Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2013, Vol. 8 Issue (4) : 408-420    https://doi.org/10.1007/s11515-013-1271-1
REVIEW
The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors
Michael S. FLEMING, Wenqin LUO()
Department of Neuroscience, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19014, USA
 Download: PDF(310 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
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     
Corresponding Author(s): LUO Wenqin,Email:luow@mail.med.upenn.edu   
Issue Date: 01 August 2013
 Cite this article:   
Michael S. FLEMING,Wenqin LUO. The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors[J]. Front Biol, 2013, 8(4): 408-420.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-013-1271-1
https://academic.hep.com.cn/fib/EN/Y2013/V8/I4/408
Fig.1  Illustration to demonstrate the morphologies and physiological properties of mammalian Aβ low-threshold mechanoreceptors. In glabrous skin (left side of the illustration), Meissner’s corpuscles are located in the dermal papillae of the dermis, Merkel cells are located in the basal epidermis, Ruffini corpuscles are located in the dermis, and Pacinian corpuscles are located in the dermis, deeper than the other mechanosensory end organs. In hairy skin (right side of the illustration), hair follicles are surrounded by lanceolate endings and Merkel cells. The bottom panel shows the neural activity of different types of Aβ low-threshold mechanoreceptors in response to a sustained stimulus. Meissner’s corpuscle, Pacinian corpuscle and lanceolate ending mechanoreceptors display rapidly adapting mechanosensitive physiological properties, while Merkel cell and Ruffini corpuscle mechanoreceptors display slowly adapting mechanosensitive properties, which fire action potentials (APs) throughout the duration of the stimulus.
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
doi: 10.1111/j.1460-9568.2011.07883.x pmid:22103411
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
doi: 10.1016/S0896-6273(00)80047-1 pmid:8789944
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
doi: 10.1016/0301-0082(94)90022-1 pmid:7480788
5 Bentivoglio M, Pacini P (1995). Filippo Pacini: a determined observer. Brain Res Bull , 38(2): 161–165
doi: 10.1016/0361-9230(95)00083-Q pmid:7583342
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
doi: 10.1016/0006-8993(78)90631-5 pmid:415796
7 Boulais N, Misery L (2007). Merkel cells. J Am Acad Dermatol , 57(1): 147–165
doi: 10.1016/j.jaad.2007.02.009 pmid:17412453
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
doi: 10.1016/j.neuron.2009.12.004 pmid:20064392
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
pmid:10200190
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
pmid:7205669
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
doi: 10.1002/cne.902310408 pmid:3968252
14 Calavia M G, Feito J, López-Iglesias L, de Carlos F, García-Suarez O, Pérez-Pi?era P, Cobo J, Vega J A (2010). The lamellar cells in human Meissner corpuscles express TrkB. Neurosci Lett , 468(2): 106–109
doi: 10.1016/j.neulet.2009.10.076 pmid:19879330
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
doi: 10.1038/242 pmid:10195107
16 Cauna N (1956). Nerve supply and nerve endings in Meissner’s corpuscles. Am J Anat , 99(2): 315–350
doi: 10.1002/aja.1000990206 pmid:13372495
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
pmid:13513492
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
doi: 10.1083/jcb.8.2.467 pmid:13691669
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
pmid:4484588
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
pmid:12117822
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
doi: 10.1016/S0079-6123(08)62997-0 pmid:3055053
22 English K B, Burgess P R, Kavka-Van Norman D (1980). Development of rat Merkel cells. J Comp Neurol , 194(2): 475–496
doi: 10.1002/cne.901940212 pmid:7440811
23 Fagan B M, Cahusac P M (2001). Evidence for glutamate receptor mediated transmission at mechanoreceptors in the skin. Neuroreport , 12(2): 341–347
doi: 10.1097/00001756-200102120-00032 pmid:11209947
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
doi: 10.1006/dbio.1997.8658 pmid:9331334
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
pmid:2341881
26 González-Martínez T, Fari?as 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
doi: 10.1016/j.neulet.2004.11.078 pmid:15722178
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
doi: 10.1016/j.brainres.2004.01.003 pmid:14988041
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
pmid:4763992
29 Gottschaldt K M, Vahle-Hinz C (1981). Merkel cell receptors: structure and transducer function. Science , 214(4517): 183–186
