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

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  • Published:
Frontiers in Biology

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.

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References

  • 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

    Article  PubMed  Google Scholar 

  • Airaksinen MS, 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Bell J, Bolanowski S, Holmes MH (1994). The structure and function of Pacinian corpuscles: a review. Prog Neurobiol, 42(1): 79–128

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Brown A G (1981). Organization in the Spinal Cord: the Anatomy and Physiology of Identified Neurones. Berlin, New York: Springer-Verlag

    Book  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fundin B T, Silos-Santiago I, Ernfors P, Fagan A M, Aldskogius H, DeChiara TM, 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heidenreich M, Lechner S G, Vardanyan V, Wetzel C, Cremers CW, De Leenheer EM, 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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Li L, Rutlin M, Abraira V E, Cassidy C, Kus L, Gong S, Jankowski MP, 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

    Article  CAS  PubMed  Google Scholar 

  • Loewenstein W R, Mendelson M (1965). Components of receptor adaptation in a Pacinian corpuscle. J Physiol, 177: 377–397

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maricich SM, Morrison KM, Mathes E L, Brewer BM(2012). Rodents rely on Merkel cells for texture discrimination tasks. J Neurosci, 32(10): 3296–3300

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wende H, Lechner S G, Cheret C, Bourane S, Kolanczyk ME, 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

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zelena J (1994). Nerves and Mechanoreceptors. London, Chapman & Hall

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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  1. Department of Neuroscience, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, 19014, USA

    Michael S. Fleming & Wenqin Luo

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  1. Michael S. Fleming
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  2. Wenqin Luo
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Correspondence to Wenqin Luo.

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Fleming, M.S., Luo, W. The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors. Front. Biol. 8, 408–420 (2013). https://doi.org/10.1007/s11515-013-1271-1

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  • DOI: https://doi.org/10.1007/s11515-013-1271-1

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