Skip to main content
Log in

Morphology and chemical characteristics of subepithelial laminar nerve endings in the rat epiglottic mucosa

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

The laminar nerve endings are distributed in the laryngeal mucosa, and described as sensory receptors evoked by laryngeal pressure changes. The present study aimed to determine detailed morphological characteristics of the laryngeal laminar endings of the rat. Immunohistochemistry for Na+-K+-ATPase, α3 subunit, showed that laminar endings were distributed in the entire laryngeal surface of the epiglottis. The parent axons of the endings were thick in diameter, and they were branched and continued to the endings. In some cases, several endings from different parent axons fused into a large complex structure of 500 μm in width. The laminar endings were also immunoreactive for vesicular glutamate transporter 1 (vGLUT1) and vGLUT2, but not for P2X3 purinoceptor. Around the laminar endings, terminal Schwann cells with immunoreactivity for S-100 protein were closely associated with axon terminals. Use of scanning electron microscopy with alkaline maceration method showed that the terminal Schwann cells consisted of a rounded perinuclear region and lamellar cytoplasmic processes. Ultrastructurally, axon terminals with numerous mitochondria were partly covered with Schwann cell sheath, and some terminals intruded into the epithelial layer. Clear vesicles of 50 nm in diameter were also observed especially in small cytoplasmic processes of 400 nm to 1 μm in size. The results in the present study suggested that the laminar endings in epiglottic mucosa have morphological characteristics of slowly adapting mechanoreceptors and contribute to sensation of laryngeal pressure via mucosal tension.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Andres KH, von Düring M (1973) Morphology of cutaneous receptors. In: Iggo A (ed) Handbook of sensory physiology, vol II, Somatosensory system. Springer, Berlin, pp 3–28

    Google Scholar 

  • Arystarkhova E, Sweadner KJ (1996) Isoform-specific monoclonal antibodies to Na, K-ATPase α subunits: Evidence for a tissue-specific post-translational modification of the α3 subunit. J Biol Chem 271:23407–23417

    Article  PubMed  CAS  Google Scholar 

  • Bewick GS, Reid B, Richardson C, Banks RW (2005) Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic-like vesicles: evidence from the rat muscle spindle primary sensory ending. J Physiol 562:381–394

    Article  PubMed  CAS  Google Scholar 

  • Blanco G, Mercer RW (1998) Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol 275:F633–F650

    PubMed  CAS  Google Scholar 

  • Blanco G, Sánchez G, Mercer RW (1995) Comparison of the enzymatic properties of the Na, K-ATPase α3β1 and α3β2 isozymes. Biochemistry 34:9897–9903

    Article  PubMed  CAS  Google Scholar 

  • Brouns I, Pintelon I, De Proost I, Alewaters R, Timmermans J-P, Adriaensen D (2006) Neurochemical characterisation of sensory receptors in airway smooth muscle: comparison with pulmonary neuroepithelial bodies. Histochem Cell Biol 125:351–367

    Article  PubMed  CAS  Google Scholar 

  • Brouns I, Oztay F, Pintelon I, De Proost I, Lembrechts R, Timmermans J-P, Adriaensen D (2009) Neurochemical pattern of the complex innervation of neuroepithelial bodies in mouse lungs. Histochem Cell Biol 131:55–74

    Article  PubMed  CAS  Google Scholar 

  • Burnstock G (2009) Purinergic mechanosensory transduction and visceral pain. Mol Pain 5:69. doi:10.1186/1744-8069-5-69

    Article  PubMed  Google Scholar 

  • Cahusac PMB, Mavulati SC (2009) Non-competitive metabotropic glutamate 1 receptor antagonists block activity of slowly adapting type 1 mechanoreceptor units in the rat sinus hair follicle. Neuroscience 163:933–941

    Article  PubMed  CAS  Google Scholar 

  • Cahusac PMB, Senok SS, Hitchcock IS, Genever PG, Baumann KI (2005) Are unconventional NMDA receptors involved in slowly adapting type I mechanoreceptor responses? Neuroscience 133:763–773

