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PMID: 11826095 Published · ppublish English Journal Article

Development of vesicle pools during maturation of hippocampal synapses.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 22 ·No. 3 ·2002-02-01 ·Pages 654-65

Mozhayeva MG, Sara Y, Liu X, Kavalali ET

Abstract

We studied the emergence of vesicle pool organization at developing hippocampal synapses by monitoring vesicle recycling and neurotransmitter release as well as examining electron micrographs. Our analysis suggests that presynaptic boutons go through three distinct functional states to mature. At the onset the synapses lack readily releasable vesicles although they possess a pool of recycling vesicles that can release neurotransmitters under strong stimulation. In the next stage the majority of these recycling vesicles switches to a functionally docked state and forms the readily releasable pool (RRP). After assembly of the RRP, new vesicles build the reserve pool. At the mature state the size of the RRP increases linearly with increasing recycling pool size. Furthermore, this preferential filling of the RRP during early synapse maturation is reduced strikingly in synapses deficient in synapsin I and II. Taken together, these results expose a mechanism that ensures functionally effective allocation of a limited number of vesicles in a CNS synapse.

MeSH Terms
Action Potentials/physiology Aging/metabolism Animals Cells, Cultured Electric Stimulation Fluorescent Dyes/metabolism,pharmacokinetics Hippocampus/cytology,metabolism,ultrastructure Hypertonic Solutions/pharmacology Mice Microscopy, Electron Patch-Clamp Techniques Presynaptic Terminals/drug effects,metabolism,ultrastructure Pyridinium Compounds/metabolism,pharmacokinetics Quaternary Ammonium Compounds/metabolism,pharmacokinetics Rats Rats, Sprague-Dawley Stimulation, Chemical Synapses/drug effects,metabolism,ultrastructure Synapsins/metabolism Synaptic Vesicles/metabolism,ultrastructure
Chemicals
FM1 43 Fluorescent Dyes Hypertonic Solutions Pyridinium Compounds Quaternary Ammonium Compounds Synapsins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Mozhayeva Marina G
Center for Basic Neuroscience and Department of Physiology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111, USA.
Sara Yildirim
Liu Xinran
Kavalali Ege T
References (58)
58 references, click to expand
  1. Kinetics and regulation of fast endocytosis at hippocampal synapses.
    Nature. 1998 Aug 6;394(6693):581-5 PMID: 9707119
  2. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation.
    Neuron. 1996 Jul;17(1):91-102 PMID: 8755481
  3. Vesicle pool mobilization during action potential firing at hippocampal synapses.
    Neuron. 1995 May;14(5):983-9 PMID: 7748565
  4. Heterogeneity of release probability, facilitation, and depletion at central synapses.
    Neuron. 1997 Jun;18(6):995-1008 PMID: 9208866
  5. Dynamics of synaptic vesicles in cultured spinal cord neurons in relationship to synaptogenesis.
    Mol Cell Neurosci. 1996 Jun;7(6):443-52 PMID: 8875428
  6. Target-specific expression of presynaptic mossy fiber plasticity.
    Science. 1998 Feb 27;279(5355):1368-70 PMID: 9478900
  7. Kinetics of synaptic depression and vesicle recycling after tetanic stimulation of frog motor nerve terminals.
    Biophys J. 1998 Jun;74(6):3003-9 PMID: 9635754
  8. Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus.
    Neuron. 1997 Sep;19(3):635-51 PMID: 9331354
  9. Short-term synaptic plasticity is altered in mice lacking synapsin I.
    Cell. 1993 Nov 19;75(4):661-70 PMID: 7902212
  10. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression.
    Neuron. 1999 Aug;23(4):821-32 PMID: 10482247
  11. Short-term synaptic plasticity.
    Annu Rev Neurosci. 1989;12:13-31 PMID: 2648947
  12. Development of excitatory circuitry in the hippocampus.
    J Neurophysiol. 1998 Apr;79(4):2013-24 PMID: 9535965
  13. Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin.
    J Neurosci. 1998 Mar 15;18(6):2028-39 PMID: 9482790
  14. Activity-dependent regulation of synaptic clustering in a hippocampal culture system.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12893-900 PMID: 10536019
  15. Imaging exocytosis and endocytosis.
    Curr Opin Neurobiol. 1996 Jun;6(3):365-71 PMID: 8794083
  16. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions.
    J Comp Neurol. 1981 Jan 1;195(1):51-86 PMID: 7204652
  17. Readily releasable pool size changes associated with long term depression.
    Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1283-8 PMID: 9448323
  18. Fine structure of synaptogenesis in the vertebrate central nervous system.
    Synapse. 1989;3(3):255-85 PMID: 2655146
  19. Definition of the readily releasable pool of vesicles at hippocampal synapses.
    Neuron. 1996 Jun;16(6):1197-207 PMID: 8663996
  20. Long-term potentiation and functional synapse induction in developing hippocampus.
    Nature. 1996 May 2;381(6577):71-5 PMID: 8609991
  21. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells.
    J Physiol. 1999 Feb 15;515 ( Pt 1):181-202 PMID: 9925888
  22. Developmental regulation of basket/stellate cell-->Purkinje cell synapses in the cerebellum.
