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

TLDR

Using confocal fluorescence microscopy of indo‑1–loaded acute rat brain slices, the authors mapped the spatial–temporal characteristics of Ca²⁺ changes in neurons and astrocytes, identifying cell types by morphology, electrophysiology, and pharmacology. Neuronal afferent stimulation induces periodic astrocytic Ca²⁺ oscillations whose frequency is dynamically modulated by the stimulation pattern and can be persistently elevated by repeated stimulation, with accompanying neuronal Ca²⁺ rises likely driven by glutamate release via a tetanus‑toxin‑resistant pathway, demonstrating that astrocytic Ca²⁺ oscillations constitute a highly plastic bidirectional communication system between neurons and astrocytes.

Abstract

The spatial–temporal characteristics of intracellular calcium ([Ca 2+ ] 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 Ca 2+ 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 [Ca 2+ ] 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 [Ca 2+ ] i oscillation frequency. Oscillating astrocytes were accompanied by repetitive [Ca 2+ ] i elevations in adjacent neurons, most likely because of the release of glutamate via a tetanus toxin-resistant process. These results reveal that [Ca 2+ ] i oscillations in astrocytes represent a highly plastic signaling system that underlies the reciprocal communication between neurons and astrocytes.