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Petri Ala-Laurila, Fred Rieke; Nonlinear Integration Of Quantal Signals In The Inner Retina Sets An Absolute Limit To Rod Vision. Invest. Ophthalmol. Vis. Sci. 2012;53(14):1940.
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Dark-adapted humans can detect flashes producing only a few photons absorbed in a small region of the retina (Hecht et al., 1942; van der Velden, 1944). Today we still do not fully understand the neural mechanisms that allow this striking sensitivity, nor do we understand where in the visual pathway the absolute limit of vision is set. We investigated these questions in the primate retina and correlated our results with the classic results of human psychophysics.
Synaptic input currents and spike responses of ON-parasol ganglion cells were recorded in flat mount preparations of the isolated, dark-adapted primate (Macaca & Papio) retinae by whole-cell and cell-attached patch clamp configurations. Parasol (magnocellular-projecting) ganglion cells are thought to mediate vision at the lowest light levels. Dark-noise, light induced noise, and responses to brief flashes of light (10-20 ms) were measured in complete darkness and in the presence of dim background lights.
In complete darkness, ON-parasols nonlinearly integrated signals originating from single photon absorptions in rod photoreceptors. This novel nonlinearity was observed in the excitatory input currents and the spike output of ON-parasols. Integration became linear in the presence of dim background light. The release of nonlinearity was associated with a significant increase in noise in the parasol cell synaptic inputs and a much larger drop in the signal-to-noise ratio than predicted by a purely linear model. The neural location underlying nonlinearity has access to at least a few hundred rod photoreceptors, and thus cannot be explained by nonlinearities operating in rods or rod bipolar cells. Our results are consistent with a location at the level of the AII amacrine cells or ON cone bipolar cells.
Our results, together with an earlier work showing a thresholding nonlinearity between rods and rod-bipolar cells (Field & Rieke, 2002), are consistent with the idea that nonlinearities operating at different levels of convergence of rod signals protect sparse signals from being overwhelmed by neural noise in the rod-bipolar pathway. The novel nonlinearity limits information about single photon absorptions available to higher visual centers right at the absolute threshold of vision and thereby sets a fundamental limit to detection as assessed by psychophysics experiments.
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