 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 16, Number 19, Issue of October 1, 1996 pp. 5951-5960
Copyright ©1996 Society for NeuroscienceInduction of Hippocampal Long-Term Depression Requires Release of Ca2+ from Separate Presynaptic and Postsynaptic Intracellular Stores
Received April 1, 1996; revised July 1, 1996; accepted July 8, 1996.
Magali Reyes and Patric K. Stanton Departments of Neuroscience and Neurology, Albert Einstein College of Medicine, Bronx, New York 10461-1602
Studies have suggested that an increase in intracellular [Ca2+] is necessary for the induction of both long-term potentiation (LTP) and long-term depression (LTD) of synaptic transmission, and that release of Ca2+ from intracellular storage pools can be necessary to induce LTP. We investigated whether release of Ca2+ from intracellular stores also is required for the induction of LTD at Schaffer collateral-CA1 synapses in hippocampal slices. Both thapsigargin (1 µM) and cyclopiazonic acid (1 µM), compounds that deplete all intracellular Ca2+ pools by blocking ATP-dependent Ca2+ uptake into intracellular compartments, blocked the induction, but not maintenance, of LTD by low-frequency stimulation (LFS) (1 Hz/15 min) without affecting baseline synaptic transmission. Washout of the reversible inhibitor cyclopiazonic acid restored the ability to induce LTD. In contrast, thapsigargin did not block depotentiation of LTP by 1 Hz LFS, suggesting that LTP causes a reduction in the threshold [Ca2+] necessary for LTD. Selective depletion of the ryanodine receptor-gated Ca2+ pool by bath application of ryanodine (10 µM) also blocked the induction of LTD, indicating a requirement for Ca2+-induced Ca2+ release. Impalement of CA1 pyramidal neurons with microelectrodes containing thapsigargin (500 nM to 200 µM) prevented the induction of LTD at synapses on that neuron without blocking LTD in the rest of the slice. In contrast, similar filling of CA1 pyramidal neurons with ryanodine (2 µM to 5 mM) did not block the induction of LTD. From these data, we conclude that the induction of LTD requires release of Ca2+ both from a presynaptic ryanodine-sensitive pool and from postsynaptic (presumably IP3-gated) stores.
Key words: calcium; CA1; cyclopiazonic acid; hippocampus; inositol triphosphate; learning and memory; long-term depression; ryanodine; synaptic plasticity; thapsigargin
This article has been cited by other articles:
N. Holbro, A. Grunditz, and T. G. Oertner
Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses
PNAS, September 1, 2009; 106(35): 15055 - 15060.
[Abstract] [Full Text] [PDF]
J. E. Geiger and N. S. Magoski
Ca2+-Induced Ca2+ Release in Aplysia Bag Cell Neurons Requires Interaction Between Mitochondrial and Endoplasmic Reticulum Stores
J Neurophysiol, July 1, 2008; 100(1): 24 - 37.
[Abstract] [Full Text] [PDF]
C. P. Bailey, R. E. Nicholls, X.-l. Zhang, Z.-y. Zhou, W. Muller, E. R. Kandel, and P. K. Stanton
G{alpha}i2 inhibition of adenylate cyclase regulates presynaptic activity and unmasks cGMP-dependent long-term depression at Schaffer collateral-CA1 hippocampal synapses
Learn. Mem., April 7, 2008; 15(4): 261 - 270.
[Abstract] [Full Text] [PDF]
S. Kim, H.-M. Yun, J.-H. Baik, K. C. Chung, S.-Y. Nah, and H. Rhim
Functional Interaction of Neuronal Cav1.3 L-type Calcium Channel with Ryanodine Receptor Type 2 in the Rat Hippocampus
J. Biol. Chem., November 9, 2007; 282(45): 32877 - 32889.
[Abstract] [Full Text] [PDF]
C. Supnet, J. Grant, H. Kong, D. Westaway, and M. Mayne
Amyloid-beta-(1-42) Increases Ryanodine Receptor-3 Expression and Function in Neurons of TgCRND8 Mice
J. Biol. Chem., December 15, 2006; 281(50): 38440 - 38447.
[Abstract] [Full Text] [PDF]
S. L. Mironov and N. Symonchuk
ER vesicles and mitochondria move and communicate at synapses
J. Cell Sci., December 1, 2006; 119(23): 4926 - 4934.
[Abstract] [Full Text] [PDF]
X.-l. Zhang, Z.-y. Zhou, J. Winterer, W. Muller, and P. K. Stanton
NMDA-Dependent, But Not Group I Metabotropic Glutamate Receptor-Dependent, Long-Term Depression at Schaffer Collateral-CA1 Synapses Is Associated with Long-Term Reduction of Release from the Rapidly Recycling Presynaptic Vesicle Pool
J. Neurosci., October 4, 2006; 26(40): 10270 - 10280.
[Abstract] [Full Text] [PDF]
F.-M. Lu and R. D. Hawkins
Presynaptic and postsynaptic Ca2+ and CamKII contribute to long-term potentiation at synapses between individual CA3 neurons.
