Abstract
Mossy fiber activity can evoke Ca2+ release from internal stores in CA3 neurons, but the physiological conditions under which this occurs and the mechanisms underlying the release are not understood. Using rat hippocampal slices we report here that short trains of mossy fiber stimulation activate group I metabotropic glutamate receptors (mGluRs) on CA3 pyramidal neurons and elicit waves of Ca2+ release from inositol 1,4,5-trisphosphate (IP3) sensitive internal stores that propagate from stratum lucidum to the soma and in some cases distally out the dendrites. Activation of mGluR1,5 receptors by an agonist trans-azetidine-2,4-dicarboxylic acid (tADA) applied to stratum lucidum was also sufficient to induce waves of Ca2+ release. This release was blocked by internal heparin, but not by dantrolene, suggesting the involvement of IP3 rather than ryanodine receptors in not only the initial release but also in the maintenance of the propagating waves. Release could be facilitated by Ca2+ influx through voltage-gated Ca2+ channels, which is consistent with the known Ca2+ sensitivity of IP3 receptors.These results provide insight into the mechanisms and conditions of Ca2+ release in CA3 neurons and demonstrate the powerful influence mossy fiber input can have on these neurons.
MeSH Terms
Action Potentials/drug effects,physiology
Animals
Calcium/metabolism
Calcium Channels/drug effects,metabolism
Calcium Signaling/drug effects,physiology
Dantrolene/pharmacology
Dendrites/drug effects,metabolism,ultrastructure
Electric Stimulation
Excitatory Amino Acid Agonists/pharmacology
Excitatory Amino Acid Antagonists/pharmacology
Heparin/pharmacology
Inositol 1,4,5-Trisphosphate Receptors
Intracellular Fluid/drug effects,metabolism
Mossy Fibers, Hippocampal/drug effects,metabolism,ultrastructure
Muscle Relaxants, Central/pharmacology
Narcotic Antagonists/pharmacology
Neuronal Plasticity/drug effects,physiology
Pyramidal Cells/drug effects,physiology
Rats
Rats, Sprague-Dawley
Reaction Time/drug effects,physiology
Receptors, Cytoplasmic and Nuclear/antagonists & inhibitors,metabolism
Receptors, Metabotropic Glutamate/drug effects,metabolism
Ryanodine Receptor Calcium Release Channel/drug effects,metabolism
Synaptic Transmission/physiology
Chemicals
Calcium Channels
Excitatory Amino Acid Agonists
Excitatory Amino Acid Antagonists
Inositol 1,4,5-Trisphosphate Receptors
Muscle Relaxants, Central
Narcotic Antagonists
Receptors, Cytoplasmic and Nuclear
Receptors, Metabotropic Glutamate
Ryanodine Receptor Calcium Release Channel
Heparin
Dantrolene
Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kapur A
Division of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
Yeckel M
Johnston D
References (34)
34 references, click to expand
-
Dynamics of dendritic calcium transients evoked by quantal release at excitatory hippocampal synapses.
Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):901-6
PMID: 10639177
-
Comparison of two forms of long-term potentiation in single hippocampal neurons.
Science. 1990 Jun 29;248(4963):1619-24
PMID: 2114039
-
Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons.
J Neurophysiol. 1990 Jul;64(1):91-104
PMID: 1696962
-
Long-term potentiation of hippocampal mossy fiber synapses is blocked by postsynaptic injection of calcium chelators.
Neuron. 1989 Nov;3(5):583-8
PMID: 2577129
-
Induction of long-term potentiation at hippocampal mossy-fiber synapses follows a Hebbian rule.
J Neurophysiol. 1990 Sep;64(3):948-60
PMID: 2230936
-
Stimulation of endogenous opioid release displaces mu receptor binding in rat hippocampus.
Neuroscience. 1990;37(1):45-53
PMID: 1978741
-
Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release.
Science. 1991 Apr 19;252(5004):443-6
PMID: 2017683
-
Endogenous opioids released from perforant path modulate norepinephrine actions and inhibitory postsynaptic potentials in guinea pig CA3 pyramidal cells.
