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Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2

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Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2. / Lee, Sang Hun; Lutz, David; Drexler, Dagmar; Frotscher, Michael; Shen, Jie.

In: PLOS ONE, Vol. 15, No. 10, e0240610, 13.10.2020.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Lee, SH, Lutz, D, Drexler, D, Frotscher, M & Shen, J 2020, 'Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2', PLOS ONE, vol. 15, no. 10, e0240610. https://doi.org/10.1371/journal.pone.0240610

APA

Lee, S. H., Lutz, D., Drexler, D., Frotscher, M., & Shen, J. (2020). Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2. PLOS ONE, 15(10), [e0240610]. https://doi.org/10.1371/journal.pone.0240610

Vancouver

Lee SH, Lutz D, Drexler D, Frotscher M, Shen J. Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2. PLOS ONE. 2020 Oct 13;15(10). e0240610. https://doi.org/10.1371/journal.pone.0240610

Bibtex

@article{24956a5219eb4efab8a64de76d2bc253,
title = "Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2",
abstract = "Presynaptic mitochondrial Ca2+ plays a critical role in the regulation of synaptic transmission and plasticity. The presynaptic bouton of the hippocampal mossy fiber (MF) is much larger in size than that of the Schaffer collateral (SC) synapse. Here we compare the structural and physiological characteristics of MF and SC presynaptic boutons to reveal functional and mechanistic differences between these two synapses. Our quantitative ultrastructural analysis using electron microscopy show many more mitochondria in MF presynaptic bouton cross-section profiles compared to SC boutons. Consistent with these results, post-tetanic potentiation (PTP), a form of presynaptic short-term plasticity dependent on mitochondrial Ca2+, is reduced by inhibition of mitochondrial Ca2+ release at MF synapses but not at SC synapses. However, blockade of mitochondrial Ca2+ release results in reduction of PTP at SC synapses by disynaptic MF stimulation. Furthermore, inhibition of mitochondrial Ca2+ release selectively decreases frequency facilitation evoked by short trains of presynaptic stimulation at MF synapses, while having no effect at SC synapses. Moreover, depletion of ER Ca2+ stores leads to reduction of PTP at MF synapses, but PTP is unaffected by ER Ca2+ depletion at SC synapses. These findings show that MF and SC synapses differ in presynaptic mitochondrial content as well as mitochondrial Ca2+ dependent synaptic plasticity, highlighting differential regulatory mechanisms of presynaptic plasticity at MF and SC synapses.",
keywords = "Animals, Calcium/metabolism, Calcium Signaling/drug effects, Excitatory Postsynaptic Potentials/drug effects, Hippocampus/cytology, Male, Mice, Microscopy, Electron, Mitochondria/drug effects, Mossy Fibers, Hippocampal/drug effects, Neuronal Plasticity/drug effects, Onium Compounds/pharmacology, Organophosphorus Compounds/pharmacology, Patch-Clamp Techniques, Thiazepines/pharmacology",
author = "Lee, {Sang Hun} and David Lutz and Dagmar Drexler and Michael Frotscher and Jie Shen",
year = "2020",
month = oct,
day = "13",
doi = "10.1371/journal.pone.0240610",
language = "English",
volume = "15",
journal = "PLOS ONE",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "10",

}

RIS

TY - JOUR

T1 - Differential modulation of short-term plasticity at hippocampal mossy fiber and Schaffer collateral synapses by mitochondrial Ca2

AU - Lee, Sang Hun

AU - Lutz, David

AU - Drexler, Dagmar

AU - Frotscher, Michael

AU - Shen, Jie

PY - 2020/10/13

Y1 - 2020/10/13

N2 - Presynaptic mitochondrial Ca2+ plays a critical role in the regulation of synaptic transmission and plasticity. The presynaptic bouton of the hippocampal mossy fiber (MF) is much larger in size than that of the Schaffer collateral (SC) synapse. Here we compare the structural and physiological characteristics of MF and SC presynaptic boutons to reveal functional and mechanistic differences between these two synapses. Our quantitative ultrastructural analysis using electron microscopy show many more mitochondria in MF presynaptic bouton cross-section profiles compared to SC boutons. Consistent with these results, post-tetanic potentiation (PTP), a form of presynaptic short-term plasticity dependent on mitochondrial Ca2+, is reduced by inhibition of mitochondrial Ca2+ release at MF synapses but not at SC synapses. However, blockade of mitochondrial Ca2+ release results in reduction of PTP at SC synapses by disynaptic MF stimulation. Furthermore, inhibition of mitochondrial Ca2+ release selectively decreases frequency facilitation evoked by short trains of presynaptic stimulation at MF synapses, while having no effect at SC synapses. Moreover, depletion of ER Ca2+ stores leads to reduction of PTP at MF synapses, but PTP is unaffected by ER Ca2+ depletion at SC synapses. These findings show that MF and SC synapses differ in presynaptic mitochondrial content as well as mitochondrial Ca2+ dependent synaptic plasticity, highlighting differential regulatory mechanisms of presynaptic plasticity at MF and SC synapses.

AB - Presynaptic mitochondrial Ca2+ plays a critical role in the regulation of synaptic transmission and plasticity. The presynaptic bouton of the hippocampal mossy fiber (MF) is much larger in size than that of the Schaffer collateral (SC) synapse. Here we compare the structural and physiological characteristics of MF and SC presynaptic boutons to reveal functional and mechanistic differences between these two synapses. Our quantitative ultrastructural analysis using electron microscopy show many more mitochondria in MF presynaptic bouton cross-section profiles compared to SC boutons. Consistent with these results, post-tetanic potentiation (PTP), a form of presynaptic short-term plasticity dependent on mitochondrial Ca2+, is reduced by inhibition of mitochondrial Ca2+ release at MF synapses but not at SC synapses. However, blockade of mitochondrial Ca2+ release results in reduction of PTP at SC synapses by disynaptic MF stimulation. Furthermore, inhibition of mitochondrial Ca2+ release selectively decreases frequency facilitation evoked by short trains of presynaptic stimulation at MF synapses, while having no effect at SC synapses. Moreover, depletion of ER Ca2+ stores leads to reduction of PTP at MF synapses, but PTP is unaffected by ER Ca2+ depletion at SC synapses. These findings show that MF and SC synapses differ in presynaptic mitochondrial content as well as mitochondrial Ca2+ dependent synaptic plasticity, highlighting differential regulatory mechanisms of presynaptic plasticity at MF and SC synapses.

KW - Animals

KW - Calcium/metabolism

KW - Calcium Signaling/drug effects

KW - Excitatory Postsynaptic Potentials/drug effects

KW - Hippocampus/cytology

KW - Male

KW - Mice

KW - Microscopy, Electron

KW - Mitochondria/drug effects

KW - Mossy Fibers, Hippocampal/drug effects

KW - Neuronal Plasticity/drug effects

KW - Onium Compounds/pharmacology

KW - Organophosphorus Compounds/pharmacology

KW - Patch-Clamp Techniques

KW - Thiazepines/pharmacology

U2 - 10.1371/journal.pone.0240610

DO - 10.1371/journal.pone.0240610

M3 - SCORING: Journal article

C2 - 33049001

VL - 15

JO - PLOS ONE

JF - PLOS ONE

SN - 1932-6203

IS - 10

M1 - e0240610

ER -