    Article  PubMed  CAS  Google Scholar 

  • Chiba T, Watanabe S, Shin T (1985) Ultrastructure of the glomerular corpuscular nerve endings in the subepithelium of human epiglottis. Arch Histol Jpn 48:213–221

    Google Scholar 

  • Dobretsov M, Hastings SL, Stimers JR (1999) Non-uniform expression of α subunit isoforms of the Na+/K+ pump in rat dorsal root ganglia neurons. Brain Res 821:212–217

    Article  PubMed  CAS  Google Scholar 

  • Dobretsov M, Hastings SL, Sims TJ, Stimers JR, Romanovsky D (2003) Stretch receptor-associated expression of α3 isoform of the Na+, K+-ATPase in rat peripheral nervous system. Neuroscience 116:1069–1080

    Article  PubMed  CAS  Google Scholar 

  • Ewald P, Neuhuber WL, Raab M (2006) Vesicular glutamate transporter 1 immunoreactivity in extrinsic and intrinsic innervation of the rat esophagus. Histochem Cell Biol 125:377–395

    Article  PubMed  CAS  Google Scholar 

  • Huang L-C, Greenwood D, Thorne PR, Housley GD (2005) Developmental regulation of neuron specific P2X3 receptor expression in the rat cochlea. J Comp Neurol 484:133–143

    Article  PubMed  CAS  Google Scholar 

  • Hwang JC, St John WM, Bartlett D Jr (1984) Receptors responding to changes in upper airway pressure. Respir Physiol 55:355–366

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Inaga S, Katsumoto T, Tanaka K, Kameie T, Nakane H, Naguro T (2007) Platinum blue as an alternative to uranyl acetate for staining in transmission electron microscopy. Arch Histol Cytol 70:43–49

    Article  PubMed  Google Scholar 

  • Jeftinija SD, Jeftinija KV (1998) ATP stimulates release of excitatory amino acids from cultured Schwann cells. Neuroscience 82:927–934

    Article  PubMed  CAS  Google Scholar 

  • Lingrel JB (1992) Na,K-ATPase: isoform structure, function, and expression. J Bioenerg Biomembr 24:263–270

    Google Scholar 

  • Liu GJ, Werry EL, Bennett MR (2005) Secretion of ATP from Schwann cells in response to uridine triphosphate. Eur J Neurosci 21:151–160

    Article  PubMed  Google Scholar 

  • Lund JP, Sadeghi S, Athanassiadis T, Sales NC, Auclair F, Thivierge B, Arsenault I, Rompré P, Westberg K-G, Kolta A (2010) Assessment of the potential role of muscle spindle mechanoreceptor afferents in chronic muscle pain in the rat masseter muscle. PLoS One 5:e11131. doi:10.1371/journal.pone.0011131

    Article  PubMed  Google Scholar 

  • Maeda T, Sato O, Kobayashi S, Iwanaga T, Fujita T (1989) The ultrastructure of Ruffini endings in the periodontal ligament of rat incisors with special reference to the terminal Schwann cells (K-cells). Anat Rec 223:95–103

    Article  PubMed  CAS  Google Scholar 

  • Maeda T, Ochi K, Nakakura-Ohshima K, Youn SH, Wakisaka S (1999) The Ruffini endings as the primary mechanoreceptor in the periodontal ligament: its morphology, cytochemical features, regeneration, and development. Crit Rev Oral Biol Med 10:307–327

    Article  PubMed  CAS  Google Scholar 

  • Mathew OP, Farber JP (1983) Effect of upper airway negative pressure on respiratory timing. Respir Physiol 54:259–268

    Article  PubMed  CAS  Google Scholar 

  • Mazzone SB, McGovern AE (2008) Immunohistochemical characterization of nodose cough receptor neurons projecting to the trachea of guinea pig. Cough 4:9. doi:10.1186/1745-9974-4-9

    Article  PubMed  Google Scholar 

  • Melone M, Burette A, Weinberg RJ (2005) Light microscopic identification and immunocytochemical characterization of glutamatergic synapses in brain sections. J Comp Neurol 492:495–509

