Potentiation of ‘on’ bipolar cell flash responses by dim background light and cGMP in dogfish retinal slices

Abstract

The high sensitivity of the vertebrate visual system results from amplification inherent in phototransduction in rods and from the amplification of rod signals on their synaptic transfer at the first synapse with 'on' bipolar cells. These cells possess a metabotropic glutamate receptor linked via a cGMP cascade to the control of cGMP-activated channels. In the study presented here, we show that very dim background light, isomerising only one rhodopsin in 1 out of 10 rods per second, potentiates 'on' bipolar cell responses to superimposed flashes. Responses to dim flashes, which were undetectable above the noise in the dark, were boosted above the increased noise level induced by the background. This potentiation could be reproduced by elevating cGMP, which increases with light, or by dialysing the cells with a non-hydrolysable cGMP analogue. Inhibition of tyrosine kinase activity also reproduced the effect and induced a speeding up of the rising phase of the flash response, similar to the action of dim background light. Conversely, inhibition of tyrosine phosphatase activity blocked the potentiation. These results suggest that cGMP promotes tyrosine-site dephosphorylation of 'on' bipolar cell cGMP-activated channels, resulting in a rise in the sensitivity to cGMP, as has recently been demonstrated for rod cGMP-activated channels. This constitutes a positive feedback mechanism such that as cGMP increases with light, the sensitivity of the channels to cGMP increases and boosts the signal above background noise. This mechanism would allow stochastic resonance to occur, facilitating single-photon detection when dark-adapted, and may therefore lead to improved discrimination.