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PMID: 10562339 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Depletion of calcium in the synaptic cleft of a calyx-type synapse in the rat brainstem.

The Journal of physiology ·Vol. 521 Pt 1 ·1999-11-15 ·Pages 123-33

Borst JG, Sakmann B

Abstract

1. A new form of synaptic depression of excitatory synaptic transmission was observed when making voltage-clamp recordings from large presynaptic terminals, the calyces of Held and postsynaptic cells, the principal cells of the medial nucleus of the trapezoid body (MNTB), in slices of the rat auditory brainstem. 2. A short (100 ms) depolarization of the postsynaptic cell to 0 mV reduced the amplitude of the EPSCs by 35 +/- 5 % (n = 7), measured at 10 ms following the depolarization. Recovery occurred within 0.5 s. 3. The reduction of the EPSCs was most probably due to reduced presynaptic calcium influx, since postsynaptic depolarization reduced presynaptic calcium or barium currents. Conversely, presynaptic depolarization also reduced postsynaptic calcium or barium influx, under conditions where transmitter release was minimal. 4. The calcium currents and the postsynaptic depolarization-induced suppression of synaptic transmission recovered with a similar time course, suggesting that this form of synaptic depression was, most probably, due to depletion of Ca2+ in the synaptic cleft. 5. We conclude that when the Ca2+ influx into the pre- or postsynaptic cell is large, extracellular Ca2+ is depleted. Under these conditions, the Ca2+ concentration in the synaptic cleft is a sensitive indicator of the level of synaptic activity. However, the synaptic cleft is less sensitive to Ca2+ depletion than predicted from its estimated volume.

