Skip to main content
SpringerLink
Log in

Miniature end plate currents from teleost extraocular muscle

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

Miniature end plate currents (MEPCs) were recorded with focal extracellular electrodes from white extraocular muscle fibres of a marine teleost fish,Trachurus novaezelandiae, over a temperature range of 5 °C to 27 °C.

  1. 1.

    Teleost MEPCs rose rapidly, attaining a maximum amplitude of 250–500 μV, withT Gof about 150 μs at 15 °C (Figs. 1, 2).

  2. 2.

    Decay of MEPCs was exponential, with τ=1 ms at 15 °C (Figs. 3, 5). τ was an exponential function of absolute temperature, withE a=70 kJ (Fig. 5).

  3. 3.

    τ ofTrachurus MEPCs was consistently smaller than values of τ reported for other vertebrate end plates (Table 1). Low τ is correlated with a high degree of lipid unsaturation in teleosts, and may be caused by increased membrane fluidity.

  4. 4.

    Frequency distributions ofT G(Fig. 2) and τ (Fig. 4) at a single recording site appear to represent one population of events, skewed toward smaller values.

  5. 5.

    Teleost MEPCs also appeared to be normal cholinergic MEPCs in that their rates of decay were decreased by neostigmine, ethanol and membrane hyperpolarization.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ACh :

acetylcholine

E a :

Arrhenius activation energy

E m :

membrane potential

MEPC :

miniature end plate current

T G :

growth time of MEPC (time elapsed between 20% and 80% of peak voltage)

τ:

time constant of exponential decay of MEPC

References

  • Anderson CR, Stevens CF (1973) Voltage clamp analysis of acetylcholine produced end plate current fluctuations at frog neuromuscular junction. J Physiol (Lond) 235:655–691

    Google Scholar 

  • Bone Q, Ono RD (1982) Systematic implications of innervation patterns in teleost myotomes. Breviora (Museum of Comparative Zoology, Harvard) 470:1–23

    Google Scholar 

  • Chatfield PO, Lyman CP, Irving L (1953) Physiological adaptation to cold of peripheral nerve in the leg of the herring gull (Larus argentatus). Am J Physiol 172:639–644

    Google Scholar 

  • Colquhoun D, Dionne VE, Steinbach JH, Stevens CF (1975) Conductance of channels opened by acetylcholine-like drugs in muscle end-plate. Nature 253:204–206

    Google Scholar 

  • Cossins AR (1977) Adaptation of biological membranes to temperature. The effect of temperature acclimation of goldfish upon the viscosity of synaptosomal membranes. Biochim Biophys Acta 470:395–411

    Google Scholar 

  • Cossins AR, Christiansen J, Prosser CL (1978) Adaptation of biological membranes to temperature. The lack of homeoviscous adaptation in the sarcoplasmic reticulum. Biochim Biophys Acta 511:442–454

    Google Scholar 

  • Cossins AR, Friedlander MJ, Prosser CL (1977) Correlations between behavioral temperature adaptations of goldfish and the viscosity and fatty acid composition of their synaptic membranes. J Comp Physiol 120:109–121

    Google Scholar 

  • Cossins AR, Prosser CL (1978) Evolutionary adaptation of membranes to temperature. Proc Natl Acad Sci USA 75:2040–2043

    Google Scholar 

  • Cowey CB, Sargent JR (1972) Fish nutrition. Adv Mar Biol 10:383–492

    Google Scholar 

  • Davey DF, Mark RF, Marotte LR, Proske U (1975) Structure and innervation of extraocular muscles ofCarassius. J Anat 120:131–147

    Google Scholar 

  • Dionne VE, Parsons RL (1981) Characteristics of the acetylcholine-operated channel at twitch and slow fibre neuromuscular junctions of the garter snake. J Physiol (Lond) 310:145–158

    Google Scholar 

  • Dreyer F, Mueller KD, Peper K, Sterz R (1976) The M. omohyoideus of the mouse as a convenient mammalian muscle preparation: a study of junctional and extrajunctional acetylcholine receptors by noise analysis and cooperativity. Pflügers Arch 367:115–122

    Google Scholar 

  • Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol (Lond) 117:109–128

    Google Scholar 

  • Friedlander MJ, Kotchabhakdi N, Prosser CL (1976) Effects of cold and heat on behavior and cerebellar function in goldfish. J Comp Physiol 112:19–45

    Google Scholar 

  • Gage PW (1976) Generation of end-plate potentials. Physiol Rev 56:177–247

    Google Scholar 

  • Gage PW, Hamill OP (1976) Effects of several inhalation anaesthetics on the kinetics of postsynaptic conductance changes in mouse diaphragm. Br J Pharmacol 57:263–272

