LINEAR AND NONLINEAR BEHAVIORS OF THE PHOTORECEPTOR COUPLED NETWORK

Abstract

Photoreceptors are electrically coupled to one another, and the spatiotemporal properties of electrical synapses in a two-dimensional retinal network are still not well-studied, because of the limitation of the single electrode or pair recording techniques which do not allowsimultaneouslymeasuring responses of multiple photoreceptors at various locations in the retina. A multiple electrode recording system is needed. In this study we investigate thenetworkproperties of the two-dimensional rod coupled array of the salamander retina (both sexes were used) by using the newly available multiple patch electrode system that allows simultaneous recordings from up to 8 cells, and to determine the electrical connectivity among multiple rods. We found direct evidence that voltage signal spread in the rod-rod coupling network in the absence of Ih(mediated by HCN channels) is passive and follows the linear cable equation. Under physiological conditions, Ihshapes the network signal by progressively shortening the response time-to-peak of distant rods, compensating the time loss of signal traveling from distant rods to bipolar cell somas and facilitating synchronization of rod output signals. Under voltage clamp conditions, current flow within the coupled rods follows Ohm's Law, supporting the idea that nonlinear behaviors of the rod network are dependent on membrane voltage. Rod-rod coupling is largely symmetrical in the 2-D array,and voltage clamp blocking the next neighboring rod largely suppresses rod signal spread into the second neighboring rod, suggesting that indirect coupling pathways play a minor role in rod-rod coupling.SIGNIFICANCE STATEMENTThis study employs the newly available multiple patch electrode technique to study the network properties of photoreceptors by simultaneously recording from multiple neurons. Unraveling how the photoreceptor coupled network shapes spatiotemporal responses, voltage gains and synaptic transfer in outer retina is crucial for our understanding of how the brain senses the visual world. Moreover, the negative peak response velocity of the coupled rod network mediated by HCN channels synchronize rod signals converging to a bipolar cell and improves the temporal resolution of the rod output synapses, a strategy that may be used by other coupled neuronal networks in the brain.