Dynamic Synapses As Archives of Synaptic History: State-dependent Redistribution of Synaptic Efficacy in the Rat Hippocampal CA1

Overview

Journal J Physiol

Specialty Physiology

Date 2005 Apr 23

PMID 15845579

Citations 8

Authors

Takuya Yasui

Shigeyoshi Fujisawa

Masako Tsukamoto

Norio Matsuki

Yuji Ikegaya

Affiliations

Soon will be listed here.

Abstract

Plastic modifications of synaptic strength are putative mechanisms underlying information processing in the brain, including memory storage, signal integration and filtering. Here we describe a dynamic interplay between short-term and long-term synaptic plasticity. At rat hippocampal CA1 synapses, induction of both long-term potentiation (LTP) and depression (LTD) was accompanied by changes in the profile of short-term plasticity, termed redistribution of synaptic efficacy (RSE). RSE was presynaptically expressed and associated in part with a persistent alteration in hyperpolarization-activated I(h) channel activity. Already potentiated synapses were still capable of showing RSE in response to additional LTP-triggering stimulation. Strikingly, RSE took place even after reversal of LTP or LTD, that is, the same synapse can display different levels of short-term plasticity without changing synaptic efficacy for the initial spike in burst presynaptic firing, thereby modulating spike transmission in a firing rate-dependent manner. Thus, the history of long-term synaptic plasticity is registered in the form of short-term plasticity, and RSE extends the information storage capacity of a synapse and adds another dimension of functional complexity to neuronal operations.

Citing Articles

Incremental induction of NMDAR-STP and NMDAR-LTP in the CA1 area of ventral hippocampal slices relies on graded activation of discrete NMDA receptors.

Ingram R, Volianskis R, Georgiou J, Jane D, Michael-Titus A, Collingridge G Philos Trans R Soc Lond B Biol Sci. 2024; 379(1906):20230239.

PMID: 38853568 PMC: 11343233. DOI: 10.1098/rstb.2023.0239.

Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts.

Raja M, Preobraschenski J, Del Olmo-Cabrera S, Martinez-Turrillas R, Jahn R, Perez-Otano I Elife. 2019; 8.

PMID: 31090538 PMC: 6519982. DOI: 10.7554/eLife.40744.

Two sides to long-term potentiation: a view towards reconciliation.

Padamsey Z, Emptage N Philos Trans R Soc Lond B Biol Sci. 2013; 369(1633):20130154.

PMID: 24298155 PMC: 3843885. DOI: 10.1098/rstb.2013.0154.

The roles of STP and LTP in synaptic encoding.

Volianskis A, Collingridge G, Jensen M PeerJ. 2013; 1:e3.

PMID: 23638365 PMC: 3629019. DOI: 10.7717/peerj.3.

Structural and synaptic plasticity in stress-related disorders.

Christoffel D, Golden S, Russo S Rev Neurosci. 2011; 22(5):535-49.

PMID: 21967517 PMC: 3212803. DOI: 10.1515/RNS.2011.044.

References

Dobrunz L, Stevens C . Response of hippocampal synapses to natural stimulation patterns. Neuron. 1999; 22(1):157-66. DOI: 10.1016/s0896-6273(00)80687-x. View

Fujii S, Saito K, Miyakawa H, Ito K, Kato H . Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res. 1991; 555(1):112-22. DOI: 10.1016/0006-8993(91)90867-u. View

Lee H, Barbarosie M, Kameyama K, Bear M, Huganir R . Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature. 2000; 405(6789):955-9. DOI: 10.1038/35016089. View

Markram H, Tsodyks M . Redistribution of synaptic efficacy: a mechanism to generate infinite synaptic input diversity from a homogeneous population of neurons without changing absolute synaptic efficacies. J Physiol Paris. 1996; 90(3-4):229-32. DOI: 10.1016/s0928-4257(97)81429-5. View

Robinson R, Siegelbaum S . Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol. 2002; 65:453-80. DOI: 10.1146/annurev.physiol.65.092101.142734. View

Dudek S, Bear M . Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci. 1993; 13(7):2910-8. PMC: 6576673. View

Misgeld U, Bijak M, Jarolimek W . A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog Neurobiol. 1995; 46(4):423-62. DOI: 10.1016/0301-0082(95)00012-k. View

Pape H . Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol. 1996; 58:299-327. DOI: 10.1146/annurev.ph.58.030196.001503. View

Siegel S, Brose N, Janssen W, Gasic G, Jahn R, Heinemann S . Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc Natl Acad Sci U S A. 1994; 91(2):564-8. PMC: 42989. DOI: 10.1073/pnas.91.2.564. View

10.

Harris N, Constanti A . Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J Neurophysiol. 1995; 74(6):2366-78. DOI: 10.1152/jn.1995.74.6.2366. View

11.

Caillard O, Ben-Ari Y, Gaiarsa J . Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus. J Physiol. 1999; 518(Pt 1):109-19. PMC: 2269393. DOI: 10.1111/j.1469-7793.1999.0109r.x. View

12.

Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky G, Tibbs G . Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci. 2000; 20(14):5264-75. PMC: 6772310. View

13.

Dobrunz L, Stevens C . Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron. 1997; 18(6):995-1008. DOI: 10.1016/s0896-6273(00)80338-4. View

14.

London M, Schreibman A, Hausser M, Larkum M, Segev I . The information efficacy of a synapse. Nat Neurosci. 2002; 5(4):332-40. DOI: 10.1038/nn826. View

15.

Abbott L, Nelson S . Synaptic plasticity: taming the beast. Nat Neurosci. 2000; 3 Suppl:1178-83. DOI: 10.1038/81453. View

16.

Tanaka T, Saito H, Matsuki N . Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J Neurosci. 1997; 17(9):2959-66. PMC: 6573653. View

17.

Bolshakov V, Golan H, Kandel E, Siegelbaum S . Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron. 1997; 19(3):635-51. DOI: 10.1016/s0896-6273(00)80377-3. View

18.

Henze D, Wittner L, Buzsaki G . Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci. 2002; 5(8):790-5. DOI: 10.1038/nn887. View

19.

Soleng A, Chiu K, Raastad M . Unmyelinated axons in the rat hippocampus hyperpolarize and activate an H current when spike frequency exceeds 1 Hz. J Physiol. 2003; 552(Pt 2):459-70. PMC: 2343371. DOI: 10.1113/jphysiol.2003.048058. View

20.

Bienenstock E, Cooper L, Munro P . Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982; 2(1):32-48. PMC: 6564292. View