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The Journal of Neuroscience, November 1, 2001, 21(21):8514-8522

Potentiation of L-Type Calcium Channels Reveals Nonsynaptic Mechanisms that Correlate Spontaneous Activity in the Developing Mammalian Retina

J. H. Singer, R. R. Mirotznik, and M. B. Feller

Synapse Formation and Function Unit, National Institutes of Health, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892

Although correlated neural activity is a hallmark of many regions of the developing nervous system, the neural events underlying its propagation remain largely unknown. In the developing vertebrate retina, waves of spontaneous, correlated neural activity sweep across the ganglion cell layer. Here, we demonstrate that L-type Ca²⁺ channel agonists induce large, frequent, rapidly propagating waves of neural activity in the developing retina. In contrast to retinal waves that have been described previously, these L-type Ca²⁺ channel agonist-potentiated waves propagate independent of fast synaptic transmission. Bath application of nicotinic acetylcholine, AMPA, NMDA, glycine, and GABA_A receptor antagonists does not alter the velocity, frequency, or size of the potentiated waves. Additionally, these antagonists do not alter the frequency or magnitude of spontaneous depolarizations that are recorded in individual retinal ganglion cells. Like normal retinal waves, however, the area over which the potentiated waves propagate is reduced dramatically by 18-glycyrrhetinic acid, a blocker of gap junctions. Additionally, like normal retinal waves, L-type Ca²⁺ channel agonist-potentiated waves are abolished by adenosine deaminase, which degrades extracellular adenosine, and by aminophylline, a general adenosine receptor antagonist, indicating that they are dependent on adenosine-mediated signaling. Our study indicates that although the precise spatiotemporal properties of retinal waves are shaped by local synaptic inputs, activity may be propagated through the developing mammalian retina by nonsynaptic pathways.

Key words: retinal waves; development; visual system; calcium imaging; network; gap junctions

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21218514-09$05.00/0

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