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The Journal of Neuroscience, December 15, 2002, 22(24):10653-10661

Correlated Calcium Uptake and Release by Mitochondria and Endoplasmic Reticulum of CA3 Hippocampal Dendrites after Afferent Synaptic Stimulation

Natalia B. Pivovarova^{1, *}, Lucas D. Pozzo-Miller^{2, 3, *}, Jarin Hongpaisan¹, and S. Brian Andrews^{1, 3}

¹ Laboratory of Neurobiology, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892-4062, ² Department of Neurobiology and Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama 35294-0021, and ³ The Marine Biological Laboratory, Woods Hole, Massachusetts 02543

Mitochondria and endoplasmic reticulum (ER) are important modulators of intracellular calcium signaling pathways, but the role of these organelles in shaping synaptic calcium transients in dendrites of pyramidal neurons remains speculative. We have measured directly the concentrations of total Ca (bound plus free) within intracellular compartments of proximal dendrites of CA3 hippocampal neurons at times after synaptic stimulation corresponding to the peak of the cytoplasmic free Ca²⁺ transient (1 sec), to just after its decay (30 sec), and to well after its return to prestimulus levels (180 sec). Electron probe microanalysis of cryosections from rapidly frozen slice cultures has revealed that afferent mossy fiber stimulation evokes large, rapid elevations in the concentration of total mitochondrial Ca ([Ca]_mito) in depolarized dendrites. A single tetanus (50 Hz/1 sec) elevated [Ca]_mito more than fivefold above characteristically low basal levels within 1 sec of stimulation and >10-fold by 30 sec after stimulation. This strong Ca accumulation was reversible, because [Ca]_mito had recovered by 180 sec after the tetanus. Ca sequestered within mitochondria was localized to small inclusions that were distributed heterogeneously within, and probably among, individual mitochondria. By 30 sec after stimulation an active subpopulation of ER cisterns had accumulated more Ca than had mitochondria despite a ~1 sec delay before the onset of accumulation. Active ER cisterns retained their Ca load much longer (>3 min) than mitochondria. The complementary time courses of mitochondrial versus ER Ca²⁺ uptake and release suggest that these organelles participate in a choreographed interplay, each shaping dendritic Ca²⁺ signals within characteristic regimes of cytosolic Ca²⁺ concentration and time.

Key words: calcium; endoplasmic reticulum; mitochondria; hippocampus; synaptic activity; electron probe x-ray microanalysis

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^* N.B.P. and L.D.P.-M. contributed equally to this work.

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Copyright © 2002 Society for Neuroscience  0270-6474/02/222410653-09$05.00/0

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