PNAS, March 14, 2006; 103(11): 4264 - 4269.
[Abstract] [Full Text] [PDF]
S. Camandola, R. G. Cutler, D. S. Gary, O. Milhavet, and M. P. Mattson
Suppression of Calcium Release from Inositol 1,4,5-Trisphosphate-sensitive Stores Mediates the Anti-apoptotic Function of Nuclear Factor-{kappa}B
J. Biol. Chem., June 10, 2005; 280(23): 22287 - 22296.
[Abstract] [Full Text] [PDF]
A. Verkhratsky
Physiology and Pathophysiology of the Calcium Store in the Endoplasmic Reticulum of Neurons
Physiol Rev, January 1, 2005; 85(1): 201 - 279.
[Abstract] [Full Text] [PDF]
V. K. Unni, S. S. Zakharenko, L. Zablow, A. J. DeCostanzo, and S. A. Siegelbaum
Calcium Release from Presynaptic Ryanodine-Sensitive Stores Is Required for Long-Term Depression at Hippocampal CA3-CA3 Pyramidal Neuron Synapses
J. Neurosci., October 27, 2004; 24(43): 9612 - 9622.
[Abstract] [Full Text] [PDF]
H. Huang and A. Bordey
Glial Glutamate Transporters Limit Spillover Activation of Presynaptic NMDA Receptors and Influence Synaptic Inhibition of Purkinje Neurons
J. Neurosci., June 23, 2004; 24(25): 5659 - 5669.
[Abstract] [Full Text] [PDF]
A. Kumar and T. C. Foster
Enhanced Long-Term Potentiation During Aging Is Masked by Processes Involving Intracellular Calcium Stores
J Neurophysiol, June 1, 2004; 91(6): 2437 - 2444.
[Abstract] [Full Text] [PDF]
W. Cai, C. Hisatsune, K. Nakamura, T. Nakamura, T. Inoue, and K. Mikoshiba
Activity-dependent Expression of Inositol 1,4,5-Trisphosphate Receptor Type 1 in Hippocampal Neurons
J. Biol. Chem., May 28, 2004; 279(22): 23691 - 23698.
[Abstract] [Full Text] [PDF]
H. Bannai, T. Inoue, T. Nakayama, M. Hattori, and K. Mikoshiba
Kinesin dependent, rapid, bi-directional transport of ER sub-compartment in dendrites of hippocampal neurons
J. Cell Sci., January 15, 2004; 117(2): 163 - 175.
[Abstract] [Full Text] [PDF]
R. D. Groth and P. G. Mermelstein
Brain-Derived Neurotrophic Factor Activation of NFAT (Nuclear Factor of Activated T-Cells)-Dependent Transcription: A Role for the Transcription Factor NFATc4 in Neurotrophin-Mediated Gene Expression
J. Neurosci., September 3, 2003; 23(22): 8125 - 8134.
[Abstract] [Full Text] [PDF]
I. Jin and R. D. Hawkins
Presynaptic and Postsynaptic Mechanisms of a Novel Form of Homosynaptic Potentiation at Aplysia Sensory-Motor Neuron Synapses
J. Neurosci., August 13, 2003; 23(19): 7288 - 7297.
[Abstract] [Full Text] [PDF]
P. K. Stanton, J. Winterer, C. P. Bailey, A. Kyrozis, I. Raginov, G. Laube, R. W. Veh, C. Q. Nguyen, and W. Muller
Long-Term Depression of Presynaptic Release from the Readily Releasable Vesicle Pool Induced by NMDA Receptor-Dependent Retrograde Nitric Oxide
J. Neurosci., July 2, 2003; 23(13): 5936 - 5944.
[Abstract] [Full Text] [PDF]
M. E Larkum, S. Watanabe, T. Nakamura, N. Lasser-Ross, and W. N Ross
Synaptically activated Ca2+ waves in layer 2/3 and layer 5 rat neocortical pyramidal neurons
J. Physiol., June 1, 2003; 549(2): 471 - 488.
[Abstract] [Full Text] [PDF]
M. L Baccei, R. Bardoni, and M. Fitzgerald
Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol
J. Physiol., May 15, 2003; 549(1): 231 - 242.
[Abstract] [Full Text] [PDF]
Y.-F. Lu and R. D. Hawkins
Ryanodine Receptors Contribute to cGMP-Induced Late-Phase LTP and CREB Phosphorylation in the Hippocampus
J Neurophysiol, September 1, 2002; 88(3): 1270 - 1278.
