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A. V. Dmitriev, S. C. Mangel; Both Cellular and Network Mechanisms Contribute to Directionally Selective Light Response of Starburst Amacrine Cells. Invest. Ophthalmol. Vis. Sci. 2010;51(13):1853.
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Starburst amacrine cells (SACs) generate direction-selective (DS) light responses that strongly depend on lateral GABA-driven inputs, provided in part by other SACs. Importantly, SACs respond to GABA with either a depolarization or hyperpolarization, depending on the local Cl- equilibrium potential (Gavrikov et al., 2006). The finding that GABA can change the SAC membrane potential (Em) suggests the possibility of lateral communication through the net of densely packed SACs. We have therefore investigated how these network and cellular mechanisms together produce SAC DS responses.
Each SAC was modeled by an electrical equivalent circuit that consisted of a cell body and 8 proximal and 16 distal dendritic compartments. Each compartment had a set of transmembrane resistances (constant for K+ channels, but variable for GABA- and glutamate-gated channels) and corresponding batteries. The Em in each compartment was calculated and then Em-dependent, GABA release from distal SAC compartments was determined. The GABA concentration at each location of the network was then adjusted by a reuptake mechanism, and the Em in each compartment of each modeled SAC was recalculated according to the resultant changes in GABA-mediated resistances. To simulate light stimulation, the glutamate-gated resistances were decreased in all illuminated parts of the SACs.
The calculations showed that if the Cl- equilibrium potential was not equal to Em, GABA-mediated SAC to SAC communication supported the lateral propagation of a signal in the SAC network. As a result, the area of cells activated by light was significantly wider than the area of light stimulation. When a moving bar of light was simulated, GABA-dependent SAC-to-SAC interactions resulted in a GABA wave that preceded in time and space the light-induced glutamate-evoked excitation. This GABA wave significantly altered the SAC responses, particularly in the distal dendrites, and thus determined in large part the direction selectivity of SACs.
The results suggest that the combination of 1) the difference between the local Cl- equilibrium potential and the local Em along SAC dendrites and 2) GABA-dependent SAC-to-SAC lateral interactions plays an important role in the direction selectivity of SACs.
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