2009). Mammalian Merkel cells are descended from the epidermal lineage. Dev Biol, 336(1): 76–83

[72] Mosconi T M, Rice F L, Song M J (1993). Sensory innervation in the inner conical body of the vibrissal follicle-sinus complex of the rat. J Comp Neurol, 328(2): 232–251

[73] Mountcastle V B (1957). Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol, 20(4): 408–434

[74] Munger B L, Ide C (1988). The structure and function of cutaneous sensory receptors. Arch Histol Cytol, 51(1): 1–34

[75] Nakamura S, Senzaki K, Yoshikawa M, Nishimura M, Inoue K, Ito Y, Ozaki S, Shiga T (2008). Dynamic regulation of the expression of neurotrophin receptors by Runx3. Development, 135(9): 1703–1711

[76] Ogawa H (1996). The Merkel cell as a possible mechanoreceptor cell. Prog Neurobiol, 49(4): 317–334

[77] Palmer C I, Gardner E P (1990). Simulation of motion on the skin. IV. Responses of Pacinian corpuscle afferents innervating the primate hand to stripe patterns on the OPTACON. J Neurophysiol, 64(1): 236–247

[78] Paré M, Behets C, Cornu O (2003). Paucity of presumptive ruffini corpuscles in the index finger pad of humans. J Comp Neurol, 456(3): 260–266

[79] Paré M, Elde R, Mazurkiewicz J E, Smith A M, Rice F L (2001). The Meissner corpuscle revised: a multiafferented mechanoreceptor with nociceptor immunochemical properties. J Neurosci, 21(18): 7236–7246

[80] Paré M, Smith A M, Rice F L (2002). Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey. J Comp Neurol, 445(4): 347–359

[81] Pease D C, Pallie W (1959). Electron microscopy of digital tactile corpuscles and small cutaneous nerves. J Ultrastruct Res, 2(3): 352–365

[82] Pease D C, Quilliam T A (1957). Electron microscopy of the pacinian corpuscle. J Biophys Biochem Cytol, 3(3): 331–342

[83] Perez-Pinera P, García-Suarez O, Germanà A, Díaz-Esnal B, de Carlos F, Silos-Santiago I, del Valle M E, Cobo J, Vega J A (2008). Characterization of sensory deficits in TrkB knockout mice. Neurosci Lett, 433(1): 43–47

[84] Peters E M, Botchkarev V A, Müller-Röver S, Moll I, Rice F L, Paus R (2002). Developmental timing of hair follicle and dorsal skin innervation in mice. J Comp Neurol, 448(1): 28–52

[85] Quilliam T A, Sato M (1955). The distribution of myelin on nerve fibres from Pacinian corpuscles. J Physiol, 129(1): 167–176

[86] Rasmusson D D, Turnbull B G (1986). Sensory innervation of the raccoon forepaw: 2. Response properties and classification of slowly adapting fibers. Somatosens Res, 4(1): 63–75

[87] Rice F L, Rasmusson D D (2000). Innervation of the digit on the forepaw of the raccoon. J Comp Neurol, 417(4): 467–490

[88] Sato M (1961). Response of Pacinian corpuscles to sinusoidal vibration. J Physiol, 159: 391–409

[89] Saxod R (1996). Ontogeny of the cutaneous sensory organs. Microsc Res Tech, 34(4): 313–333

[90] Scheibel M E, Scheibel A B (1968). Terminal axonal patterns in cat spinal cord. II. The dorsal horn. Brain Res, 9(1): 32–58

[91] Scheibert J, Leurent S, Prevost A, Debrégeas G (2009). The role of fingerprints in the coding of tactile information probed with a biomimetic sensor. Science, 323(5920): 1503–1506

[92] Scott A, Hasegawa H, Sakural K, Yaron A, Cobb J, Wang F (2011). Transcription factor short stature homeobox 2 is required for proper development of tropomyosin-related kinase B-expressing mechanosensory neurons. J Neurosci, 31(18): 6741–6749

[93] Sedý J, Tseng S, Walro J M, Grim M, Kucera J (2006). ETS transcription factor ER81 is required for the Pacinian corpuscle development. Dev Dyn, 235(4): 1081–1089

[94] Semba K, Masarachia P, Malamed S, Jacquin M, Harris S, Egger M D (1984). Ultrastructure of pacinian corpuscle primary afferent terminals in the cat spinal cord. Brain Res, 302(1): 135–150

[95] Semba K, Masarachia P, Malamed S, Jacquin M, Harris S, Yang G, Egger M D (1985). An electron microscopic study of terminals of rapidly adapting mechanoreceptive afferent fibers in the cat spinal cord. J Comp Neurol, 232(2): 229–240

