Skip to main content

Muscle Mechanoreceptors in Nonmammalian Vertebrates

  • Chapter
Comparative Aspects of Mechanoreceptor Systems

Part of the book series: Advances in Comparative and Environmental Physiology ((COMPARATIVE,volume 10))

Abstract

Barker (1974) gives a comprehensive review of the anatomy of muscle receptors of mammalian and nonmammalian vertebrates. In the vertebrates, all skeletal, smooth and heart muscles are innervated by free nerve endings. They are supplied by nonmyelinated axons (0.2–1 μm in diameter; classified into group C in vertebrate or group IV in mammals), and some thin myelinated axons (2–6 μum in diameter; group Aδ of vertebrates in general or group III or II in mammals). The endings consist of numerous parallel varicose threads either on the surface of the extrafusal muscle fiber and tendon, or lying in the connective tissue in muscle and joint capsule as well as in the spindle sensory ending of frogs (cf. Barker 1974). The number and length of the nonmyelinated terminal branches varies widely between species and even between individual preparations.

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

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adal MN, Cheng BC (1980) The sensory ending of duck muscle spindles. J Anat 131:657–668

    PubMed  CAS  Google Scholar 

  • Andrews PLR (1986) Vagal afferent innervation of the gastrointestinal tract. Prog Brain Res 67:65–86

    Article  PubMed  CAS  Google Scholar 

  • Barker D (1974) The morphology of muscle receptors. In: Hunt CC (ed) Handbook of sensory physiology, III/2. Springer, Berlin Heidelberg New York, pp 1–190

    Google Scholar 

  • Beavo JA, Rogers NL, Crofford OB, Hardman JG, Sutherland EW, Newman EV (1970) Effects of xanthine derivatives on lipolysis and on adenosine 3’,5’-monophosphate phosphodiesterase activity. Mol Pharmacol 6:597–603

    PubMed  CAS  Google Scholar 

  • Berridge MJ, Irvine RF (1989) Inositol phosphates and cell signalling. Nature (Lond) 341:197–205

    Article  CAS  Google Scholar 

  • Boyd IA, Rosenberg J (1985) Review. In: Boyd IA, Gladden MH (eds) The muscle spindle. Macmillan, London, pp 327–352

    Google Scholar 

  • Bygrave FL (1978) Mitochondria and the control of intracellular calcium. Biol Rev 53:43–74

    Article  PubMed  CAS  Google Scholar 

  • Cheung WY, Bradham LS, Lynch TJ, Lin YM, Tallan EA (1975) Peptide activation of cyclic 3’:5’-nucleotide phosphodiesterase of bovine or rat brain also activates its adenylate cyclase. Biochem Biophys Res Commun 66:1055–1062

    Article  PubMed  CAS  Google Scholar 

  • Diwan FH, Ito F (1989) Intrafusal muscle fibre types in frog spindles. J Anat 163:191–200

    PubMed  CAS  Google Scholar 

  • Dockray GJ, Sharkey KA (1986) Neurochemistry of visceral afferent neurones. Prog Brain Res 67:133–148

    Article  PubMed  CAS  Google Scholar 

  • Dunkley PR, Baker CM, Robinson PJ (1986) Depolarization-dependent protein phosphorylation in rat cortical synaptosomes: characterization of active protein kinases by phosphopeptide analysis of substrates. J Neurochem 46:1692–1703

    Article  PubMed  CAS  Google Scholar 

  • Ewald DA, Williams A, Levitan IB (1985) Modulation of single Ca2+-dependent K+-channel activity by protein phosphorylation. Nature (Lond) 315:503–506

    Article  CAS  Google Scholar 

  • Fesenko EE, Kolensnikov SS, Lyubarsky AL (1985) Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature (Lond) 313:310–313

    Article  CAS  Google Scholar 

  • Flower NE (1971) Particles within membranes — a freeze-etch view. J Cell Sci 9:435–441

