 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, May 1, 2002, 22(9):3454-3462
Nuclear Calcium Signaling Evoked by Cholinergic Stimulation in Hippocampal CA1 Pyramidal Neurons
John M. Power and Pankaj Sah Division of Neuroscience, John Curtin School for Medical Research, Australian National University, Canberra, ACT 0200, Australia
The cholinergic system is thought to play an important role in hippocampal-dependent learning and memory. However, the mechanism of action of the cholinergic system in these actions in not well understood. Here we examined the effect of muscarinic receptor stimulation in hippocampal CA1 pyramidal neurons using whole-cell recordings in acute brain slices coupled with high-speed imaging of intracellular calcium. Activation of muscarinic acetylcholine receptors by synaptic stimulation of cholinergic afferents or application of muscarinic agonist in CA1 pyramidal neurons evoked a focal rise in free calcium in the apical dendrite that propagated as a wave into the soma and invaded the nucleus. The calcium rise to a single action potential was reduced during muscarinic stimulation. Conversely, the calcium rise during trains of action potentials was enhanced during muscarinic stimulation. The enhancement of free intracellular calcium was most pronounced in the soma and nuclear regions. In many cases, the calcium rise was distinguished by a clear inflection in the rising phase of the calcium transient, indicative of a regenerative response. Both calcium waves and the amplification of action potential-induced calcium transients were blocked the emptying of intracellular calcium stores or by antagonism of inositol 1,4,5-trisphosphate receptors with heparin or caffeine. Ryanodine receptors were not essential for the calcium waves or enhancement of calcium responses. Because rises in nuclear calcium are known to initiate the transcription of novel genes, we suggest that these actions of cholinergic stimulation may underlie its effects on learning and memory.
Key words: gene; learning; memory; nucleus; IP3; acetylcholine; ryanodine
Copyright © 2002 Society for Neuroscience 0270-6474/02/2293454-09$05.00/0
This article has been cited by other articles:
J. S. Fitzpatrick, A. M. Hagenston, D. N. Hertle, K. E. Gipson, L. Bertetto-D'Angelo, and M. F. Yeckel
Inositol-1,4,5-trisphosphate receptor-mediated Ca2+ waves in pyramidal neuron dendrites propagate through hot spots and cold spots
J. Physiol., April 1, 2009; 587(7): 1439 - 1459.
[Abstract] [Full Text] [PDF]
K.-H. Cho, H.-J. Jang, E.-H. Lee, S. H. Yoon, S. J. Hahn, Y.-H. Jo, M.-S. Kim, and D.-J. Rhie
Differential Cholinergic Modulation of Ca2+ Transients Evoked by Backpropagating Action Potentials in Apical and Basal Dendrites of Cortical Pyramidal Neurons
J Neurophysiol, June 1, 2008; 99(6): 2833 - 2843.
[Abstract] [Full Text] [PDF]
V. Kumar, Y.-J. I. Jong, and K. L. O'Malley
Activated Nuclear Metabotropic Glutamate Receptor mGlu5 Couples to Nuclear Gq/11 Proteins to Generate Inositol 1,4,5-Trisphosphate-mediated Nuclear Ca2+ Release
J. Biol. Chem., May 16, 2008; 283(20): 14072 - 14083.
[Abstract] [Full Text] [PDF]
B. Lendvai and E. S. Vizi
Nonsynaptic Chemical Transmission Through Nicotinic Acetylcholine Receptors
Physiol Rev, April 1, 2008; 88(2): 333 - 349.
[Abstract] [Full Text] [PDF]
J. M. Power and P. Sah
Competition between Calcium-Activated K+ Channels Determines Cholinergic Action on Firing Properties of Basolateral Amygdala Projection Neurons
J. Neurosci., March 19, 2008; 28(12): 3209 - 3220.
[Abstract] [Full Text] [PDF]
D. F. de Sevilla, A. Nunez, M. Borde, R. Malinow, and W. Buno
Cholinergic-Mediated IP3-Receptor Activation Induces Long-Lasting Synaptic Enhancement in CA1 Pyramidal Neurons
J. Neurosci., February 6, 2008; 28(6): 1469 - 1478.
[Abstract] [Full Text] [PDF]
M. E. Larkum, S. Watanabe, N. Lasser-Ross, P. Rhodes, and W. N. Ross
Dendritic Properties of Turtle Pyramidal Neurons
J Neurophysiol, February 1, 2008; 99(2): 683 - 694.
[Abstract] [Full Text] [PDF]
Myoung Kyu Park, Yu Mi Choi, Yun Kyung Kang, and O. H. Petersen
The Endoplasmic Reticulum as an Integrator of Multiple Dendritic Events
Neuroscientist, February 1, 2008; 14(1): 68 - 77.
[Abstract] [PDF]
A. M. Hagenston, J. S. Fitzpatrick, and M. F. Yeckel
MGluR-Mediated Calcium Waves that Invade the Soma Regulate Firing in Layer V Medial Prefrontal Cortical Pyramidal Neurons
Cereb Cortex, February 1, 2008; 18(2): 407 - 423.