doi: 7280690" target="_blank">10.1126/science. pmid:7280690 pmid:7280690
30 Grim M, Halata Z (2000). Developmental origin of avian Merkel cells. Anat Embryol (Berl) , 202(5): 401–410
doi: 10.1007/s004290000121 pmid:11089931
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
doi: 10.1073/pnas.0406308101 pmid:15448211
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
pmid:604339
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
doi: 10.1002/ar.a.10029 pmid:12552639
34 Halata Z, Munger B L (1980). The sensory innervation of primate eyelid. Anat Rec , 198(4): 657–670
doi: 10.1002/ar.1091980410 pmid:7212315
35 Halata Z, Munger B L (1980). Sensory nerve endings in rhesus monkey sinus hairs. J Comp Neurol , 192(4): 645–663
doi: 10.1002/cne.901920403 pmid:7419748
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
doi: 10.1038/nn.2985 pmid:22101641
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
doi: 10.1242/dev.046995 pmid:20534675
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
doi: 10.1002/ar.a.10094 pmid:12923891
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
pmid:13539833
42 Hunt C C (1961). On the nature of vibration receptors in the hind limb of the cat. J Physiol , 155: 175–186
pmid:13716841
43 Iggo A (1985). Sensory receptors in the skin of mammals and their sensory functions. Rev Neurol (Paris) , 141(10): 599–613
pmid:4089395
44 Iggo A, Andres K H (1982). Morphology of cutaneous receptors. Annu Rev Neurosci , 5(1): 1–31
doi: 10.1146/annurev.ne.05.030182.000245 pmid:6280572
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
pmid:4974746
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
pmid:853451
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
pmid:7799224
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
pmid:439026
49 Johnson K O (2001). The roles and functions of cutaneous mechanoreceptors. Curr Opin Neurobiol , 11(4): 455–461
doi: 10.1016/S0959-4388(00)00234-8 pmid:11502392
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
doi: 10.1097/00004691-200011000-00002 pmid:11151974
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
doi: 10.1046/j.1460-9568.1999.00822.x pmid:10583485
52 Knibest?l M (1973). Stimulus-response functions of rapidly adapting mechanoreceptors in human glabrous skin area. J Physiol , 232(3): 427–452
pmid:4759677
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
doi: 10.1016/j.neuron.2006.01.008 pmid:16446142
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
doi: 10.1002/cne.21074 pmid:16937395
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
pmid:10407031
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
doi: 10.1093/emboj/cdf370 pmid:12093746
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
doi: 10.1016/j.cell.2011.11.027 pmid:22196735
58 Loewenstein W R, Mendelson M (1965). Components of Receptor Adaptation in a Pacinian Corpuscle. J Physiol , 177: 377–397
pmid:14321486
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
doi: 10.1016/j.ejcb.2007.02.001 pmid:17337089
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
doi: 10.1016/j.neuron.2009.11.003 pmid:20064391
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
doi: 10.1002/ar.21194 pmid:20648571
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
doi: 10.1111/nyas.12057 pmid:23530998
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
doi: 10.1523/JNEUROSCI.5307-11.2012 pmid:22399751
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
doi: 10.1126/science.1172890 pmid:19541997
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
doi: 10.1679/aohc.68.267 pmid:16477147
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
doi: 10.1080/0899022021000009134 pmid:12396578
68 Mendelson M, Lowenstein W R (1964). Mechanisms of Receptor Adaptation. Science , 144(3618): 554–555
doi: 10.1126/science.144.3618.554 pmid:14194104
69 Merkel F (1875). Tastzellen and Tastkoerperchen bei den Hausthieren und beim Menschen. Arch Mikrosc Anat , 11(S1): 636–652
doi: 10.1007/BF02933819
70 Monta?o J A, Pérez-Pi?era 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
pmid:19839059
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
doi: 10.1016/j.ydbio.2009.09.032 pmid:19782676
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
doi: 10.1002/cne.903280206 pmid:8423242
73 Mountcastle V B (1957). Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol , 20(4): 408–434
pmid:13439410
74 Munger B L, Ide C (1988). The structure and function of cutaneous sensory receptors. Arch Histol Cytol , 51(1): 1–34
doi: 10.1679/aohc.51.1 pmid:3137944