    PubMed  CAS  Google Scholar 

  • Forscher P (1989) Calcium and polyphosphoinositide control of cytoskeletal dynamics. Trend Neurosci 12:468–474

    Article  PubMed  CAS  Google Scholar 

  • Fujitsuka N, Ito F (1983) Uptake of ruthenium red by the sensory nerve terminal of the frog muscle spindle. Okajimas Folia Anat Jpn 60:1–16

    PubMed  CAS  Google Scholar 

  • Fujitsuka N, Hama K, Ito F, Sokabe M (1987) Intramembrane particles and terminal responses following denervation of frog muscle spindles. J Neurocytol 16:185–194

    Article  PubMed  CAS  Google Scholar 

  • Fujitsuka N, Kori AA, Sokabe M, Ito F (1988) Modification of sensory-terminal responses and membrane structure of frog muscle spindle by collagenase. Brain Res 443:243–253

    Article  PubMed  CAS  Google Scholar 

  • Fujitsuka N, Yoshimura A, Sokabe M, Ito F (1989) Intramembrane particles associated with stretch-activation function in the sensory axon terminal of frog muscle spindle. Neurosci Res Suppl 9:165

    Google Scholar 

  • Fujitsuka C, Fujitsuka N, Diwan FH, Hama K, Sokabe M, Ito F (1990) Intramembrane particles and responses of sensory axon terminals during reinnervation of the frog muscle spindle. J Neurocytol 19:176–186

    Article  Google Scholar 

  • Fukami Y, Hunt CC (1970) Structure of snake muscle spindles. J Neurophysiol 33:9–27

    PubMed  CAS  Google Scholar 

  • George JS, Hagins WA (1983) Control of Ca2+ in rod outer segment disks by light and cyclic GMP. Nature (Lond) 303:344–348

    Article  CAS  Google Scholar 

  • Glagoleva IM, Liberman EA, Khashayev ZKh (1970) Effect of uncoupling agents of oxidative phosphorylation on the release of acetylcholine from nerve endings. Biofizika 15:76–82

    PubMed  CAS  Google Scholar 

  • Heuser JE, Kirshner MW (1980) Filament organization resolved in platinum replica of freeze– dried cytoskeleton. J Cell Biol 86:212–234

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N (1989) The arrangement of actin filaments in the postsynaptic cytoplasm of the cerebellar cortex revealed by quick-freeze deep-etch electron microscopy. Neurosci Res 6:269–275

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann EK, Simonsen LO (1989) Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol Rev 67:315–382

    Google Scholar 

  • Hollenbeck PJ (1989) The transport and assembly of the axonal cytoskeleton. J Cell Biol 108:223- 227

    Article  PubMed  CAS  Google Scholar 

  • Huber GC, DeWitt LM (1897) A contribution on the motor nerve endings and the nerve endings in muscle spindle. J Comp Neuol 7:169–230

    Article  Google Scholar 

  • Ito F (1968) Recovery curves of thresholds of muscle spindle, leaflike and tendon receptors in the frog sartorius muscle after an antidromic discharge. Jpn J Physiol 18:731–745

    Article  PubMed  CAS  Google Scholar 

  • Ito F (1969) The effect of ions on the steady and generator potential of frog muscle spindles. Proc Jpn Acad 45:409–412

    CAS  Google Scholar 

  • Ito F (1970a) Spindle potential of the frog muscle spindle depending upon the exclusion of extrafusal muscle fiber. J Physiol Soc Jpn 32:249–250

    CAS  Google Scholar 

  • Ito F (1970b) Effects of polarizing currents on long-lasting discharges in the frog muscle spindle. Jpn J Physiol 20:697–710

    Article  PubMed  CAS  Google Scholar 

  • Ito F (1970c) The behavior of frog muscle spindle in hyper– and hypotonic solutions. Jpn J Physiol 20:394–407

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Fujitsuka N (1983) Electrical threshold of the sensory nerve terminal of the frog muscle spindle: a role of spindle potential for generating afferent impulses. Neurosci Lett 37:233–237