MeSH Terms
Animals Barium/metabolism Brain Stem/metabolism Calcium/metabolism Calcium Channels/metabolism Calcium Signaling Egtazic Acid/analogs & derivatives,pharmacology Electric Stimulation Excitatory Postsynaptic Potentials Glutamic Acid/metabolism In Vitro Techniques Ion Transport Membrane Potentials Presynaptic Terminals/metabolism Rats Rats, Wistar Synapses/drug effects,metabolism Synaptic Transmission
Chemicals
Calcium Channels Barium Glutamic Acid Egtazic Acid 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Borst J G
Max-Planck-Institut fur medizinische Forschung, Abteilung Zellphysiologie, Jahnstrasse 29, D-69120 Heidelberg, Germany.
Sakmann B
References (60)
60 references, click to expand
  1. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat.
    J Comp Neurol. 1993 Feb 8;328(2):161-84 PMID: 8423239
  2. Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem.
    Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):347-55 PMID: 10212483
  3. The effect of surface charge on the voltage-dependent conductance induced in thin lipid membranes by monazomycin.
    J Gen Physiol. 1972 Sep;60(3):285-306 PMID: 5055790
  4. Calcium and potassium changes in extracellular microenvironment of cat cerebellar cortex.
    J Neurophysiol. 1978 Jul;41(4):1026-39 PMID: 681986
  5. Aminophospholipid asymmetry in murine synaptosomal plasma membrane.
    J Neurochem. 1980 Feb;34(2):269-77 PMID: 6251164
  6. Changes in extracellular Ca2+ and K+ activity accompanying hippocampal discharges.
    Can J Physiol Pharmacol. 1980 May;58(5):579-82 PMID: 7417888
  7. Diffusion of calcium ions in retinal rods. A theoretical calculation.
    J Gen Physiol. 1981 Apr;77(4):475-87 PMID: 7241090
  8. Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization.
    J Physiol. 1981 Mar;312:177-207 PMID: 6267262
  9. Early transient depletion of extracellular Ca during individual cardiac muscle contractions.
    Am J Physiol. 1983 Mar;244(3):H462-8 PMID: 6829789
  10. Inactivation of Ca channels.
    Prog Biophys Mol Biol. 1984;44(3):215-67 PMID: 6095365
  11. Aging in the rat medial nucleus of the trapezoid body. II. Electron microscopy.
    J Comp Neurol. 1985 Feb 15;232(3):401-13 PMID: 3973099
  12. Calcium at the surface of cardiac plasma membrane vesicles: cation binding, surface charge screening, and Na-Ca exchange.
    J Membr Biol. 1985;85(3):251-61 PMID: 4032459
  13. Extracellular calcium and potassium concentration changes in chronic epileptic brain tissue.
    Adv Neurol. 1986;44:641-61 PMID: 3518350
  14. Ultrastructural localization of calcium in the CNS of vertebrates.
    Histochemistry. 1986;85(3):231-9 PMID: 3744905
  15. Calcium diffusion in the brain cell microenvironment.
    Can J Physiol Pharmacol. 1987 May;65(5):1086-91 PMID: 3621033
  16. Age-related loss of synaptic terminals in the rat medial nucleus of the trapezoid body.
    Neuroscience. 1988 Jan;24(1):189-94 PMID: 3368047
  17. Phospholipid asymmetry in cardiac sarcolemma. Analysis of intact cells and 'gas-dissected' membranes.
    Biochim Biophys Acta. 1988 Aug 18;943(2):256-66 PMID: 3401480
  18. Divalent cation dependent inactivation of the high-voltage-activated Ca-channel current in chick sensory neurons.
    Pflugers Arch. 1988 Jun;411(6):695-7 PMID: 2457872
  19. The electrostatic properties of membranes.
    Annu Rev Biophys Biophys Chem. 1989;18:113-36 PMID: 2660821
  20. Calcium currents in bullfrog sympathetic neurons. II. Inactivation.
    J Gen Physiol. 1989 Jul;94(1):169-82 PMID: 2553857
  21. New structural features of synapses in the anteroventral cochlear nucleus prepared by direct freezing and freeze-substitution.
    J Comp Neurol. 1989 Dec 15;290(3):343-57 PMID: 2592616
  22. Membrane electrostatics.
    Biochim Biophys Acta. 1990 Oct 8;1031(3):311-82 PMID: 2223819
  23. Diffusion around a cardiac calcium channel and the role of surface bound calcium.
    Biophys J. 1991 Mar;59(3):703-21 PMID: 1646660
  24. Inactivation kinetics of calcium current of acutely dissociated CA1 pyramidal cells of the mature guinea-pig hippocampus.
    J Physiol. 1991 Jun;437:27-48 PMID: 1653853
  25. Do astrocytes process neural information?
    Prog Brain Res. 1992;94:119-36 PMID: 1337609
  26. The binaural auditory pathway: excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body.
    Proc Biol Sci. 1993 Feb 22;251(1331):151-7 PMID: 8096081
  27. Re-evaluation of calcium currents in pre- and postsynaptic neurones of the chick ciliary ganglion.
    J Physiol. 1993 Jan;460:153-72 PMID: 7683716
  28. Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology.
    Exp Brain Res. 1993;95(2):223-39 PMID: 8224048
  29. Neighboring cerebellar Purkinje cells communicate via retrograde inhibition of common presynaptic interneurons.
