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Volume 17, Number 20, Issue of October 15, 1997 pp. 7817-7830
Copyright ©1997 Society for Neuroscience

Intracellular Calcium Oscillations in Astrocytes: A Highly Plastic, Bidirectional Form of Communication between Neurons and Astrocytes In Situ

Received May 19, 1997; revised July 14, 1997; accepted Aug. 6, 1997.

Lucia Pasti1, Andrea Volterra2, Tullio Pozzan1, and Giorgio Carmignoto1

1 Department of Experimental Biomedical Sciences and Consiglio Nazionale delle Ricerche Center for Biomembranes, University of Padova, 35121 Padova, Italy, and 2 Institute of Pharmacological Sciences, University of Milan, 20133 Milan, Italy

The spatial-temporal characteristics of intracellular calcium ([Ca2+]i) changes elicited in neurons and astrocytes by various types of stimuli were investigated by means of confocal fluorescent microscopy in acute rat brain slices loaded with the Ca2+ indicator indo-1. Neurons and astrocytes from the visual cortex and CA1 hippocampal region were identified in situ on the basis of their morphological, electrophysiological, and pharmacological features. We show here that stimulation of neuronal afferents triggered periodic [Ca2+]i oscillations in astrocytes. The frequency of these oscillations was under a dynamic control by neuronal activity as it changed according to the pattern of stimulation. After repetitive episodes of neuronal stimulation as well as repetitive stimulation with a metabotropic glutamate receptor agonist, astrocytes displayed a long-lasting increase in [Ca2+]i oscillation frequency. Oscillating astrocytes were accompanied by repetitive [Ca2+]i elevations in adjacent neurons, most likely because of the release of glutamate via a tetanus toxin-resistant process. These results reveal that [Ca2+]i oscillations in astrocytes represent a highly plastic signaling system that underlies the reciprocal communication between neurons and astrocytes.

Key words: astrocytes; metabotropic glutamate receptor; intracellular calcium oscillations; synaptic plasticity; neurotransmitter release; hippocampus; visual cortex; tetanus toxin; confocal microscopy




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M. L. Cotrina, J. H.-C. Lin, A. Alves-Rodrigues, S. Liu, J. Li, H. Azmi-Ghadimi, J. Kang, C. C. G. Naus, and M. Nedergaard
Connexins regulate calcium signaling by controlling ATP release
PNAS, December 22, 1998; 95(26): 15735 - 15740.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
P. Aimar, L. Pasti, G. Carmignoto, and A. Merighi
Nitric Oxide-Producing Islet Cells Modulate the Release of Sensory Neuropeptides in the Rat Substantia Gelatinosa
J. Neurosci., December 15, 1998; 18(24): 10375 - 10388.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
A. Araque, R. P. Sanzgiri, V. Parpura, and P. G. Haydon
Calcium Elevation in Astrocytes Causes an NMDA Receptor-Dependent Increase in the Frequency of Miniature Synaptic Currents in Cultured Hippocampal Neurons
J. Neurosci., September 1, 1998; 18(17): 6822 - 6829.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
G. Carmignoto, L. Pasti, and T. Pozzan
On the Role of Voltage-Dependent Calcium Channels in Calcium Signaling of Astrocytes In Situ
J. Neurosci., June 15, 1998; 18(12): 4637 - 4645.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
A. Nadal, J.-Y. Sul, M. Valdeolmillos, and P. A McNaughton
Albumin elicits calcium signals from astrocytes in brain slices from neonatal rat cortex
J. Physiol., June 15, 1998; 509(3): 711 - 716.
[Abstract] [Full Text] [PDF]


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NeuroscientistHome page
D. S. Antanitus
A Theory of Cortical Neuron-Astrocyte Interaction
Neuroscientist, May 1, 1998; 4(3): 154 - 159.
[PDF]


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J. Neurosci.Home page
M. L. Cotrina, J. Kang, J. H-C Lin, E. Bueno, T. W. Hansen, L. He, Y. Liu, and M. Nedergaard
Astrocytic Gap Junctions Remain Open during Ischemic Conditions
J. Neurosci., April 1, 1998; 18(7): 2520 - 2537.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
G. Sharma and S. Vijayaraghavan
From the Cover: Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores
PNAS, March 27, 2001; 98(7): 4148 - 4153.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Cell Physiol.Home page
G. Su, D. B. Kintner, and D. Sun
Contribution of Na+-K+-Cl- cotransporter to high-[K+]o- induced swelling and EAA release in astrocytes
Am J Physiol Cell Physiol, May 1, 2002; 282(5): C1136 - C1146.
[Abstract] [Full Text] [PDF]



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