[96] Senok S S, Baumann K I (1997). Functional evidence for calcium-induced calcium release in isolated rat vibrissal Merkel cell mechanoreceptors. J Physiol, 500(Pt 1): 29–37

[97] Senok S S, Baumann K I, Halata Z (1996). Selective phototoxic destruction of quinacrine-loaded Merkel cells is neither selective nor complete. Exp Brain Res, 110(3): 325–334

[98] Senzaki K, Ozaki S, Yoshikawa M, Ito Y, Shiga T (2010). Runx3 is required for the specification of TrkC-expressing mechanoreceptive trigeminal ganglion neurons. Mol Cell Neurosci, 43(3): 296–307

[99] Shortland P, Woolf C J (1993). Morphology and somatotopy of the central arborizations of rapidly adapting glabrous skin afferents in the rat lumbar spinal cord. J Comp Neurol, 329(4): 491–511

[100] Skaper S D (2012). The neurotrophin family of neurotrophic factors: an overview. Methods Mol Biol, 846: 1–12

[101] Suzuki M, Ebara S, Koike T, Tonomura S, Kumamoto K (2012). How many hair follicles are innervated by one afferent axon? A confocal microscopic analysis of palisade endings in the auricular skin of thy1-YFP transgenic mouse. Proc Jpn Acad, Ser B, Phys Biol Sci, 88(10): 583–595

[102] Szeder V, Grim M, Halata Z, Sieber-Blum M (2003). Neural crest origin of mammalian Merkel cells. Dev Biol, 253(2): 258–263

[103] Tachibana T, Nawa T (2002). Recent progress in studies on Merkel cell biology. Anat Sci Int, 77(1): 26–33

[104] Takahashi-Iwanaga H (2000). Three-dimensional microanatomy of longitudinal lanceolate endings in rat vibrissae. J Comp Neurol, 426(2): 259–269

[105] Talbot W H, Darian-Smith I, Kornhuber H H, Mountcastle V B (1968). The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. J Neurophysiol, 31(2): 301–334

[106] Tapper D N (1965). Stimulus-response relationships in the cutaneous slowly-adapting mechanoreceptor in hairy skin of the cat. Exp Neurol, 13(4): 364–385

[107] Wellnitz S A, Lesniak D R, Gerling G J, Lumpkin E A (2010). The regularity of sustained firing reveals two populations of slowly adapting touch receptors in mouse hairy skin. J Neurophysiol, 103(6): 3378–3388

[108] Wende H, Lechner S G, Cheret C, Bourane S, Kolanczyk M E, Pattyn A, Reuter K, Munier F L, Carroll P, Lewin G R, Birchmeier C (2012). The transcription factor c-Maf controls touch receptor development and function. Science, 335(6074): 1373–1376

[109] Willis W D, Coggeshall R E (2004). Sensory Mechanisms of the Spinal Cord. New York, Kluwer Academic/Plenum Publishers

[110] Winkelmann R K, Breathnach A S (1973). The Merkel cell. J Invest Dermatol, 60(1): 2–15

[111] Woo S H, Baba Y, Franco A M, Lumpkin E A, Owens D M (2012). Excitatory glutamate is essential for development and maintenance of the piloneural mechanoreceptor. Development, 139(4): 740–748

[112] Woodbury C J, Ritter A M, Koerber H R (2001). Central anatomy of individual rapidly adapting low-threshold mechanoreceptors innervating the “hairy” skin of newborn mice: early maturation of hair follicle afferents. J Comp Neurol, 436(3): 304–323

[113] Yamashita Y, Akaike N, Wakamori M, Ikeda I, Ogawa H (1992). Voltage-dependent currents in isolated single Merkel cells of rats. J Physiol, 450: 143–162

[114] Yoshikawa M, Murakami Y, Senzaki K, Masuda T, Ozaki S, Ito Y, Shiga T (2013). Coexpression of Runx1 and Runx3 in mechanoreceptive dorsal root ganglion neurons. Dev Neurobiol, 73(6): 469–479

[115] Zelená J (1978). The development of Pacinian corpuscles. J Neurocytol, 7(1): 71–91

[116] Zelena J (1994). Nerves and Mechanoreceptors. London, Chapman & Hall

[117] Zelená J, Halata Z, Szeder V, Grim M (1997). Crural Herbst corpuscles in chicken and quail: numbers and structure. Anat Embryol (Berl), 196(4): 323–333

[118] Zelená J, Jirmanová I, Nitatori T, Ide C (1990). Effacement and regeneration of tactile lamellar corpuscles of rat after postnatal nerve crush. Neuroscience, 39(2): 513–522

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg