An Experimental Test of the Role of Postsynaptic Calcium Levels in Determining Synaptic Strength Using Perirhinal Cortex of Rat

Overview

Journal J Physiol

Specialty Physiology

Date 2001 Apr 18

PMID 11306664

Citations 57

Authors

K Cho

J P Aggleton

M W Brown

Z I Bashir

Affiliations

Soon will be listed here.

Abstract

1. We have investigated the prediction of a relationship between the magnitude of activity-dependent increases in postsynaptic calcium and both the magnitude and direction of synaptic plastic change in the central nervous system. 2. Activity-dependent increases in calcium were buffered to differing degrees using a range of concentrations of EGTA and the effects on synaptic plasticity were assessed. Activity-dependent synaptic plasticity was induced during whole-cell recording in rat perirhinal cortex in vitro. In control conditions (0.5 mM EGTA) low frequency stimulation (LFS; 200 stimuli) delivered to neurones held at -40 or -70 mV induced long-term depression (LTD) or, at -10 mV, induced long-term potentiation (LTP). 3. The relationship between EGTA concentration (0.2 to 10 mM) and the magnitude of LTD was examined. This relationship described a U-shaped curve, as predicted by models of synaptic plasticity. This provides strong evidence that the magnitude of LTD is determined by the magnitude of the increase in intracellular calcium concentration. 4. LFS paired with depolarisation to -10 mV induced LTD, no change or LTP as activity-dependent postsynaptic calcium levels were allowed to increase progressively by the use of progressively lower concentrations of buffer (10 to 0.2 mM EGTA). 5. We investigated if the lack of plasticity that occurs at the transition between LTD and LTP is due to induction of both of these processes with zero net change, or is due to neither LTD nor LTP being induced. These experiments were possible as LTP but not LTD was blocked by the protein kinase inhibitor staurosporine while LTD but not LTP was blocked by the mGlu receptor antagonist MCPG. At the transition between LTD and LTP, blocking LTP mechanisms did not uncover LTD whilst blocking LTD mechanisms did not uncover LTP. This suggests that the transition between LTD and LTP is due to the lack of induction of both of these processes and also suggests that these two processes are induced independently of one another.

Citing Articles

Competitive processes shape multi-synapse plasticity along dendritic segments.

Chater T, Eggl M, Goda Y, Tchumatchenko T Nat Commun. 2024; 15(1):7572.

PMID: 39217140 PMC: 11365941. DOI: 10.1038/s41467-024-51919-0.

Reversible synaptic adaptations in a subpopulation of murine hippocampal neurons following early-life seizures.

Xing B, Barbour A, Vithayathil J, Li X, Dutko S, Fawcett-Patel J J Clin Invest. 2024; 134(5).

PMID: 38227384 PMC: 10904056. DOI: 10.1172/JCI175167.

Dendritic distribution of autophagosomes underlies pathway-selective induction of LTD.

Keary 3rd K, Gu Q, Chen J, Li Z Cell Rep. 2023; 42(8):112898.

PMID: 37516958 PMC: 10528062. DOI: 10.1016/j.celrep.2023.112898.

Asymmetric Voltage Attenuation in Dendrites Can Enable Hierarchical Heterosynaptic Plasticity.

Moldwin T, Kalmenson M, Segev I eNeuro. 2023; 10(7).

PMID: 37414554 PMC: 10354808. DOI: 10.1523/ENEURO.0014-23.2023.

The Therapeutic Potential of Non-Invasive and Invasive Cerebellar Stimulation Techniques in Hereditary Ataxias.

Benussi A, Batsikadze G, Franca C, Cury R, Maas R Cells. 2023; 12(8).

PMID: 37190102 PMC: 10137097. DOI: 10.3390/cells12081193.

References

Hansel C, Artola A, Singer W . Relation between dendritic Ca2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons. Eur J Neurosci. 1998; 9(11):2309-22. DOI: 10.1111/j.1460-9568.1997.tb01648.x. View

Cho K, Kemp N, Noel J, Aggleton J, Brown M, Bashir Z . A new form of long-term depression in the perirhinal cortex. Nat Neurosci. 2000; 3(2):150-6. DOI: 10.1038/72093. View

Bear M, Abraham W . Long-term depression in hippocampus. Annu Rev Neurosci. 1996; 19:437-62. DOI: 10.1146/annurev.ne.19.030196.002253. View

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

Bliss T, Collingridge G . A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993; 361(6407):31-9. DOI: 10.1038/361031a0. View

Malenka R, Nicoll R . Long-term potentiation--a decade of progress?. Science. 1999; 285(5435):1870-4. DOI: 10.1126/science.285.5435.1870. View

Brown M, Xiang J . Recognition memory: neuronal substrates of the judgement of prior occurrence. Prog Neurobiol. 1998; 55(2):149-89. DOI: 10.1016/s0301-0082(98)00002-1. View

Dudek S, Bear M . 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; 89(10):4363-7. PMC: 49082. DOI: 10.1073/pnas.89.10.4363. View

Mulkey R, Malenka R . Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron. 1992; 9(5):967-75. DOI: 10.1016/0896-6273(92)90248-c. View

10.

Artola A, Singer W . Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci. 1993; 16(11):480-7. DOI: 10.1016/0166-2236(93)90081-v. View

11.

Yang S, Tang Y, Zucker R . Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol. 1999; 81(2):781-7. DOI: 10.1152/jn.1999.81.2.781. View

12.

Anderson W, Collingridge G . The LTP Program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. J Neurosci Methods. 2001; 108(1):71-83. DOI: 10.1016/s0165-0270(01)00374-0. View

13.

Gold J, Bear M . A model of dendritic spine Ca2+ concentration exploring possible bases for a sliding synaptic modification threshold. Proc Natl Acad Sci U S A. 1994; 91(9):3941-5. PMC: 43698. DOI: 10.1073/pnas.91.9.3941. View

14.

Strack S, Barban M, Wadzinski B, Colbran R . Differential inactivation of postsynaptic density-associated and soluble Ca2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J Neurochem. 1997; 68(5):2119-28. DOI: 10.1046/j.1471-4159.1997.68052119.x. View

15.

Donella-Deana A, KRINKS M, Ruzzene M, Klee C, Pinna L . Dephosphorylation of phosphopeptides by calcineurin (protein phosphatase 2B). Eur J Biochem. 1994; 219(1-2):109-17. DOI: 10.1111/j.1432-1033.1994.tb19920.x. View

16.

Ziakopoulos Z, TILLETT C, Brown M, Bashir Z . Input-and layer-dependent synaptic plasticity in the rat perirhinal cortex in vitro. Neuroscience. 1999; 92(2):459-72. DOI: 10.1016/s0306-4522(98)00764-7. View

17.

Egger V, Feldmeyer D, Sakmann B . Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat Neurosci. 1999; 2(12):1098-105. DOI: 10.1038/16026. View

18.

Lisman J . A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci U S A. 1989; 86(23):9574-8. PMC: 298540. DOI: 10.1073/pnas.86.23.9574. View

19.

Ngezahayo A, Schachner M, Artola A . Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J Neurosci. 2000; 20(7):2451-8. PMC: 6772243. View

20.

Mulkey R, Endo S, Shenolikar S, Malenka R . Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature. 1994; 369(6480):486-8. DOI: 10.1038/369486a0. View