    Neuron. 1993 Nov;11(5):885-93 PMID: 8240811
  30. Inactivation of N-type calcium current in chick sensory neurons: calcium and voltage dependence.
    J Gen Physiol. 1994 Aug;104(2):311-36 PMID: 7807051
  31. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS.
    Neuron. 1995 Jul;15(1):193-204 PMID: 7619522
  32. Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons.
    J Neurosci. 1996 Jan;16(1):115-22 PMID: 8613777
  33. Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices.
    J Physiol. 1995 Oct 15;488 ( Pt 2):387-406 PMID: 8568678
  34. High resolution ultrastructural mapping of total calcium: electron spectroscopic imaging/electron energy loss spectroscopy analysis of a physically/chemically processed nerve-muscle preparation.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4799-803 PMID: 8643483
  35. Ca(2+)-dependent exocytosis in the somata of dorsal root ganglion neurons.
    Neuron. 1996 Jul;17(1):135-45 PMID: 8755485
  36. Calcium in the nerve terminals of chick ciliary ganglia during facilitation, augmentation and potentiation.
    J Physiol. 1995 Dec 15;489 ( Pt 3):637-48 PMID: 8788930
  37. Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat.
    J Physiol. 1995 Dec 15;489 ( Pt 3):825-40 PMID: 8788946
  38. Calcium influx and transmitter release in a fast CNS synapse.
    Nature. 1996 Oct 3;383(6599):431-4 PMID: 8837774
  39. Presynaptic calcium currents at voltage-clamped excitor and inhibitor nerve terminals of crayfish.
    J Physiol. 1996 Oct 15;496 ( Pt 2):347-61 PMID: 8910221
  40. Calcium dynamics associated with a single action potential in a CNS presynaptic terminal.
    Biophys J. 1997 Mar;72(3):1458-71 PMID: 9138591
  41. Assessment of frequency-dependent alterations in the level of extracellular Ca2+ in the synaptic cleft.
    Biophys J. 1997 May;72(5):2103-16 PMID: 9129812
  42. Ca2+- and voltage-dependent inactivation of Ca2+ channels in nerve terminals of the neurohypophysis.
    J Neurosci. 1997 Aug 1;17(15):5772-81 PMID: 9221775
  43. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression.
    Neuron. 1999 Aug;23(4):821-32 PMID: 10482247
  44. Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors.
    J Neurosci. 1997 Nov 1;17(21):8137-46 PMID: 9334389
  45. Encoding of timing in the brain stem auditory nuclei of vertebrates.
    Neuron. 1997 Nov;19(5):959-62 PMID: 9390510
  46. Retrograde signaling in the development and modification of synapses.
    Physiol Rev. 1998 Jan;78(1):143-70 PMID: 9457171
  47. Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem.
    J Physiol. 1998 Jan 1;506 ( Pt 1):143-57 PMID: 9481678
  48. Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release.
    Neuron. 1998 Mar;20(3):389-99 PMID: 9539117
  49. R-type Ca2+ currents evoke transmitter release at a rat central synapse.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4720-5 PMID: 9539805
  50. Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse.
    Neuron. 1998 Apr;20(4):797-807 PMID: 9581770
  51. Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem.
    J Physiol. 1998 Jun 1;509 ( Pt 2):419-23 PMID: 9575291
  52. Preferential closed-state inactivation of neuronal calcium channels.
    Neuron. 1998 May;20(5):1027-38 PMID: 9620706
  53. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles.
    Nature. 1998 Jul 23;394(6691):384-8 PMID: 9690475
  54. Synapses in hippocampus occupy only 1-2% of cell membranes and are spaced less than half-micron apart: a quantitative ultrastructural analysis with discussion of physiological implications.
    Neuropharmacology. 1998 Apr-May;37(4-5):513-21 PMID: 9704992
  55. Calcium influx during an action potential.
    Methods Enzymol. 1998;293:352-71 PMID: 9711618
  56. Facilitation of presynaptic calcium currents in the rat brainstem.
    J Physiol. 1998 Nov 15;513 ( Pt 1):149-55 PMID: 9782166
  57. Computational properties of peri-dendritic calcium fluctuations.
    J Neurosci. 1998 Nov 1;18(21):8580-9 PMID: 9786966
  58. Postsynaptic Ca2+ influx mediated by three different pathways during synaptic transmission at a calyx-type synapse.
    J Neurosci. 1998 Dec 15;18(24):10409-19 PMID: 9852578
  59. Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses.
    J Neurosci. 1999 Jan 15;19(2):726-36 PMID: 9880593
  60. The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus.
    Am J Anat. 1966 Mar;118(2):375-89 PMID: 5917192
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
DOI
10.1111/j.1469-7793.1999.00123.x
Published
1999-11-15
Pages
123-33
Language
English
Region
England
NLM ID
0266262
PMCID
PMC2269650
Subset
IM
External Links
PubMed source DOI: 10.1111/j.1469-7793.1999.00123.x PMC Full Text View journal details
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