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PMID: 18701072 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Local dendritic activity sets release probability at hippocampal synapses.

Neuron ·Vol. 59 ·No. 3 ·2008-08-14 ·Pages 475-85

Branco T, Staras K, Darcy KJ, Goda Y

Abstract

The arrival of an action potential at a synapse triggers neurotransmitter release with a limited probability, p(r). Although p(r) is a fundamental parameter in defining synaptic efficacy, it is not uniform across all synapses, and the mechanisms by which a given synapse sets its basal release probability are unknown. By measuring p(r) at single presynaptic terminals in connected pairs of hippocampal neurons, we show that neighboring synapses on the same dendritic branch have very similar release probabilities, and p(r) is negatively correlated with the number of synapses on the branch. Increasing dendritic depolarization elicits a homeostatic decrease in p(r), and equalizing activity in the dendrite significantly reduces its variability. Our results indicate that local dendritic activity is the major determinant of basal release probability, and we suggest that this feedback regulation might be required to maintain synapses in their operational range.

MeSH Terms
Action Potentials/physiology Animals Animals, Newborn Cells, Cultured Dendrites/metabolism,ultrastructure Electric Stimulation/methods Excitatory Postsynaptic Potentials/physiology,radiation effects Hippocampus/cytology Image Processing, Computer-Assisted Microscopy, Electron, Transmission Models, Neurological Neurons/cytology Patch-Clamp Techniques Probability Pyridinium Compounds/metabolism Quaternary Ammonium Compounds/metabolism Rats Synapses/metabolism,ultrastructure
Chemicals
FM1 43 Pyridinium Compounds Quaternary Ammonium Compounds
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Branco Tiago
MRC Laboratory for Molecular Cell Biology and Cell Biology Unit, University College London, Gower Street, London WC1E6BT, UK. [email protected]
Staras Kevin
Darcy Kevin J
Goda Yukiko
References (57)
57 references, click to expand
  1. Temporal regulation of the expression locus of homeostatic plasticity.
    J Neurophysiol. 2006 Oct;96(4):2127-33 PMID: 16760351
  2. Heterogeneity of release probability, facilitation, and depletion at central synapses.
    Neuron. 1997 Jun;18(6):995-1008 PMID: 9208866
  3. Quantal release at visualized terminals of a crayfish motor axon: intraterminal and regional differences.
    J Comp Neurol. 1996 Nov 25;375(4):583-600 PMID: 8930787
  4. Computational subunits in thin dendrites of pyramidal cells.
    Nat Neurosci. 2004 Jun;7(6):621-7 PMID: 15156147
  5. Long-term regulation of short-term plasticity: a postsynaptic influence on presynaptic transmitter release.
    J Physiol Paris. 1995;89(1):33-41 PMID: 7581297
  6. Heterogeneous release properties of visualized individual hippocampal synapses.
    Neuron. 1997 Apr;18(4):599-612 PMID: 9136769
  7. Non-uniform release at the frog neuromuscular junction: evidence of morphological and physiological plasticity.
    Brain Res. 1987 Mar;434(1):95-116 PMID: 2882823
  8. Nonuniform probability of glutamate release at a hippocampal synapse.
    Science. 1993 Oct 29;262(5134):754-7 PMID: 7901909
  9. The probability of transmitter release at a mammalian central synapse.
    Nature. 1993 Dec 9;366(6455):569-72 PMID: 7902955
  10. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons.
    Nat Neurosci. 2006 Mar;9(3):315-21 PMID: 16462738
  11. Optical detection of a quantal presynaptic membrane turnover.
    Nature. 1997 Jul 31;388(6641):478-82 PMID: 9242407
  12. Adaptation to synaptic inactivity in hippocampal neurons.
    Neuron. 2005 Sep 1;47(5):725-37 PMID: 16129401
  13. Hebb and homeostasis in neuronal plasticity.
    Curr Opin Neurobiol. 2000 Jun;10(3):358-64 PMID: 10851171
  14. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons.
    J Neurosci. 2004 Dec 8;24(49):11046-56 PMID: 15590921
  15. Enhancement of synaptic plasticity through chronically reduced Ca2+ flux during uncorrelated activity.
    Neuron. 2004 Dec 2;44(5):835-49 PMID: 15572114
  16. Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites.
    Nat Neurosci. 2004 Apr;7(4):373-9 PMID: 15004561
  17. Amplitude fluctuations in synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses.
    J Physiol. 1983 Oct;343:135-45 PMID: 6644615
  18. Pharmacology and functions of metabotropic glutamate receptors.
    Annu Rev Pharmacol Toxicol. 1997;37:205-37 PMID: 9131252
  19. Matching of excitatory and inhibitory inputs to crustacean muscle fibers.
    J Neurophysiol. 1971 Jan;34(1):157-70 PMID: 4322251
  20. Quantal size is independent of the release probability at hippocampal excitatory synapses.
    J Neurosci. 2005 Jan 5;25(1):223-32 PMID: 15634785
  21. The probability of quantal secretion along visualized terminal branches at amphibian (Bufo marinus) neuromuscular synapses.
    J Physiol. 1986 Oct;379:257-74 PMID: 2882019
  22. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis.
    Cell. 2006 May 19;125(4):785-99 PMID: 16713568
  23. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis.