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Ito Y (1976) Selective blockage of the sensory terminal activities by micro-application of tetrodotoxin in the frog muscle spindle. Brain Res Bull 1:363–366

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Komatsu Y (1979) Calcium-dependent regenerative responses in the afferent nerve terminal of the frog muscle spindle. Brain Res 175:160–164

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Yokoyama N (1978) Potential deflections at the terminal of the frog muscle spindle during stretch. Nagoya J Med Sci 40:13–23

    PubMed  CAS  Google Scholar 

  • Ito F, Toyama K, Ito R (1964) A comparative study on structure and function between the extrafusal receptor and the spindle receptor in the frog. Jpn J Physiol 14:12–33

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Kanamori N, Kuroda H (1974) Structural and functional asymmetries of myelinated branches in the frog muscle spindle. J Physiol 241:389–405

    PubMed  CAS  Google Scholar 

  • Ito F, Komatsu Y, Kaneko N (1980a) Site of origin of calcium spike in frog muscle spindle. Brain Res 202:459–463

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Komatsu Y, Kaneko N (1980b) Delayed rectification in the afferent nerve terminal of frog muscle spindle. Integrated Control Function of Brain 3:65–66

    Google Scholar 

  • Ito F, Komatsu Y, Fujitsuka N (1981) Calcium spike induced by electrical stimulation to the sensory nerve terminal of the frog muscle spindle. Neurosci Lett 27:135–137

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Komatsu Y, Fujitsuka N (1982) GK(Ca)-dependent cyclic potential changes in the sensory nerve terminal of frog muscle spindle. Brain Res 252:39–50

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Fujitsuka N, Hanaichi T (1984) Effects of dantrolene and methylxanthines on the sensory nerve terminal of the frog muscle spindle. Brain Res 294:269–280

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Fujitsuka N, Fan XL (1985a) Reversal of the static component of spindle potential by imposed depolarizing current in the frog muscle spindle. Brain Res 326:107–116

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Fujitsuka N, Funahashi A, Hama K (1985b) Ionic channels in the sensory terminal of the frog muscle spindle. In: Boyd IA, Gladden MH (ed) The muscle spindle. Macmillan, London, pp 353–358

    Google Scholar 

  • Ito F, Sokabe M, Diwan FH, Fujitsuka N, Yoshimura A (1988) Effects of intracellular Ca2+ on the frog muscle spindle in relation to cyclic AMP action. In: Hnik P, Soukup T, Vejsada R, Zelena J (eds) Mechanoreceptors. Plenum Press, New York, pp 195–199

    Google Scholar 

  • Ito F, Fujitsuka N, Sokabe N, Yoshimura A (1989) Effects of protein-synthesis blocker on intramembrane particles in sensory axon terminal of frog muscle spindle. Neurosci Res (Suppl) 9:167

    Google Scholar 

  • Ito F, Sokabe M, Fujitsuka N, Yoshimura A (1990a) Activities of sensory nerve terminal of frog muscle spindle and C kinase. Neurosci Res 11:S130

    Google Scholar 

  • Ito F, Sokabe M, Nomura K, Naruse K, Fujitsuka N, Yoshimura A (1990b) Effects of ions and drugs on the responses of sensory axon terminals of decapsulated frog muscle spindle. Neurosci Res 12:S 15–26

    Google Scholar 

  • Karlsson U, Andersson-Cedergren E, Ottoson D (1966) Cellular organization of the frog muscle spindles as revealed by serial sections for electron microscopy. J Ultrastruct 14:1–35

    Article  Google Scholar 

  • Katz B (1950) Depolarization of sensory terminal and the initiation of impulses in the muscle spindle. J Physiol 111:261–282

    PubMed  CAS  Google Scholar 

  • Katz B (1961) The terminations of the afferent nerve fibre in the muscle spindle of the frog. Philos Trans R Soc Lond B 243:221–240

