Received March 15, 2002
Accepted after revision June 25, 2002

Spatial segregation and interaction of calcium signalling mechanisms in rat hippocampal CA1 pyramidal neurons

¹ Department of Physiology, New York Medical College, Valhalla, NY 10595, USA
² Department of Physiology, New York Medical College, Valhalla, NY 10595, USA. Email: ross@nymc.edu

^* To whom correspondence should be addressed.

Postsynaptic [Ca²⁺]_i increases result from Ca²⁺ entry through ligand-gated channels, entry through voltage-gated channels, or release from intracellular stores. We found that these sources have distinct spatial distributions in hippocampal CA1 pyramidal neurons. Large amplitude regenerative release of Ca²⁺ from IP₃-sensitive stores in the form of Ca²⁺ waves were found almost exclusively on the thick apical shaft. Smaller release events did not extend more than 15 µm into the oblique dendrites. These synaptically activated regenerative waves initiated at points where the stimulated oblique dendrites branch from the apical shaft. In contrast, NMDA receptor-mediated increases were observed predominantly in oblique dendrites where spines are found at high density. These [Ca²⁺]_i increases were typically more than eight times larger than [Ca²⁺]_i from this source on the main aspiny apical shaft. Ca²⁺ entry through voltage-gated channels, activated by backpropagating action potentials, was detected at all dendritic locations. These mechanisms were not independent. Ca²⁺ entry through NMDA receptor channels or voltage-gated channels (as previously demonstrated) synergistically enhanced Ca²⁺ release generated by mGluR mobilization of IP₃.

This article has been cited by other articles:

				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]

				P. J. Sjostrom, E. A. Rancz, A. Roth, and M. Hausser Dendritic Excitability and Synaptic Plasticity Physiol Rev, April 1, 2008; 88(2): 769 - 840. [Abstract] [Full Text] [PDF]

				C. R. Raymond Different requirements for action potentials in the induction of different forms of long-term potentiation J. Physiol., April 1, 2008; 586(7): 1859 - 1865. [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]

				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]

				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]

				M. Canepari, M. Djurisic, and D. Zecevic Dendritic signals from rat hippocampal CA1 pyramidal neurons during coincident pre- and post-synaptic activity: a combined voltage- and calcium-imaging study J. Physiol., April 15, 2007; 580(2): 463 - 484. [Abstract] [Full Text] [PDF]

				N. Fedirko, M. Avshalumov, M. E. Rice, and M. Chesler Regulation of Postsynaptic Ca2+ Influx in Hippocampal CA1 Pyramidal Neurons via Extracellular Carbonic Anhydrase J. Neurosci., January 31, 2007; 27(5): 1167 - 1175. [Abstract] [Full Text] [PDF]

				C. L. Jasoni, M. G. Todman, M. M. Strumia, and A. E. Herbison Cell Type-Specific Expression of a Genetically Encoded Calcium Indicator Reveals Intrinsic Calcium Oscillations in Adult Gonadotropin-Releasing Hormone Neurons J. Neurosci., January 24, 2007; 27(4): 860 - 867. [Abstract] [Full Text] [PDF]

				D. Billups, B. Billups, R. A. J. Challiss, and S. R. Nahorski Modulation of Gq-Protein-Coupled Inositol Trisphosphate and Ca2+ Signaling by the Membrane Potential J. Neurosci., September 27, 2006; 26(39): 9983 - 9995. [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]

				A. B. Taylor and J. R. Fallon Dendrites Contain a Spacing Pattern J. Neurosci., January 25, 2006; 26(4): 1154 - 1163. [Abstract] [Full Text] [PDF]

				C. R. Raymond and S. J. Redman Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus J. Physiol., January 1, 2006; 570(1): 97 - 111. [Abstract] [Full Text] [PDF]

				M. Migliore, M. Ferrante, and G. A. Ascoli Signal Propagation in Oblique Dendrites of CA1 Pyramidal Cells J Neurophysiol, December 1, 2005; 94(6): 4145 - 4155. [Abstract] [Full Text] [PDF]

				T. Heinbockel, D. H. Brager, C. G. Reich, J. Zhao, S. Muralidharan, B. E. Alger, and J. P. Y. Kao Endocannabinoid Signaling Dynamics Probed with Optical Tools J. Neurosci., October 12, 2005; 25(41): 9449 - 9459. [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]

				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]

				N. Sakai, H. Tsubokawa, M. Matsuzaki, T. Kajimoto, E. Takahashi, Y. Ren, S. Ohmori, Y. Shirai, H. Matsubayashi, J. Chen, et al. Propagation of {gamma}PKC translocation along the dendrites of Purkinje cell in {gamma}PKC-GFP transgenic mice Genes Cells, October 1, 2004; 9(10): 945 - 957. [Abstract] [Full Text] [PDF]

				G. Viana Di Prisco and S. Alford Quantitative Investigation of Calcium Signals for Locomotor Pattern Generation in the Lamprey Spinal Cord J Neurophysiol, September 1, 2004; 92(3): 1796 - 1806. [Abstract] [Full Text] [PDF]

				K. A. Kohlmeier, T. Inoue, and C. S. Leonard Hypocretin/Orexin Peptide Signaling in the Ascending Arousal System: Elevation of Intracellular Calcium in the Mouse Dorsal Raphe and Laterodorsal Tegmentum J Neurophysiol, July 1, 2004; 92(1): 221 - 235. [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]

				J. Connor, L. D. Pozzo-Miller, and B. Ross Synaptically driven Ca2+ release in hippocampal neurons J Neurophysiol, November 1, 2003; 90(5): 3579 - 3579. [Full Text] [PDF]

				A. Frick, J. Magee, H. J. Koester, M. Migliore, and D. Johnston Normalization of Ca2+ Signals by Small Oblique Dendrites of CA1 Pyramidal Neurons J. Neurosci., April 15, 2003; 23(8): 3243 - 3250. [Abstract] [Full Text] [PDF]

				G. E. Stutzmann, F. M. LaFerla, and I. Parker Ca2+ Signaling in Mouse Cortical Neurons Studied by Two-Photon Imaging and Photoreleased Inositol Triphosphate J. Neurosci., February 1, 2003; 23(3): 758 - 765. [Abstract] [Full Text] [PDF]