    Google Scholar 

  • Gage PW, Hamill OP (1980) Lifetime and conductance of acetylcholine-activated channels in normal and denervated toad sartorius muscle. J Physiol (Lond) 298:525–538

    Google Scholar 

  • Gage PW, Hamill OP, Van Helden DF, Barry PH (1979) Acetylcholine receptors and end-plate channels. In: Kidman AD, Tomkins JK (eds) Muscle, nerve and brain degeneration. Elsevier North-Holland, Amsterdam, pp 166–173

    Google Scholar 

  • Gage PW, McBurney RN (1975) Effects of membrane potential, temperature and neostigmine on the conductance change caused by a quantum of acetylcholine at the toad neuromuscular junction. J Physiol (Lond) 244:385–407

    Google Scholar 

  • Gage PW, McBurney RN, Schneider GT (1975) Effects of some aliphatic alcohols on the conductance change caused by a quantum of acetylcholine at the toad end plate. J Physiol (Lond) 244:409–429

    Google Scholar 

  • Gage PW, McBurney RN, Van Helden D (1978) Octanol reduces end-plate channel lifetime. J Physiol (Lond) 274:279–298

    Google Scholar 

  • Gestrin P, Sterling P (1977) Anatomy and physiology of goldfish oculomotor system. II. Firing patterns of neurons in abducens nucleus and surrounding medulla and their relation to eye movements. J Neurophysiol 40:573–588

    Google Scholar 

  • Hamill OP (1978) The effects of general anaesthetics on transmitter activated postsynaptic channels. PhD thesis, University of New South Wales

  • Harvey AL, Van Helden D (1981) Acetylcholine receptors in singly and multiply innervated skeletal muscle fibres of the chicken during development. J Physiol (Lond) 317:397–411

    Google Scholar 

  • Hazel JR, Prosser CL (1974) Molecular mechanisms of temperature compensation in poikilotherms. Physiol Rev 54:620–677

    Google Scholar 

  • Hidaka T, Toida N (1969) Biophysical and mechanical properties of red and white muscle fibres in fish. J Physiol (Lond) 201:49–59

    Google Scholar 

  • Hilditch TP, Williams PN (1964) The chemical constitution of natural fats, 4th edn. Chapman & Hall, London

    Google Scholar 

  • Housley GD (1982) Aspects of the vestibular reflex pathway in the carpet sharkCephaloscyllium isabella. MSc thesis, Zoology, University of Auckland

  • Hudson RCL (1969) Polyneuronal innervation of the fast muscles of the marine teleostCottus scorpius L. J Exp Biol 50:47–67

    Google Scholar 

  • Katz B, Miledi R (1973) The binding of acetylcholine to receptors and its removal from the synaptic cleft. J Physiol (Lond) 231:549–574

    Google Scholar 

  • Kreps EM, Avrova NF, Chebotarëva MA, Chirkovskaya EV, Levitina MV, Pomazanskaya LF, Pravdina NI (1975) Some aspects of comparative biochemistry of brain lipids in teleost and elasmobranch fish. Comp Biochem Physiol B 52: 293–299

    Google Scholar 

  • Large WA, Rang HP (1979) Studies on a false transmitter at the neuromuscular junction. Prog Brain Res 49:267–275

    Google Scholar 

  • Lewis RW (1962) Temperature and pressure effects on the fatty acids of some marine ectotherms. Comp Biochem Physiol 6:75–89

    Google Scholar 

  • Macdonald JA (1981) Temperature compensation in the peripheral nervous system: antarctic vs temperate poikilotherms. J Comp Physiol 142:411–418

    Google Scholar 

  • Macdonald JA (1983a) Fast decay of fish synaptic currents. Experientia 39:230–231

    Google Scholar 

  • Macdonald JA (1983b) Neuromuscular cold adaptation in an antarctic fish. N.Z. Antarctic Record 5:1–10

    Google Scholar 

  • Macdonald JA, Montgomery JC (1982) Thermal limits of neuromuscular function in an antarctic fish. J Comp Physiol 147:237–250

    Google Scholar 

  • Magazanik LG, Fedorov VV, Snetkov VA (1979) The time course of postsynaptic currents in fast and slow junctions and its alteration by cholinesterase inhibition. Prog Brain Res 49:225–240

    Google Scholar 

  • Magleby KL, Stevens CF (1972) A quantitative description of end-plate currents. J Physiol (Lond) 223:173–179

    Google Scholar 

  • Mallart A, Molgó J (1978) The effects of pH and curare on the time course of end-plate currents at the neuromuscular junction of the frog. J Physiol (Lond) 276:343–352