    Article  Google Scholar 

  • Kim N, Fujitsuka N, Ito F (1985) Ultrastructural changes of the sensory nerve terminals in frog muscle spindle during dynamic stretch. J Neurocytol 14:105–112

    Article  PubMed  CAS  Google Scholar 

  • Krueger BK, Forn J, Greengard P (1977) Depolarization-induced phosphorylation of specific proteins, mediated by calcium ion influx, in rat synaptosomes. J Biol Chem 252:2764–2773

    PubMed  CAS  Google Scholar 

  • Kulchitsky N (1924) Nerve endings in muscles of the frog. J Anat 59:1–43

    PubMed  CAS  Google Scholar 

  • Lipton SA, Rasmussen H, Dowling JE (1977) Electrical and adaptive properties of rod photoreceptors in Bufo marinus. II. Effects of cyclic nucleotides and prostaglandins. J Gen Physiol 70:771–791

    Article  PubMed  CAS  Google Scholar 

  • Loewenstein WR (1971) Mechano-electric transduction in the Pacinian corpuscle. Initiation of sensory impulses in mechanoreceptors. In: Loewenstein WR (ed) The handbook of sensory physiology, vol 1. Springer, Berlin Heidelberg New York, pp 269–290

    Google Scholar 

  • Maeda N, Miyoshi S, Toh H (1983) First observation of a muscle spindle in fish. Nature (Lond) 302:61–62

    Article  CAS  Google Scholar 

  • Magleby KL, Pallotta BS (1983) Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle. J Physiol 344:585–604

    PubMed  CAS  Google Scholar 

  • Miller WH, Nicol GD (1979) Evidence that cyclic GMP regulates membrane potential in rod photoreceptors. Nature (Lond) 280:64–66

    Article  CAS  Google Scholar 

  • Mills FW, Lubin M (1986) Effect of adenosine 3’,5’-cyclic monophosphate on volume and cyto– skeleton of MDCK cells. Am J Physiol 250:C319-C324

    PubMed  CAS  Google Scholar 

  • Montague W, Cook JR (1971) The role of adenosine 3’,5’-cyclic monophosphate in the regulation of insulin release by isolated rat islets of Langerhans. Biochem J 122:115–120

    PubMed  CAS  Google Scholar 

  • Nairn AC, Hemmings Jr NC, Greengard P (1985) Protein kinases in the brain. Annu Rev Biochem 54:931–976

    Article  PubMed  CAS  Google Scholar 

  • Nieuwenhuys R, Opdam P (1976) Structure of the brain stem. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 811–855

    Google Scholar 

  • Ohnishi ST, Devlin TM (1979) Calcium ionophore activity of a prostaglandin Biderivative (PGBx). Biochem Biophys Res Commun 89:240–245

    Article  PubMed  CAS  Google Scholar 

  • Ottoson D (1976) Morphology and physiology of muscle spindle. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 643–675

    Google Scholar 

  • Ottoson D, Shepherd GM (1971) Transducer properties and integrative mechanisms in the frog’s muscle spindle. In: Loewenstein WR (ed) Handbook of sensory physiology. Springer, Berlin Heidelberg New York, pp 442–499

    Google Scholar 

  • Oyama O (1970) The effects of temperature on the dynamic and static sensitivities of the frog muscle spindle. Nagoya J Med Sci 33:13–25

    PubMed  CAS  Google Scholar 

  • Pace U, Hanski E, Salomon Y, Lancet D (1985) Odorant-sensitive adenylate cyclase may modify olfactory reception. Nature (Lond) 316:255–258

    Article  CAS  Google Scholar 

  • Partridge LD, Swandulla D (1988) Calcium-activated non-specific cation channels. Trends Neurosci 11:69–72

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen H (1970) Cell communication, calcium ion, and cyclic adenosine monophosphate. Science 170:404–412

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen H, Goodman DBP (1977) Relationship between calcium and cyclic nucleotides in cell activation. Physiol Rev 57:421–509

    PubMed  CAS  Google Scholar 

  • Rasmussen H, Tenenhouse A (1968) Cyelic-adenosine monophosphate, calcium and membranes. Proc Natl Acad Sci USA 59:1364–1370