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Parekh A, Campbell AJM, Djouhri L, Fang X, McMullan S, Berry C, Acosta C, Lawson SN (2010) Immunostaining for the α3 isoform of the Na+/K+-ATPase is selective for functionally identified muscle spindle afferents in vivo. J Physiol 588:4131–4143

    Article  PubMed  CAS  Google Scholar 

  • Peng L, Martin-Vasallo P, Sweadner KJ (1997) Isoforms of Na, K-ATPase α and β subunits in the rat cerebellum and in granule cell cultures. J Neurosci 17:3488–3502

    PubMed  CAS  Google Scholar 

  • Pintelon I, Brouns I, De Proost I, Van Meir F, Timmermans J-P, Adriaensen D (2007) Sensory receptors in the visceral pleura. Am J Respir Cell Mol Biol 36:541–551

    Article  PubMed  CAS  Google Scholar 

  • Ploschko A (1897) Die Nervenendigungen und Gaglien der Respirationsorgane. Anat Anz 13:12–22

    Google Scholar 

  • Raab M, Neuhuber WL (2004) Intraganglionic laminar endings and their relationships with nuronal and glial structures of myenteric ganglia in the esophagus of rat and mouse. Histochem Cell Biol 122:445–459

    Article  PubMed  CAS  Google Scholar 

  • Rousse I, Robitaille R (2006) Calcium signaling in Schwann cells at synaptic and extra-synaptic sites: active glial modulation of neuronal activity. Glia 54:691–699

    Article  PubMed  Google Scholar 

  • Ryan S, McNicholas WT, O’Regan RG, Nolan P (2001) Reflex respiratory response to changes in upper airway pressure in the anaesthetized rat. J Physiol 537:251–265

    Article  PubMed  CAS  Google Scholar 

  • Sant’Ambrogio G, Mathew OP, Fisher JT, Sant’Ambrogio FB (1983) Laryngeal receptors responding to transmural pressure, airflow and local muscle activity. Respir Physiol 54:317–330

    Article  PubMed  Google Scholar 

  • Sato O, Maeda T, Kobayashi S, Iwanaga T, Fujita T, Takahashi Y (1988) Innervation of periodontal ligament and dental pulp in the rat incisor: an immunohistochemical investigation of neurofilament protein and glia-specific S-100 protein. Cell Tissue Res 251:13–21

    Article  PubMed  CAS  Google Scholar 

  • Schoultz TW, Swett JE (1974) Ultrastructural organization of the sensory fibers innervating the Golgi tendon organ. Anat Rec 179:147–162

    Article  PubMed  CAS  Google Scholar 

  • Sekizawa S, Tsubone H (1991) The respiratory activity of the superior laryngeal nerve in the rat. Respir Physiol 86:335–368

    Article  Google Scholar 

  • Soiza-Reilly M, Commons KG (2011) Quantitative analysis of glutamatergic innervation of the mouse dorsal raphe nucleus using array tomography. J Comp Neurol 519:3802–3814

    Article  PubMed  CAS  Google Scholar 

  • Song X, Gao X, Guo D, Yu Q, Guo W, He C, Burnstock G, Xiang Z (2011) Expression of P2X2 and P2X3 receptors in the rat carotid sinus, aortic arch, vena cava, and heart, as well as petrosal and nodose ganglia. Purin Signal. doi:10.1007/s11302-011-9249-4

  • Spencer PS, Schaumburg HH (1973) An ultrastructural study of the inner core of the Pacinian corpuscle. J Neurocytol 2:217–235

    Article  PubMed  CAS  Google Scholar 

  • Stevens B, Fields RD (2000) Response of Schwann cells to action potentials in development. Science 287:2267–2271

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takahashi-Iwanaga H, Fujita T (1986) Application of an NaOH maceration method to a scanning electron microscopic observation of Ito cells in the rat liver. Arch Histol Jpn 49:349–357

    Article  PubMed  CAS  Google Scholar 

  • Takahashi-Iwanaga H, Habara Y (2004) Oscillatory calcium responses mediated by P2Y2 purinergic receptors in terminal Schwann cells of longitudinal lanceolate endings isolated from rat vibrissae. J Comp Neurol 475:416–425

