JN Journal of Neurophysiology
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J Neurophysiol 82: 2947-2955, 1999;
0022-3077/99 $5.00
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The Journal of Neurophysiology Vol. 82 No. 6 December 1999, pp. 2947-2955
Copyright ©1999 by the American Physiological Society

Adenosine A1 and Class II Metabotropic Glutamate Receptors Mediate Shared Presynaptic Inhibition of Retinotectal Transmission

Chunyi Zhang and John T. Schmidt

Department of Biological Sciences and Neurobiology Research Center, University at Albany, State University of New York, Albany, New York 12222

Zhang, Chunyi and John T. Schmidt. Adenosine A1 and Class II Metabotropic Glutamate Receptors Mediate Shared Presynaptic Inhibition of Retinotectal Transmission. J. Neurophysiol. 82: 2947-2955, 1999. Presynaptic inhibition is one of the major control mechanisms in the CNS. Previously we reported that adenosine A1 receptors mediate presynaptic inhibition at the retinotectal synapse of goldfish. Here we extend these findings to metabotropic glutamate receptors (mGluRs) and report that presynaptic inhibition produced by both A1 adenosine receptors and group II mGluRs is due to Gi protein coupling to inhibition of N-type calcium channels in the retinal ganglion cells. Adenosine (100 µM) and an A1 (but not A2) receptor agonist reduced calcium current (ICa2+) by 16-19% in cultured retinal ganglion cells, consistent with their inhibition of retinotectal synaptic transmission (-30% amplitude of field potentials). The general metabotropic glutamate receptor (mGluR) agonist 1S,3R-1-amino-cyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD, 50 µM) and the selective group II mGluR receptor agonist (2S,2'R,3'R)-2-(2',3'-dicarboxy-cyclopropyl)glycine (DCG-IV, 300 nM) inhibited both synaptic transmission and ICa2+, whereas the group III mGluR agonist L-2-amino-4-phosphono-butyrate (L-AP4) inhibited neither synaptic transmission nor ICa2+. When the N-type calcium channels were blocked with omega -conotoxin GVIA, both adenosine and DCG-IV had much smaller percentage effects on the residual 20% of ICa2+, suggesting effects mainly on the N-type calcium channels. The inhibitory effects of A1 adenosine receptors and mGluRs were both blocked by pertussis toxin, indicating that they are mediated by either Gi or Go. They were also inhibited by activation of protein kinase C (PKC), which is known to phosphorylate and inhibit Gi. Finally, when applied sequentially, inhibition by adenosine and DCG-IV were not additive but occluded each other. Together these results suggest that adenosine A1 receptors and group II mGluRs mediate presynaptic inhibition of retinotectal synaptic transmission by sharing a pertussis toxin (PTX)-sensitive, PKC-regulated Gi protein coupled to N-type calcium channels.




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