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This Article Full Text Full Text (PDF) All Versions of this Article: 586/12/2889    most recent jphysiol.2008.151050v1 Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Pang, J.-J. Articles by Wu, S. M. Search for Related Content PubMed PubMed Citation Articles by Pang, J.-J. Articles by Wu, S. M. Related Collections Neuroscience

¹ Cullen Eye Institute, Baylor College of Medicine, Houston, TX 77030, USA

Photoreceptor output synapses are the best known tonic chemical synapses in the nervous system, in which glutamate is continuously released in darkness, activating AMPA/kainate receptors in postsynaptic neurons. It has been shown that glutamate receptors in certain types of second-order retinal cells are largely desensitized in darkness, leading to small postsynaptic currents and reduced response dynamic ranges. Here we show that the tonic glutamatergic synapses between photoreceptors and rod-dominated hyperpolarizing bipolar cells (HBC_Rs) in the salamander retina evade postsynaptic receptor desensitization by using (1) multiple invaginating ribbon junctions as releasing sites for low-frequency, synchronized multiquantal release at each site; and (2) the GluR4 AMPA receptors as the postsynaptic receptors. The multiquantal events exhibit faster decay time than the GluR4 receptor desensitization time constant and therefore self-desensitization is minimized, and the average inter-event duration in darkness is much longer than the GluR4 desensitization recovery time and thus mutual desensitization is avoided. Consequently, the HBC_Rs are not desensitized in darkness, allowing light signals to be encoded by the full operating range of the glutamate-gated postsynaptic currents. Our study illustrates for the first time how a tonic glutamatergic synapse avoids postsynaptic receptor desensitization, a strategy that may be shared by many other synapses in the nervous system that need extended operation capacity.

(Received 11 January 2008; accepted after revision 15 April 2008; first published online 17 April 2008)
Corresponding author S. M. Wu: Cullen Eye Institute, Baylor College of Medicine, One Baylor Plaza, NC-205, Houston, TX 77030, USA. Email: swu{at}bcm.tmc.edu