A rise in intracellular Ca2+ underlies light adaptation in dogfish retinal ‘on’ bipolar cells

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Abstract
1 This investigation was to determine the extent to which retinal ‘on’ bipolar cells contribute to the adaptive changes that occur with light, which enable the rod visual system to operate over a wide range of ambient light intensities, and to elucidate the underlying adaptive mechanism. 2 Whole‐cell voltage clamp recordings were obtained from bipolar cells in dark‐adapted dogfish retinal slices. Current responses to brief flashes and steps of light were analysed. ‘On’ bipolar cell inward current light responses are mediated by a metabotropic glutamate receptor linked to the control of a cGMP cascade, with cGMP opening cation channels. Outward current responses to light of ‘off’ bipolar cells are mediated by the closure of ionotropic glutamate receptor channels. 3 When Ca2+ buffer was omitted from the patch pipette solution, ‘on’ bipolar cells rapidly desensitized to steps of light as dim as one rhodopsin molecule bleached per rod per second (1 Rh* s−1), whereas ‘off’ bipolar cells did not desensitize. Responses of ‘on’ bipolar cells to flashes in the presence of dim backgrounds recovered after a delay, but with diminished sensitivity, i.e. the cells adapted. 4 With the Ca2+ chelator BAPTA in the patch pipette solution, step responses of ‘on’ bipolar cells were sustained and flash responses following steps showed rapid recovery. Buffering Ca2+ in the patch pipette solution to 1 μm prevented desensitization, whereas 50 μm free Ca2+ reduced the ‘on’ bipolar cell flash responses, suppressed inward dark current and decreased input conductance. 5 We conclude that a major component of adaptation of the visual system is due to a reduction in gain at the rod‐‘on’ bipolar cell synapse as a result of Ca2+ loading of the dendrites when their cGMP‐gated cation channels open with light.