    Article  PubMed  CAS  Google Scholar 

  • Takahashi-Iwanaga H, Maeda T, Abe K (1997) Scanning and transmission electron microscopy of Ruffini endings in the periodontal ligament of rat incisors. J Comp Neurol 389:177–184

    Article  PubMed  CAS  Google Scholar 

  • Todd AJ, Hughes DI, Polgár E, Nagy GG, Mackie M, Ottersen OP, Maxwell DJ (2003) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17:13–27

    Article  PubMed  CAS  Google Scholar 

  • Tsubone H, Mathew OP, Sant’Ambrogio G (1987) Respiratory activity in the superior laryngeal nerve of the rabbit. Respir Physiol 69:195–207

    Article  PubMed  CAS  Google Scholar 

  • van Lunteren E, van de Graaff WB, Parker DM, Mitra J, Haxhiu MA, Strohl KP, Cherniack NS (1984) Nasal and laryngeal reflex responses to negative upper airway pressure. J Appl Physiol 56:746–752

    Article  PubMed  Google Scholar 

  • Vulchanova L, Riedl MS, Shuster SJ, Buell G, Surprenant A, North RA, Elde R (1997) Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology 36:1229–1242

    Article  PubMed  CAS  Google Scholar 

  • Wang ZJ, Neuhuber WL (2003) Intraganglionic laminar endings in the rat esophagus contain purinergic P2X2 and P2X3 receptor immunoreactivity. Anat Embryol 207:363–371

    Article  PubMed  CAS  Google Scholar 

  • Wu S-X, Koshimizu Y, Feng Y-P, Okamoto K, Fujiyama F, Hioki H, Li Y-Q, Kaneko T, Mizuno N (2004) Vesicular glutamate transporter immunoreactivity in the central and peripheral endings of muscle-spindle afferents. Brain Res 1011:247–251

    Article  PubMed  CAS  Google Scholar 

  • Xu GY and Huang LY (2004) Ca2+/calmodulin-dependent protein kinase II potentiates ATP responses by promoting trafficking of P2X receptors. Proc Natl Acad Sci USA 101:11868–11873

    Google Scholar 

  • Yamamoto Y, Hayashi M, Atoji Y, Suzuki Y (1994) Vagal afferent nerve endings in the trachealis muscle of the dog. Arch Histol Cytol 57:473–480

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Hosono I, Atoji Y, Suzuki Y (1997) Morphological study of the vagal afferent nerve endings in the laryngeal mucosa of the dog. Ann Anat 179:65–73

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Atoji Y, Kuramoto H, Suzuki Y (1998) Calretinin-immunoreactive laminar nerve endings in the laryngeal mucosa of the rat. Cell Tissue Res 292:613–617

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Atoji Y, Suzuki Y (2000) Calbindin D28k-immunoreactive afferent nerve endings in the laryngeal mucosa. Anat Rec 259:237–247

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Atoji Y, Hobo S, Yoshihara T, Suzuki Y (2001) Morphology of the nerve endings in laryngeal mucosa of the horse. Equine Vet J 33:150–158

    Article  PubMed  CAS  Google Scholar 

  • Yasaka T, Thiong SYX, Hughes DI, Riddell JS, Todd AJ (2010) Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain 151:475–488

    Article  PubMed  Google Scholar 

  • Yu J (2005) Airway mechanoreceptors. Resp Physiol Neurobiol 148:217–243

    Article  Google Scholar 

  • Yu J, Wang F, Zhang JW (2003) Structure of slowly adapting pulmonary stretch receptors in the lung periphery. J Appl Physiol 95:385–393

    PubMed  CAS  Google Scholar 

  • Zhang X, Bruce EN (1998) Response of breathing pattern to flow and pressure in the upper airway of rats. Respir Physiol 113:191–200

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Misuzu Yamaguchi-Yamada for valuable comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoshio Yamamoto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soda, Y., Yamamoto, Y. Morphology and chemical characteristics of subepithelial laminar nerve endings in the rat epiglottic mucosa. Histochem Cell Biol 138, 25–39 (2012). https://doi.org/10.1007/s00418-012-0939-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-012-0939-y

Keywords