    Article  PubMed  CAS  Google Scholar 

  • Robinson PJ, Dunkley PR (1983) Depolarization-dependent protein phosphorylation in rat cortical synaptosomes: factors determining the magnitude of the response. J Neurochem 41:909–918

    Article  PubMed  CAS  Google Scholar 

  • Robinson PJ, Hauptschein R, Lovenberg W, Dunkley P (1987) Dephosphorylation of synaptosomal proteins P96 and P139 is regulated by both depolarization and calcium, but not by a rise in cytosolic calcium alone. J Neurochem 48:187–195

    Article  PubMed  CAS  Google Scholar 

  • Roper SD (1989) The cell biology of vertebrate taste receptors. Annu Rev Neurosci 12:329–353

    Article  PubMed  CAS  Google Scholar 

  • Shuster MJ, Camardo JS, Siegelbaum SA, Kandel ER (1985) Cyclic AMP-dependent protein kinase closes the serotonin-sensitive K+ channels in Aplysia sensory neurones in cell-free membrane patches. Nature (Lond) 313:392–395

    Article  CAS  Google Scholar 

  • Sikdar SK, Mcintosh RP, Mason WT (1989) Differential modulation of Ca2+-activated K+ channels in ovin pituitary gonadotrophs by GnRH, Ca2+ and cyclic AMP. Brain Res 496:113–123

    Article  PubMed  CAS  Google Scholar 

  • Smith SJ, Thompson SH (1987) Slow membrane current in bursting pace-maker neurones of Tritonia. J Physiol 382:425–448

    PubMed  CAS  Google Scholar 

  • Sokabe M, Fujitsuka N, Kori AA, Ito F (1988) Effects of cyclic nucleotides and calcium on transduction and encoding processes in frog muscle spindle. Brain Res 443:254–260

    Article  PubMed  CAS  Google Scholar 

  • Tasaki I (1968) Nerve Excitation. Charles Thomas, Illinois

    Google Scholar 

  • Thompson SH, Smith SJ (1976) Depolarizing afterpotentials and burst production in molluscan pacemaker neurons. J Neurophysiol 39:153–161

    PubMed  CAS  Google Scholar 

  • Tonosaki K, Funakoshi M (1988) Cyclic nucleotides may mediate taste transduction. Nature (Lond) 331:354–356

    Article  CAS  Google Scholar 

  • Wang JKT, Walaas SI, Greengard P (1988) Protein phosphorylation in nerve terminals: comparison of calcium/calmodulin-dependent and calcium/diacylglycerol-dependent systems. J Neurosci 8:281–288

    PubMed  CAS  Google Scholar 

  • Widdicomb JG (1986) Sensory innervation of the lungs and airways. Prog Brain Res 67:49–64

    Article  Google Scholar 

  • Wu WC-S, Walaas SI, Greengard P (1982) Calcium/phospholipid regulates phosphorylation of a Mr “87K” substrate protein in brain synaptosomes. Proc Natl Acad Sci USA 79:5249–5253

    Article  PubMed  CAS  Google Scholar 

  • Yip RK, Kelly PT (1989) In situ protein phosphorylation in hippocampal tissue slices. J Neurosci 9:3618–3630

    PubMed  CAS  Google Scholar 

  • Zigmond RE, Schwarzschield MA, Rittenhous AR (1989) Acute regulation of tyrosine hydroxylase by nerve activity and by neurotransmitters via phosphorylation. Annu Rev Neurosci 12:415–461

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Ito, F., Sokabe, M., Fujitsuka, N. (1992). Muscle Mechanoreceptors in Nonmammalian Vertebrates. In: Ito, F. (eds) Comparative Aspects of Mechanoreceptor Systems. Advances in Comparative and Environmental Physiology, vol 10. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-76690-9_12

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-76690-9_12

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-76692-3

  • Online ISBN: 978-3-642-76690-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics