Home LiteratureArticle Details
PMID: 9852584 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type.

Bi GQ, Poo MM

Abstract

In cultures of dissociated rat hippocampal neurons, persistent potentiation and depression of glutamatergic synapses were induced by correlated spiking of presynaptic and postsynaptic neurons. The relative timing between the presynaptic and postsynaptic spiking determined the direction and the extent of synaptic changes. Repetitive postsynaptic spiking within a time window of 20 msec after presynaptic activation resulted in long-term potentiation (LTP), whereas postsynaptic spiking within a window of 20 msec before the repetitive presynaptic activation led to long-term depression (LTD). Significant LTP occurred only at synapses with relatively low initial strength, whereas the extent of LTD did not show obvious dependence on the initial synaptic strength. Both LTP and LTD depended on the activation of NMDA receptors and were absent in cases in which the postsynaptic neurons were GABAergic in nature. Blockade of L-type calcium channels with nimodipine abolished the induction of LTD and reduced the extent of LTP. These results underscore the importance of precise spike timing, synaptic strength, and postsynaptic cell type in the activity-induced modification of central synapses and suggest that Hebb's rule may need to incorporate a quantitative consideration of spike timing that reflects the narrow and asymmetric window for the induction of synaptic modification.

MeSH Terms
6-Cyano-7-nitroquinoxaline-2,3-dione/pharmacology Action Potentials/drug effects,physiology Animals Bicuculline/pharmacology Calcium Channels/drug effects,physiology Cells, Cultured Embryo, Mammalian Excitatory Postsynaptic Potentials/drug effects,physiology Glutamic Acid/physiology Hippocampus/physiology In Vitro Techniques Long-Term Potentiation Neurons/drug effects,physiology Nimodipine/pharmacology Patch-Clamp Techniques Rats Synapses/drug effects,physiology Time Factors gamma-Aminobutyric Acid/physiology
Chemicals
Calcium Channels Glutamic Acid gamma-Aminobutyric Acid Nimodipine 6-Cyano-7-nitroquinoxaline-2,3-dione Bicuculline
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bi G Q
Department of Biology, University of California at San Diego, La Jolla, California 92093, USA.
Poo M M
References (57)
57 references, click to expand
  1. Hebbian synapses: biophysical mechanisms and algorithms.
    Annu Rev Neurosci. 1990;13:475-511 PMID: 2183685
  2. Hippocampal interneurons express a novel form of synaptic plasticity.
    Neuron. 1997 Feb;18(2):295-305 PMID: 9052799
  3. The role of dendritic action potentials and Ca2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons.
    Learn Mem. 1996 Sep-Oct;3(2-3):160-9 PMID: 10456086
  4. Experience-dependent, asymmetric expansion of hippocampal place fields.
    Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8918-21 PMID: 9238078
  5. Target-specific expression of presynaptic mossy fiber plasticity.
    Science. 1998 Feb 27;279(5355):1368-70 PMID: 9478900
  6. Alpha isoform of calcium-calmodulin dependent protein kinase II (CAM II kinase-alpha) restricted to excitatory synapses in the CA1 region of rat hippocampus.
    Neuroreport. 1997 Apr 14;8(6):1475-9 PMID: 9172157
  7. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex.
    J Neurosci. 1982 Jan;2(1):32-48 PMID: 7054394
  8. Synaptic plasticity in a cerebellum-like structure depends on temporal order.
    Nature. 1997 May 15;387(6630):278-81 PMID: 9153391
  9. The role of calcium-calmodulin kinase II in three forms of synaptic plasticity.
    Curr Biol. 1994 Aug 1;4(8):687-93 PMID: 7953554
  10. Why spikes? Hebbian learning and retrieval of time-resolved excitation patterns.
    Biol Cybern. 1993;69(5-6):503-15 PMID: 7903867
  11. Reliability of spike timing in neocortical neurons.
    Science. 1995 Jun 9;268(5216):1503-6 PMID: 7770778
  12. Calcium signaling in dendritic spines of hippocampal neurons.
    J Neurobiol. 1994 Mar;25(3):234-42 PMID: 8195788
  13. A synaptic model of memory: long-term potentiation in the hippocampus.
    Nature. 1993 Jan 7;361(6407):31-9 PMID: 8421494
  14. Postsynaptic induction and presynaptic expression of hippocampal long-term depression.
    Science. 1994 May 20;264(5162):1148-52 PMID: 7909958
  15. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9574-8 PMID: 2556718
  16. Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons.
    Nature. 1995 Jan 12;373(6510):155-8 PMID: 7816097
  17. Properties of inhibitory and excitatory synapses between hippocampal neurons in very low density cultures.
    Synapse. 1994 Oct;18(2):128-51 PMID: 7839312
  18. Learning-related synaptic plasticity: LTP and LTD.
    Curr Opin Neurobiol. 1991 Jun;1(1):113-20 PMID: 1822291
  19. Presynaptic calcium in transmitter release and posttetanic potentiation.
    Ann N Y Acad Sci. 1991;635:191-207 PMID: 1683751
