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J Neurophysiol 83: 1710-1721, 2000;
0022-3077/00 $5.00
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The Journal of Neurophysiology Vol. 83 No. 3 March 2000, pp. 1710-1721
Copyright ©2000 by the American Physiological Society

Ca2+- and Metabolism-Related Changes of Mitochondrial Potential in Voltage-Clamped CA1 Pyramidal Neurons In Situ

S. Schuchmann,2 M. Lückermann,1 A. Kulik,1 U. Heinemann,2 and K. Ballanyi1

 1II. Physiologisches Institut, Universität Göttingen, D-37073 Göttingen; and  2Institut für Physiologie, Humboldt-Universität Berlin, Universitätsklinikum Charité, D-10117 Berlin, Germany

Schuchmann, S., M. Lückermann, A. Kulik, U. Heinemann, and K. Ballanyi. Ca2+- and Metabolism-Related Changes of Mitochondrial Potential in Voltage-Clamped CA1 Pyramidal Neurons In Situ. J. Neurophysiol. 83: 1710-1721, 2000. In hippocampal slices from rats, dialysis with rhodamine-123 (Rh-123) and/or fura-2 via the patch electrode allowed monitoring of mitochondrial potential (Delta Psi ) changes and intracellular Ca2+ ([Ca2+]i) of CA1 pyramidal neurons. Plasmalemmal depolarization to 0 mV caused a mean [Ca2+]i rise of 300 nM and increased Rh-123 fluorescence signal (RFS) by <= 50% of control. The evoked RFS, indicating depolarization of Delta Psi , and the [Ca2+]i transient were abolished by Ca2+-free superfusate or exposure of Ni2+/Cd2+. Simultaneous measurements of RFS and [Ca2+]i showed that the kinetics of both the Ca2+ rise and recovery were considerably faster than those of the Delta Psi depolarization. The plasmalemmal Ca2+/H+ pump blocker eosin-B potentiated the peak of the depolarization-induced RFS and delayed recovery of both the RFS and [Ca2+]i transient. Thus the Delta Psi depolarization due to plasmalemmal depolarization is related to mitochondrial Ca2+ sequestration secondary to Ca2+ influx through voltage-gated Ca2+ channels. CN- elevated [Ca2+]i by <50 nM but increased RFS by 221% as a result of extensive depolarization of Delta Psi . Oligomycin decreased RFS by 52% without affecting [Ca2+]i. In the presence of oligomycin, CN- and p-trifluoromethoxy-phenylhydrazone (FCCP) elevated [Ca2+]i by <50 nM and increased RFS by 285 and 290%, respectively. Accordingly, the metabolism-related Delta Psi changes are independent of [Ca2+]i. Imaging techniques revealed that evoked [Ca2+]i rises are distributed uniformly over the soma and primary dendrites, whereas corresponding changes in RFS occur more localized in subregions within the soma. The results show that microfluorometric measurement of the relation between mitochondrial function and intracellular Ca2+ is feasible in whole cell recorded mammalian neurons in situ.




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