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The Journal of Neuroscience, June 8, 2005, 25(23):5502-5510; doi:10.1523/JNEUROSCI.1354-05.2005

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Cellular/Molecular
Calcium Increases in Retinal Glial Cells Evoked by Light-Induced Neuronal Activity

Eric A. Newman

Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455

Electrical stimulation of neurons in brain slices evokes increases in cytoplasmic Ca²⁺ in neighboring astrocytes. The present study tests whether similar neuron-to-glial signaling occurs in the isolated rat retina in response to light stimulation. Results demonstrate that Müller cells, the principal retinal glial cells, generate transient increases in Ca²⁺ under constant illumination. A flickering light stimulus increases the occurrence of these Ca²⁺ transients. Antidromic activation of ganglion cell axons also increases the generation of Müller cell Ca²⁺ transients. The increases in Ca²⁺ transients evoked by light and antidromic stimulation are blocked by the purinergic antagonist suramin and by TTX. The addition of adenosine greatly potentiates the response to light, with light ON evoking large Ca²⁺ increases in Müller cells. Suramin, apyrase (an ATP-hydrolyzing enzyme), and TTX substantially reduce the adenosine-potentiated response. NMDA, metabotropic glutamate, GABA_B, and muscarinic receptor antagonists, in contrast, are mainly ineffective in blocking the response. Light-evoked Ca²⁺ responses begin in Müller cell processes within the inner plexiform (synaptic) layer of the retina and then spread into cell endfeet at the inner retinal surface. These results represent the first demonstration that Ca²⁺ increases in CNS glia can be evoked by a natural stimulus (light flashes). The results suggest that neuron-to-glia signaling in the retina is mediated by neuronal release of ATP, most likely from amacrine and/or ganglion cells, and that the response is augmented under pathological conditions when adenosine levels increase.

Key words: calcium; astrocyte; Müller cell; glial cell; retina; ATP; adenosine; light response; ganglion cell

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Received Dec 13, 2004; revised April 25, 2005; accepted April 25, 2005.

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