  20. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons.
    Nature. 1997 Jun 26;387(6636):869-75 PMID: 9202119
  21. Activity-dependent long-term enhancement of transmitter release by presynaptic 3',5'-cyclic GMP in cultured hippocampal neurons.
    Nature. 1995 Jul 6;376(6535):74-80 PMID: 7596438
  22. Hebbian learning reconsidered: representation of static and dynamic objects in associative neural nets.
    Biol Cybern. 1989;60(6):457-67 PMID: 11455966
  23. The absence of a major Ca2+ signaling pathway in GABAergic neurons of the hippocampus.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3245-50 PMID: 9501248
  24. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4363-7 PMID: 1350090
  25. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons.
    Science. 1997 Jan 10;275(5297):209-13 PMID: 8985013
  26. Contrasting properties of two forms of long-term potentiation in the hippocampus.
    Nature. 1995 Sep 14;377(6545):115-8 PMID: 7675078
  27. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus.
    Neuron. 1992 Nov;9(5):967-75 PMID: 1419003
  28. Long-term synaptic depression.
    Annu Rev Neurosci. 1995;18:319-57 PMID: 7605065
  29. Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation.
    Neuron. 1992 Jul;9(1):121-8 PMID: 1632966
  30. Active properties of neuronal dendrites.
    Annu Rev Neurosci. 1996;19:165-86 PMID: 8833440
  31. Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity.
    Neuron. 1996 Jun;16(6):1147-57 PMID: 8663991
  32. A physiological mechanism for Hebb's postulate of learning.
    Proc Natl Acad Sci U S A. 1973 Apr;70(4):997-1001 PMID: 4352227
  33. Muscarinic activation of ionic currents measured by a new whole-cell recording method.
    J Gen Physiol. 1988 Aug;92(2):145-59 PMID: 2459299
  34. Propagation of activity-dependent synaptic depression in simple neural networks.
    Nature. 1997 Jul 31;388(6641):439-48 PMID: 9242402
  35. Simple neural models of classical conditioning.
    Biol Cybern. 1986;55(2-3):187-200 PMID: 3801536
  36. Learning navigational maps through potentiation and modulation of hippocampal place cells.
    J Comput Neurosci. 1997 Jan;4(1):79-94 PMID: 9046453
  37. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.
    Science. 1997 Jan 10;275(5297):213-5 PMID: 8985014
  38. Presynaptic mechanism for long-term potentiation in the hippocampus.
    Nature. 1990 Aug 23;346(6286):724-9 PMID: 2167454
  39. Toward a modern theory of adaptive networks: expectation and prediction.
    Psychol Rev. 1981 Mar;88(2):135-70 PMID: 7291377
  40. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures.
    J Physiol. 1998 Feb 15;507 ( Pt 1):237-47 PMID: 9490845
  41. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity.
    Neuron. 1996 Jan;16(1):89-101 PMID: 8562094
  42. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  43. Postsynaptic levels of [Ca2+]i needed to trigger LTD and LTP.
    Neuron. 1996 Mar;16(3):619-29 PMID: 8785059
  44. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path.
    J Physiol. 1973 Jul;232(2):331-56 PMID: 4727084
  45. A critical window for cooperation and competition among developing retinotectal synapses.
    Nature. 1998 Sep 3;395(6697):37-44 PMID: 9738497
  46. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms.
    Trends Neurosci. 1993 Dec;16(12):521-7 PMID: 7509523
  47. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons.
    J Physiol. 1995 Aug 15;487(1):67-90 PMID: 7473260
  48. Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7332-6 PMID: 8692993
  49. Low access resistance perforated patch recordings using amphotericin B.
    J Neurosci Methods. 1991 Mar;37(1):15-26 PMID: 2072734
  50. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus.
    Neuroscience. 1983 Apr;8(4):791-7 PMID: 6306504
  51. Long-term depression properties in a simple system.
    Neuron. 1996 Jan;16(1):103-11 PMID: 8562073
  52. Dendritic spines as basic functional units of neuronal integration.
    Nature. 1995 Jun 22;375(6533):682-4 PMID: 7791901
  53. Pattern recognition computation using action potential timing for stimulus representation.
    Nature. 1995 Jul 6;376(6535):33-6 PMID: 7596429
  54. Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx.
    J Neurophysiol. 1995 Jun;73(6):2553-7 PMID: 7666160
  55. Contribution of voltage-gated Ca2+ channels to homosynaptic long-term depression in the CA1 region in vitro.
    J Neurophysiol. 1997 Mar;77(3):1651-5 PMID: 9084630
  56. Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons.
    Nature. 1998 Mar 12;392(6672):198-202 PMID: 9515967
  57. Reproducibility and variability in neural spike trains.
    Science. 1997 Mar 21;275(5307):1805-8 PMID: 9065407
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1998-12-15
Pages
10464-72
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6793365
Subset
IM
Grants
NINDS NIH HHS · R01 NS036999 · United States
NINDS NIH HHS · NS36999 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]