[Abstract] [Full Text] [PDF]
S.-T. Li, K. Kato, K. Tomizawa, M. Matsushita, A. Moriwaki, H. Matsui, and K. Mikoshiba
Calcineurin Plays Different Roles in Group II Metabotropic Glutamate Receptor- and NMDA Receptor-Dependent Long-Term Depression
J. Neurosci., June 15, 2002; 22(12): 5034 - 5041.
[Abstract] [Full Text] [PDF]
A. Araque, E. D. Martin, G. Perea, J. I. Arellano, and W. Buno
Synaptically Released Acetylcholine Evokes Ca2+ Elevations in Astrocytes in Hippocampal Slices
J. Neurosci., April 1, 2002; 22(7): 2443 - 2450.
[Abstract] [Full Text] [PDF]
Y. Liang, L.-L. Yuan, D. Johnston, and R. Gray
Calcium Signaling at Single Mossy Fiber Presynaptic Terminals in the Rat Hippocampus
J Neurophysiol, February 1, 2002; 87(2): 1132 - 1137.
[Abstract] [Full Text] [PDF]
A. G. Carter, K. E. Vogt, K. A. Foster, and W. G. Regehr
Assessing the Role of Calcium-Induced Calcium Release in Short-Term Presynaptic Plasticity at Excitatory Central Synapses
J. Neurosci., January 1, 2002; 22(1): 21 - 28.
[Abstract] [Full Text] [PDF]
W. ZHAO, N. MEIRI, H. XU, S. CAVALLARO, A. QUATTRONE, L. ZHANG, and D. L. ALKON
Spatial learning induced changes in expression of the ryanodine type II receptor in the rat hippocampus
FASEB J, February 1, 2000; 14(2): 290 - 300.
[Abstract] [Full Text]
M. Reyes-Harde, B. V. L. Potter, A. Galione, and P. K. Stanton
Induction of Hippocampal LTD Requires Nitric-Oxide-Stimulated PKG Activity and Ca2+ Release From Cyclic ADP-Ribose-Sensitive Stores
J Neurophysiol, September 1, 1999; 82(3): 1569 - 1576.
[Abstract] [Full Text] [PDF]
L. Santschi, M. Reyes-Harde, and P. K. Stanton
Chemically Induced, Activity-Independent LTD Elicited by Simultaneous Activation of PKG and Inhibition of PKA
J Neurophysiol, September 1, 1999; 82(3): 1577 - 1589.
[Abstract] [Full Text] [PDF]
O. Caillard, Y. Ben-Ari, and J.-L. Gaiarsa
Mechanisms of Induction and Expression of Long-Term Depression at GABAergic Synapses in the Neonatal Rat Hippocampus
J. Neurosci., September 1, 1999; 19(17): 7568 - 7577.
[Abstract] [Full Text] [PDF]
N Kato, T Tanaka, K Yamamoto, and Y Isomura
Distinct temporal profiles of activity-dependent calcium increase in pyramidal neurons of the rat visual cortex
J. Physiol., September 1, 1999; 519(2): 467 - 479.
[Abstract] [Full Text] [PDF]
M. Reyes-Harde, R. Empson, B. V. L. Potter, A. Galione, and P. K. Stanton
Evidence of a role for cyclic ADP-ribose in long-term synaptic depression in hippocampus
PNAS, March 30, 1999; 96(7): 4061 - 4066.
[Abstract] [Full Text] [PDF]
H. Dvorak-Carbone and E. M. Schuman
Long-Term Depression of Temporoammonic-CA1 Hippocampal Synaptic Transmission
J Neurophysiol, March 1, 1999; 81(3): 1036 - 1044.
[Abstract] [Full Text] [PDF]
G. Woodhall, C. E. Gee, R. Robitaille, and J.-C. Lacaille
Membrane Potential and Intracellular Ca2+ Oscillations Activated by mGluRs in Hippocampal Stratum Oriens/Alveus Interneurons
J Neurophysiol, January 1, 1999; 81(1): 371 - 382.
