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The Journal of Neuroscience, December 7, 2005, 25(49):11412-11423; doi:10.1523/JNEUROSCI.2203-05.2005

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Cellular/Molecular
Prolonged Reciprocal Signaling via NMDA and GABA Receptors at a Retinal Ribbon Synapse

Jozsef Vigh and Henrique von Gersdorff

The Vollum Institute, Oregon Health and Science University, Portland, Oregon 97239

AMPA and GABA_A receptors mediate most of the fast signaling in the CNS. However, the retina must, in addition, also convey slow and sustained signals. Given that AMPA and GABA_A receptors desensitize quickly in the continuous presence of agonist, how are sustained excitatory and inhibitory signals transmitted reliably across retinal synapses? Reciprocal synapses between bipolar and amacrine cells in the retina are thought to play a fundamental role in tuning the bipolar cell output to the dynamic range of ganglion cells. Here, we report that glutamate release from goldfish bipolar cell terminals activates first AMPA receptors, followed by fast and transient GABA_A-mediated feedback. Subsequently, prolonged NMDA receptor activation triggers GABA_A and a slow, sustained GABA_C-mediated reciprocal inhibition. The synaptic delay of the NMDA/GABA_C-mediated feedback showed stronger dependence on the depolarization of the bipolar cell terminal than the fast AMPA/GABA_A-mediated response. Although the initial depolarization mediated by AMPA receptors was important to prime the NMDA action, NMDA receptors could trigger feedback by themselves in most of the bipolar terminals tested. This AMPA-independent feedback (delay 10 ms) was eliminated in 2 mM external Mg²⁺ and reduced in some terminals, but not eliminated, by TTX. NMDA receptors on amacrine cells with depolarized resting membrane potentials therefore can mediate the late reciprocal feedback triggered by continuous glutamate release. Our findings suggest that the characteristics of NMDA receptors (high agonist affinity, slow desensitization, and activation/deactivation kinetics) are well suited to match the properties of GABA_C receptors, which thus provide part of the prolonged inhibition to bipolar cell terminals.

Key words: neurotransmission; amacrine cells; GABA_C receptor; retinal bipolar cell; NMDA receptor; GABA_A receptor; AMPA receptor

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Received May 31, 2005; revised October 25, 2005; accepted October 26, 2005.

This article has been cited by other articles:

				Y. Xu, P. Sulaiman, R. M. Feddersen, J. Liu, R. G. Smith, and N. Vardi Retinal ON Bipolar Cells Express a New PCP2 Splice Variant That Accelerates the Light Response J. Neurosci., September 3, 2008; 28(36): 8873 - 8884. [Abstract] [Full Text] [PDF]

				A. E. Chavez and J. S. Diamond Diverse Mechanisms Underlie Glycinergic Feedback Transmission onto Rod Bipolar Cells in Rat Retina J. Neurosci., July 30, 2008; 28(31): 7919 - 7928. [Abstract] [Full Text] [PDF]

				G.-L. Li, J. Vigh, and H. von Gersdorff Short-Term Depression at the Reciprocal Synapses between a Retinal Bipolar Cell Terminal and Amacrine Cells J. Neurosci., July 11, 2007; 27(28): 7377 - 7385. [Abstract] [Full Text] [PDF]

				M. J. Palmer Functional segregation of synaptic GABAA and GABAC receptors in goldfish bipolar cell terminals J. Physiol., November 15, 2006; 577(1): 45 - 53. [Abstract] [Full Text] [PDF]

				E. Wersinger, Y. Schwab, J.-A. Sahel, A. Rendon, D. V. Pow, S. Picaud, and M. J. Roux The glutamate transporter EAAT5 works as a presynaptic receptor in mouse rod bipolar cells J. Physiol., November 15, 2006; 577(1): 221 - 234. [Abstract] [Full Text] [PDF]

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