    Neuron. 2006 Nov 22;52(4):663-77 PMID: 17114050
  24. Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons.
    J Neurosci. 2000 Nov 1;20(21):7922-31 PMID: 11050112
  25. Estimating the distribution of synaptic reliabilities.
    J Neurophysiol. 1997 Dec;78(6):2870-80 PMID: 9405507
  26. Quantal analysis of synaptic potentials in neurons of the central nervous system.
    Physiol Rev. 1990 Jan;70(1):165-98 PMID: 2404288
  27. The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents.
    J Physiol. 1981 Dec;321:65-96 PMID: 6279826
  28. Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion.
    Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12748-53 PMID: 11675506
  29. Quantal components of the end-plate potential.
    J Physiol. 1954 Jun 28;124(3):560-73 PMID: 13175199
  30. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse.
    Nature. 2001 May 17;411(6835):317-21 PMID: 11357135
  31. The interplay between homeostatic synaptic plasticity and functional dendritic compartments.
    J Neurophysiol. 2006 Jul;96(1):276-83 PMID: 16554518
  32. Different properties of synapses between a single sensory neurone and two different motor cells in the leech C.N.S.
    J Physiol. 1974 Apr;238(2):357-69 PMID: 4366432
  33. Inactivity produces increases in neurotransmitter release and synapse size.
    Neuron. 2001 Nov 20;32(4):673-82 PMID: 11719207
  34. Visualization of changes in presynaptic function during long-term synaptic plasticity.
    Nat Neurosci. 2001 Jul;4(7):711-7 PMID: 11426227
  35. Target-cell-specific facilitation and depression in neocortical circuits.
    Nat Neurosci. 1998 Aug;1(4):279-85 PMID: 10195160
  36. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons.
    Nature. 2002 Nov 28;420(6914):414-8 PMID: 12459783
  37. Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons.
    Eur J Neurosci. 2006 Sep;24(5):1286-98 PMID: 16987216
  38. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses.
    Neuron. 2006 Sep 21;51(6):773-86 PMID: 16982422
  39. Nonuniform release probabilities underlie quantal synaptic transmission at a mammalian excitatory central synapse.
    J Neurophysiol. 1988 Sep;60(3):889-908 PMID: 2845016
  40. Morphological correlates of functionally defined synaptic vesicle populations.
    Nat Neurosci. 2001 Apr;4(4):391-5 PMID: 11276229
  41. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors.
    Nat Neurosci. 2004 Mar;7(3):244-53 PMID: 14770185
  42. 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
  43. The NEURON simulation environment.
    Neural Comput. 1997 Aug 15;9(6):1179-209 PMID: 9248061
  44. Changes in reliability of synaptic function as a mechanism for plasticity.
    Nature. 1994 Oct 20;371(6499):704-7 PMID: 7935816
  45. Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release.
    J Neurosci. 1993 Jul;13(7):3075-89 PMID: 8331385
  46. 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
  47. Novel presynaptic mechanisms for coincidence detection in synaptic plasticity.
    Curr Opin Neurobiol. 2006 Jun;16(3):312-22 PMID: 16713246
  48. Synaptic gain control and homeostasis.
    Curr Opin Neurobiol. 2003 Oct;13(5):560-7 PMID: 14630218
  49. Matching of facilitation at the neuromuscular junction of the lobster: a possible case for influence of muscle on nerve.
    J Physiol. 1973 Sep;233(3):635-58 PMID: 4356843
  50. Chronic blockade of glutamate receptors enhances presynaptic release and downregulates the interaction between synaptophysin-synaptobrevin-vesicle-associated membrane protein 2.
    J Neurosci. 2001 Sep 1;21(17):6588-96 PMID: 11517248
  51. Homeostatic control of neural activity: from phenomenology to molecular design.
    Annu Rev Neurosci. 2006;29:307-23 PMID: 16776588
  52. Dynamic stochastic synapses as computational units.
    Neural Comput. 1999 May 15;11(4):903-17 PMID: 10226188
  53. Target cell-dependent normalization of transmitter release at neocortical synapses.
    Science. 2005 May 6;308(5723):863-6 PMID: 15774725
  54. Quantal analysis of excitatory synapses in rat hippocampal CA1 in vitro during low-frequency depression.
    J Physiol. 1997 Dec 1;505 ( Pt 2):457-71 PMID: 9423186
  55. Modulation of synaptic transmission at Ia-afferent fiber connections on motoneurons during high-frequency stimulation: role of postsynaptic target.
    J Neurophysiol. 1991 Mar;65(3):590-7 PMID: 1646867
  56. Paired-pulse modulation of fast excitatory synaptic currents in microcultures of rat hippocampal neurons.
    J Physiol. 1995 Oct 1;488 ( Pt 1):85-101 PMID: 8568668
  57. Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1.
    J Neurosci. 1993 Sep;13(9):3736-48 PMID: 8366344
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
1097-4199
DOI
10.1016/j.neuron.2008.07.006
Email
[email protected]
Published
2008-08-14
Pages
475-85
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC6390949
Subset
IM
Grants
Wellcome Trust · United Kingdom
Wellcome Trust · 068718 · United Kingdom
Medical Research Council · MC_U122669937 · United Kingdom
External Links
PubMed source DOI: 10.1016/j.neuron.2008.07.006 PMC Full Text View journal details
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