[Abstract] [Full Text] [PDF]
Y.-X. Li, Y. Zhang, H. A. Lester, E. M. Schuman, and N. Davidson
Enhancement of Neurotransmitter Release Induced by Brain-Derived Neurotrophic Factor in Cultured Hippocampal Neurons
J. Neurosci., December 15, 1998; 18(24): 10231 - 10240.
[Abstract] [Full Text] [PDF]
S. Mochida, C. T. Yokoyama, D. K. Kim, K. Itoh, and W. A. Catterall
Evidence for a voltage-dependent enhancement of neurotransmitter release mediated via the synaptic protein interaction site of N-type Ca2+ channels
PNAS, November 24, 1998; 95(24): 14523 - 14528.
[Abstract] [Full Text] [PDF]
K. Narita, T. Akita, M. Osanai, T. Shirasaki, H. Kijima, and K. Kuba
A Ca2+-induced Ca2+ Release Mechanism Involved in Asynchronous Exocytosis at Frog Motor Nerve Terminals
J. Gen. Physiol., November 1, 1998; 112(5): 593 - 609.
[Abstract] [Full Text] [PDF]
C. Dettbarn and P. Palade
Effects of Three Sarcoplasmic/Endoplasmic Reticulum Ca++ Pump Inhibitors on Release Channels of Intracellular Stores
J. Pharmacol. Exp. Ther., May 1, 1998; 285(2): 739 - 745.
[Abstract] [Full Text]
D. Wang and L. Maler
In Vitro Plasticity of the Direct Feedback Pathway in the Electrosensory System of Apteronotus leptorhynchus
J Neurophysiol, October 1, 1997; 78(4): 1882 - 1889.
[Abstract] [Full Text] [PDF]
G. C. Carlson, M. L. Slawecki, E. Lancaster, and A. Keller
Distribution and Activation of Intracellular Ca2+ Stores in Cultured Olfactory Bulb Neurons
J Neurophysiol, October 1, 1997; 78(4): 2176 - 2185.
[Abstract] [Full Text] [PDF]
Y. M. Usachev and S. A. Thayer
All-or-None Ca2+ Release from Intracellular Stores Triggered by Ca2+ Influx through Voltage-Gated Ca2+ Channels in Rat Sensory Neurons
J. Neurosci., October 1, 1997; 17(19): 7404 - 7414.
[Abstract] [Full Text] [PDF]
R. M. Empson and A. Galione
Cyclic ADP-ribose Enhances Coupling between Voltage-gated Ca2+ Entry and Intracellular Ca2+ Release
J. Biol. Chem., August 22, 1997; 272(34): 20967 - 20970.
[Abstract] [Full Text] [PDF]
H. Katsuki, Y. Izumi, and C. F. Zorumski
Noradrenergic Regulation of Synaptic Plasticity in the Hippocampal CA1 Region
J Neurophysiol, June 1, 1997; 77(6): 3013 - 3020.
[Abstract] [Full Text] [PDF]
D. Manahan-Vaughan
Group 1 and 2 Metabotropic Glutamate Receptors Play Differential Roles in Hippocampal Long-Term Depression and Long-Term Potentiation in Freely Moving Rats
J. Neurosci., May 1, 1997; 17(9): 3303 - 3311.
[Abstract] [Full Text] [PDF]
G. M. J. Ramakers, K. Heinen, W.-H. Gispen, and P. N. E. de Graan
Long Term Depression in the CA1 Field Is Associated with a Transient Decrease in Pre- and Postsynaptic PKC Substrate Phosphorylation
J. Biol. Chem., September 8, 2000; 275(37): 28682 - 28687.
[Abstract] [Full Text] [PDF]
G. W. Glazner, S. Camandola, J. D. Geiger, and M. P. Mattson
Endoplasmic Reticulum D-myo-Inositol 1,4,5-Trisphosphate-sensitive Stores Regulate Nuclear Factor-kappa B Binding Activity in a Calcium-independent Manner
J. Biol. Chem., June 15, 2001; 276(25): 22461 - 22467.
[Abstract] [Full Text] [PDF]
O. Caillard, Y. Ben-Ari, and J.-L. Gaiarsa
Activation of Presynaptic and Postsynaptic Ryanodine-Sensitive Calcium Stores Is Required for the Induction of Long-Term Depression at GABAergic Synapses in the Neonatal Rat Hippocampus Amphetamine
J. Neurosci., September 1, 2000; 20(17): RC94 - RC94.
[Abstract] [Full Text] [PDF]
P. K. Stanton, U. Heinemann, and W. Muller
FM1-43 Imaging Reveals cGMP-Dependent Long-Term Depression of Presynaptic Transmitter Release
J. Neurosci., October 1, 2001; 21(19): RC167 - RC167.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|