    Google Scholar 

  • McCarthy D (1982) Temperature effects upon the parore oculomotor system. MSc thesis, Zoology, University of Auckland

  • McMullin GF, Smith SC, Wright PA (1968) Tissue fatty acid composition in four diverse vertebrate species. Comp Biochem Physiol 26:211–221

    Google Scholar 

  • Miledi R, Reiser G (1984) Miniature end plate currents in two different types of fish muscle fibres. J Physiol (Lond) 346:80P

    Google Scholar 

  • Miledi R, Uchitel OD (1981) Properties of postsynaptic channels induced by acetylcholine in different frog muscle fibres. Nature 291:162–165

    Google Scholar 

  • Miller LK (1967) Caudal nerve function as related to temperature in some Alaskan mammals. Comp Biochem Physiol 21:679–686

    Google Scholar 

  • Miller LK (1970) Temperature-dependent characteristics of peripheral nerves exposed to different thermal conditions in the same animal. Can J Zool 48:75–81

    Google Scholar 

  • Montgomery JC (1980) Dogfish horizontal canal system: responses of primary afferent, vestibular and cerebellar neurons to rotational stimulation. Neuroscience 5:1761–1769

    Google Scholar 

  • Montgomery JC (1983) Eye movement dynamics in the dogfish. J Exp Biol 105:297–304

    Google Scholar 

  • Montgomery JC, Macdonald JA (1980) Stretch receptors in the eye muscles of a teleost fish. Experientia 36:1176–1177

    Google Scholar 

  • Montgomery JC, Macdonald JA (1984) Performance of motor systems in antarctic fishes. J Comp Physiol A 154:241–248

    Google Scholar 

  • Montgomery JC, McVean A, McCarthy D (1983) Effects of lowered temperature on spontaneous eye movements in a teleost fish. Comp Biochem Physiol A 75:363–368

    Google Scholar 

  • Prince JH (1956) Comparative anatomy of the eye. Thomas, Springfield

    Google Scholar 

  • Pennefather P, Quastel DMJ (1980) The effects of myasthenic IgG on miniature end-plate currents in mouse diaphragm. Life Sci 27:2047–2054

    Google Scholar 

  • Prosser CL (1965) Electrical responses of fish optic tectum to visual stimulation: modification by cooling and conditioning. Z Vergl Physiol 50:102–118

    Google Scholar 

  • Prosser CL, Farhi E (1965) Effects of temperature on conditioned reflexes and on nerve conduction in fish. Z Vergl Physiol 50:91–101

    Google Scholar 

  • Prosser CL, Nelson DO (1981) The role of nervous systems in temperature adaptation of poikilotherms. Annu Rev Physiol 43:281–300

    Google Scholar 

  • Sinensky M (1974) Homeoviscous adaptation — a homeostatic process that regulates the viscosity of membrane lipids inEscherichia coli. Proc Natl Acad Sci USA 71:522–525

    Google Scholar 

  • Stephenson AB, Robertson DA (1977) The New Zealand species ofTrachurus (Pisces: Carangidae). J R Soc NZ 7:243–253

    Google Scholar 

  • Sterling P (1977) Anatomy and physiology of goldfish oculomotor system. I. Structure of abducens nucleus. J Neurophysiol 40:557–572

    Google Scholar 

  • Takeda K, Gage PW, Barry PH (1982) Effects of divalent cations on toad end-plate channels. J Membrane Biol 64: 55–66

    Google Scholar 

  • Takeuchi A (1959) Neuromuscular transmission of fish skeletal muscles investigated with intracellular microelectrode. J Cell Comp Physiol 54:211–220

    Google Scholar 

  • Teräväinen H (1971) Anatomical and physiological studies on muscles of lamprey. J Neurophysiol 34:954–973

    Google Scholar 

  • Torda TA, Gage PW (1977) Postsynaptic effect of I.V. anaesthetic agents at the neuromuscular junction. Br J Anaesth 49:771–776

    Google Scholar 

  • Yamamoto T (1972) Electrical and mechanical properties of the red and white muscles in the silver carp. J Exp Biol 57:551–567

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Auckland, Private Bag, Auckland, New Zealand

    John A. Macdonald & Ron J. Balnave

  2. Department of Biological Sciences, Cumberland College of Health Sciences, P.O. Box 170, 2141, Lidcombe, NSW, Australia

    John A. Macdonald & Ron J. Balnave

Authors
  1. John A. Macdonald
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ron J. Balnave
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Macdonald, J.A., Balnave, R.J. Miniature end plate currents from teleost extraocular muscle. J. Comp. Physiol. 155, 649–659 (1984). https://doi.org/10.1007/BF00610851

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00610851

Keywords

Search

Navigation