    J Neurosci. 1997 Dec 1;17(23):9104-12 PMID: 9364057
  23. Visualization of synaptic activity in hippocampal slices with FM1-43 enabled by fluorescence quenching.
    Neuron. 1999 Dec;24(4):803-8 PMID: 10624944
  24. Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors.
    J Neurosci. 1997 Nov 1;17(21):8137-46 PMID: 9334389
  25. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells.
    Neuron. 1993 Jan;10(1):21-30 PMID: 8427700
  26. Properties of fast endocytosis at hippocampal synapses.
    Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):337-46 PMID: 10212482
  27. Regulation of hippocampal transmitter release during development and long-term potentiation.
    Science. 1995 Sep 22;269(5231):1730-4 PMID: 7569903
  28. Tetanus toxin blocks the exocytosis of synaptic vesicles clustered at synapses but not of synaptic vesicles in isolated axons.
    J Neurosci. 1999 Aug 15;19(16):6723-32 PMID: 10436029
  29. Heterogeneous release properties of visualized individual hippocampal synapses.
    Neuron. 1997 Apr;18(4):599-612 PMID: 9136769
  30. Assembly of presynaptic active zones from cytoplasmic transport packets.
    Nat Neurosci. 2000 May;3(5):445-51 PMID: 10769383
  31. Quantitative ultrastructural analysis of hippocampal excitatory synapses.
    J Neurosci. 1997 Aug 1;17(15):5858-67 PMID: 9221783
  32. The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis.
    J Neurocytol. 1983 Aug;12(4):599-616 PMID: 6619906
  33. Cytosolic Ca2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells.
    Neuron. 1998 Jun;20(6):1243-53 PMID: 9655511
  34. Ca2+ or Sr2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin.
    J Neurosci. 1997 Oct 1;17(19):7190-202 PMID: 9295365
  35. Maturation of a central glutamatergic synapse.
    Science. 1996 Nov 8;274(5289):972-6 PMID: 8875937
  36. Hippocampal synaptogenesis in cell culture: developmental time course of synapse formation, calcium influx, and synaptic protein distribution.
    J Neurosci. 1994 Nov;14(11 Pt 1):6402-11 PMID: 7965045
  37. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment.
    Neuron. 2000 Jul;27(1):57-69 PMID: 10939331
  38. Differential signaling via the same axon of neocortical pyramidal neurons.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5323-8 PMID: 9560274
  39. A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation.
    Neuron. 2001 Feb;29(2):469-84 PMID: 11239436
  40. Synaptic vesicle recycling in synapsin I knock-out mice.
    J Cell Biol. 1996 Sep;134(5):1219-27 PMID: 8794863
  41. Essential functions of synapsins I and II in synaptic vesicle regulation.
    Nature. 1995 Jun 8;375(6531):488-93 PMID: 7777057
  42. Nonuniform probability of glutamate release at a hippocampal synapse.
    Science. 1993 Oct 29;262(5134):754-7 PMID: 7901909
  43. Synapsins as regulators of neurotransmitter release.
    Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):269-79 PMID: 10212475
  44. Rapid reuse of readily releasable pool vesicles at hippocampal synapses.
    Neuron. 2000 Oct;28(1):221-31 PMID: 11086996
  45. Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 neuronal cultures.
    Nat Neurosci. 1999 Jan;2(1):24-30 PMID: 10195176
  46. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons.
    J Cell Biol. 1992 May;117(4):849-61 PMID: 1577861
  47. Target-cell-specific facilitation and depression in neocortical circuits.
    Nat Neurosci. 1998 Aug;1(4):279-85 PMID: 10195160
  48. Reversal of synaptic vesicle docking at central synapses.
    Nat Neurosci. 1999 Jun;2(6):503-7 PMID: 10448213
  49. Distinct pools of synaptic vesicles in neurotransmitter release.
    Nature. 1995 Jun 8;375(6531):493-7 PMID: 7777058
  50. The probability of transmitter release at a mammalian central synapse.
    Nature. 1993 Dec 9;366(6455):569-72 PMID: 7902955
  51. Genetics of synaptic vesicle function: toward the complete functional anatomy of an organelle.
    Annu Rev Physiol. 1999;61:753-76 PMID: 10099709
  52. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses.
    Neuropharmacology. 1995 Nov;34(11):1387-95 PMID: 8606788
  53. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex.
    J Neurosci. 1999 May 15;19(10):3827-35 PMID: 10234015
  54. Quantitation of terminal parameters and their inter-relationships in maturing central synapses: a perspective for experimental studies.
    Brain Res. 1980 Feb 3;183(1):43-59 PMID: 7357409
  55. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9235-9 PMID: 7568108
  56. Reconstitution of the hippocampal mossy fiber and associational-commissural pathways in a novel dissociated cell culture system.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4706-11 PMID: 8643467
  57. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse.
    Neuron. 1999 Jun;23(2):399-409 PMID: 10399944
  58. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons.
    Neuron. 1993 Oct;11(4):713-24 PMID: 8398156
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-02-01
Pages
654-65
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6758530
Subset
IM
External Links
PubMed source PMC Full Text View journal details
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