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

Abstract

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 identifiedin situon the basis of their morphological, electrophysiological, and pharmacological features. We show here that stimulation of neuronal afferents triggered periodic [Ca²⁺]_ioscillations 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⁺]_ioscillation frequency. Oscillating astrocytes were accompanied by repetitive [Ca²⁺]_ielevations in adjacent neurons, most likely because of the release of glutamate via a tetanus toxin-resistant process. These results reveal that [Ca²⁺]_ioscillations in astrocytes represent a highly plastic signaling system that underlies the reciprocal communication between neurons and astrocytes.