J Pharmacol Exp Ther. 1991 Jul 1;258(1):18-26
PMID: 2072294
-
Roles of glutamate receptors in long-term potentiation at hippocampal mossy fiber synapses.
Neuroreport. 1991 Jun;2(6):333-6
PMID: 1680482
-
The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons.
Nature. 1992 May 21;357(6375):244-6
PMID: 1350327
-
Evidence for multiple types of Ca2+ channels in acutely isolated hippocampal CA3 neurones of the guinea-pig.
J Physiol. 1991 Feb;433:259-81
PMID: 1668752
-
Inositol trisphosphate and calcium signalling.
Nature. 1993 Jan 28;361(6410):315-25
PMID: 8381210
-
Differential localization of phosphoinositide-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain.
J Neurosci. 1993 May;13(5):2001-12
PMID: 8386753
-
Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain.
J Neurosci. 1993 Jul;13(7):3051-63
PMID: 8392539
-
The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation.
Neuron. 1994 Feb;12(2):261-9
PMID: 8110457
-
The pharmacology of intracellular Ca(2+)-release channels.
Trends Pharmacol Sci. 1994 May;15(5):145-9
PMID: 7754532
-
Posttetanic potentiation and presynaptically induced long-term potentiation at the mossy fiber synapse in rat hippocampus.
J Neurobiol. 1995 Mar;26(3):370-85
PMID: 7775970
-
Neuronal Ca2+ stores: activation and function.
Trends Neurosci. 1995 Jul;18(7):299-306
PMID: 7571010
-
Role of calcium channel subtypes in calcium transients in hippocampal CA3 neurons.
J Neurosci. 1995 Oct;15(10):6433-44
PMID: 7472406
-
G protein-coupled receptors mediate a fast excitatory postsynaptic current in CA3 pyramidal neurons in hippocampal slices.
J Neurosci. 1995 Dec;15(12):8320-30
PMID: 8613765
-
Induction of hebbian and non-hebbian mossy fiber long-term potentiation by distinct patterns of high-frequency stimulation.
J Neurosci. 1996 Jul 1;16(13):4293-9
PMID: 8753890
-
Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus.
Eur J Neurosci. 1996 Jul;8(7):1488-500
PMID: 8758956
-
Multiple channel types contribute to the low-voltage-activated calcium current in hippocampal CA3 pyramidal neurons.
J Neurosci. 1996 Sep 15;16(18):5567-82
PMID: 8795613
-
Ca2+ release from intracellular stores induced by afferent stimulation of CA3 pyramidal neurons in hippocampal slices.
J Neurophysiol. 1996 Jul;76(1):554-62
PMID: 8836243
-
Metabotropic glutamate receptors coupled to IP3 production mediate inhibition of IAHP in rat dentate granule neurons.
J Neurophysiol. 1996 Oct;76(4):2691-700
PMID: 8899638
-
Calcium dynamics in thorny excrescences of CA3 pyramidal neurons.
J Neurophysiol. 1997 Jul;78(1):10-8
PMID: 9242255
-
Inositol 1,4,5-trisphosphate (InsP3) and calcium interact to increase the dynamic range of InsP3 receptor-dependent calcium signaling.
J Gen Physiol. 1997 Nov;110(5):529-38
PMID: 9348325
-
L-Type calcium channels are required for one form of hippocampal mossy fiber LTP.
J Neurophysiol. 1998 Apr;79(4):2181-90
PMID: 9535977
-
Neuronal calcium signaling.
Neuron. 1998 Jul;21(1):13-26
PMID: 9697848
-
Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites.
Nature. 1998 Dec 24-31;396(6713):753-6
PMID: 9874372
-
A new class of synaptic response involving calcium release in dendritic spines.
Nature. 1998 Dec 24-31;396(6713):757-60
PMID: 9874373
-
Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism.
Nat Neurosci. 1999 Jul;2(7):625-33
PMID: 10404192
-
G-protein-independent signaling mediated by metabotropic glutamate receptors.
Nat Neurosci. 1999 Dec;2(12):1070-7
PMID: 10570483
-
Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials.
Neuron. 1999 Nov;24(3):727-37
PMID: 10595522