[Abstract] [Full Text] [PDF]
M. Hong and W. N. Ross
Priming of intracellular calcium stores in rat CA1 pyramidal neurons
J. Physiol., October 1, 2007; 584(1): 75 - 87.
[Abstract] [Full Text] [PDF]
J. M. Power and P. Sah
Distribution of IP3-mediated calcium responses and their role in nuclear signalling in rat basolateral amygdala neurons
J. Physiol., May 1, 2007; 580(3): 835 - 857.
[Abstract] [Full Text] [PDF]
G. Cui, B. E. Bernier, M. T. Harnett, and H. Morikawa
Differential Regulation of Action Potential- and Metabotropic Glutamate Receptor-Induced Ca2+ Signals by Inositol 1,4,5-Trisphosphate in Dopaminergic Neurons
J. Neurosci., April 25, 2007; 27(17): 4776 - 4785.
[Abstract] [Full Text] [PDF]
M. Kubota, T. Kasahara, T. Nakamura, M. Ishiwata, T. Miyauchi, and T. Kato
Abnormal Ca2+ Dynamics in Transgenic Mice with Neuron-Specific Mitochondrial DNA Defects.
J. Neurosci., November 22, 2006; 26(47): 12314 - 12324.
[Abstract] [Full Text] [PDF]
S. Watanabe, M. Hong, N. Lasser-Ross, and W. N. Ross
Modulation of calcium wave propagation in the dendrites and to the soma of rat hippocampal pyramidal neurons
J. Physiol., September 1, 2006; 575(2): 455 - 468.
[Abstract] [Full Text] [PDF]
S. M Marchenko, V. V Yarotskyy, T. N Kovalenko, P. G Kostyuk, and R. C Thomas
Spontaneously active and InsP3-activated ion channels in cell nuclei from rat cerebellar Purkinje and granule neurones
J. Physiol., June 15, 2005; 565(3): 897 - 910.
[Abstract] [Full Text] [PDF]
J. M. Power and P. Sah
Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials
J. Physiol., January 15, 2005; 562(2): 439 - 453.
[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]
S. R. Cobb and C. H. Davies
Cholinergic modulation of hippocampal cells and circuits
J. Physiol., January 1, 2005; 562(1): 81 - 88.
[Abstract] [Full Text] [PDF]
M. S. Nash, J. M. Willets, B. Billups, R. A. John Challiss, and S. R. Nahorski
Synaptic Activity Augments Muscarinic Acetylcholine Receptor-stimulated Inositol 1,4,5-Trisphosphate Production to Facilitate Ca2+ Release in Hippocampal Neurons
J. Biol. Chem., November 19, 2004; 279(47): 49036 - 49044.
[Abstract] [Full Text] [PDF]
S.-I. Yamada, H. Takechi, I. Kanchiku, T. Kita, and N. Kato
Small-Conductance Ca2+-Dependent K+ Channels Are the Target of Spike-Induced Ca2+ Release in a Feedback Regulation of Pyramidal Cell Excitability
J Neurophysiol, May 1, 2004; 91(5): 2322 - 2329.
[Abstract] [Full Text] [PDF]
J. M. Willets, M. S. Nash, R. A. J. Challiss, and S. R. Nahorski
Imaging of Muscarinic Acetylcholine Receptor Signaling in Hippocampal Neurons: Evidence for Phosphorylation-Dependent and -Independent Regulation by G-Protein-Coupled Receptor Kinases
J. Neurosci., April 28, 2004; 24(17): 4157 - 4162.
[Abstract] [Full Text] [PDF]
M. B. Parent and M. G. Baxter
Septohippocampal Acetylcholine: Involved in but not Necessary for Learning and Memory?
Learn. Mem., January 1, 2004; 11(1): 9 - 20.
[Abstract] [Full Text] [PDF]
O. Kann, R. Kovacs, and U. Heinemann
Metabotropic Receptor-Mediated Ca2+ Signaling Elevates Mitochondrial Ca2+ and Stimulates Oxidative Metabolism in Hippocampal Slice Cultures
J Neurophysiol, August 1, 2003; 90(2): 613 - 621.
[Abstract] [Full Text] [PDF]
K. L. O'Malley, Y.-J. I. Jong, Y. Gonchar, A. Burkhalter, and C. Romano
Activation of Metabotropic Glutamate Receptor mGlu5 on Nuclear Membranes Mediates Intranuclear Ca2+ Changes in Heterologous Cell Types and Neurons
J. Biol. Chem., July 18, 2003; 278(30): 28210 - 28219.
[Abstract] [Full Text] [PDF]
T. F. FREUND, I. KATONA, and D. PIOMELLI
Role of Endogenous Cannabinoids in Synaptic Signaling
Physiol Rev, July 1, 2003; 83(3): 1017 - 1066.
[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]
H. Morikawa, K. Khodakhah, and J. T. Williams
Two Intracellular Pathways Mediate Metabotropic Glutamate Receptor-Induced Ca2+ Mobilization in Dopamine Neurons
J. Neurosci., January 1, 2003; 23(1): 149 - 157.
[Abstract] [Full Text] [PDF]
T. G Oertner and K. Svoboda
Subliminal messages in hippocampal pyramidal cells
J. Physiol., September 1, 2002; 543(2): 397 - 397.
[Full Text] [PDF]
|
|
|
|
 |
|