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
doi: 10.1242/dev.015248 pmid:18385258
76 Ogawa H (1996). The Merkel cell as a possible mechanoreceptor cell. Prog Neurobiol , 49(4): 317–334
pmid:8888113
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
pmid:2388068
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
doi: 10.1002/cne.10519 pmid:12528190
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
pmid:11549734
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
doi: 10.1002/cne.10196 pmid:11920712
81 Pease D C, Pallie W (1959). Electron microscopy of digital tactile corpuscles and small cutaneous nerves. J Ultrastruct Res , 2(3): 352–365
doi: 10.1016/S0022-5320(59)80007-1 pmid:13655354
82 Pease D C, Quilliam T A (1957). Electron microscopy of the pacinian corpuscle. J Biophys Biochem Cytol , 3(3): 331–342
doi: 10.1083/jcb.3.3.331 pmid:13438918
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
doi: 10.1016/j.neulet.2007.12.035 pmid:18248898
84 Peters E M, Botchkarev V A, Müller-R?ver 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
doi: 10.1002/cne.10212 pmid:12012374
85 Quilliam T A, Sato M (1955). The distribution of myelin on nerve fibres from Pacinian corpuscles. J Physiol , 129(1): 167–176
pmid:13252591
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
doi: 10.3109/07367228609144598 pmid:3797915
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
doi: 10.1002/(SICI)1096-9861(20000221)417:4<467::AID-CNE6>3.0.CO;2-Q pmid:10701867
88 Sato M (1961). Response of Pacinian corpuscles to sinusoidal vibration. J Physiol , 159: 391–409
pmid:14497425
89 Saxod R (1996). Ontogeny of the cutaneous sensory organs. Microsc Res Tech , 34(4): 313–333
doi: 10.1002/(SICI)1097-0029(19960701)34:4<313::AID-JEMT4>3.0.CO;2-P pmid:8807616
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
doi: 10.1016/0006-8993(68)90256-4 pmid:5699822
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
doi: 10.1126/science.1166467 pmid:19179493
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 Sedy 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
doi: 10.1002/dvdy.20710 pmid:16493690
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
doi: 10.1016/0006-8993(84)91293-9 pmid:6203612
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
doi: 10.1002/cne.902320208 pmid:3973092
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
pmid:9097930
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
doi: 10.1007/BF00229133 pmid:8871092
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
doi: 10.1016/j.mcn.2009.12.003 pmid:20034568
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
doi: 10.1002/cne.903290406 pmid:8454737
100 Skaper S D (2012). The neurotrophin family of neurotrophic factors: an overview. Methods Mol Biol , 846: 1–12
doi: 10.1007/978-1-61779-536-7_1 pmid:22367796
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
doi: 10.2183/pjab.88.583 pmid:23229751
102 Szeder V, Grim M, Halata Z, Sieber-Blum M (2003). Neural crest origin of mammalian Merkel cells. Dev Biol , 253(2): 258–263
doi: 10.1016/S0012-1606(02)00015-5 pmid:12645929
103 Tachibana T, Nawa T (2002). Recent progress in studies on Merkel cell biology. Anat Sci Int , 77(1): 26–33
doi: 10.1046/j.0022-7722.2002.00008.x pmid:12418081
104 Takahashi-Iwanaga H (2000). Three-dimensional microanatomy of longitudinal lanceolate endings in rat vibrissae. J Comp Neurol , 426(2): 259–269
doi: 10.1002/1096-9861(20001016)426:2<259::AID-CNE7>3.0.CO;2-N pmid:10982467
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
pmid:4972033
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
doi: 10.1016/0014-4886(65)90125-1 pmid:5847283
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
doi: 10.1152/jn.00810.2009 pmid:20393068
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
doi: 10.1126/science.1214314 pmid:22345400
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
doi: 10.1111/1523-1747.ep13069480 pmid:4346159
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
doi: 10.1242/dev.070847 pmid:22241839
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
doi: 10.1002/cne.1069 pmid:11438932
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
pmid:1331421
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
doi: 10.1002/dneu.22073 pmid:23378040
115 Zelená J (1978). The development of Pacinian corpuscles. J Neurocytol , 7(1): 71–91
doi: 10.1007/BF01213461 pmid:632855
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
doi: 10.1007/s004290050101 pmid:9363854
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
doi: 10.1016/0306-4522(90)90287-E pmid:2087271
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed