DeVries, S., Qi, X., Smith, R., Makous, W., & Sterling, P. (2002). Electrical coupling between mammalian cones. Current Biology, 12, 1900-7.

Background

Cone photoreceptors are noisy due to random fluctuations of photon absorption, signaling molecules, and ion channels. But each cone's noise is independent of the others, whereas their signals are partially shared. Therefore, prior to forward transmission and subsequent nonlinear processing, noise can be appreciably reduced relative to the signal by electrically coupling the synaptic terminals. This signal-processing strategy has been clearly demonstrated in lower vertebrates with rather coarse vision, but whether it occurs in mammals with fine acuity has been doubted (even though gap junctions are present) because coupling would blur the neural image.

Results

In slices of ground squirrel retina, whose triangular cone lattice resembles the human fovea, we made paired electrical recordings from adjacent cones. These clearly demonstrated electrical coupling with an average conductance of ~320 pS. Blur caused by this degree of coupling was calculated to have a space constant of ~0.5 cone diameters. We also made psychophysical measurements, using laser interferometry to bypass the eye's optical blur. These suggest that human foveal cones experience a similar degree of neural blur and that it is invariant with light intensity. This neural blur is narrower than the eye's optical blur, and we calculate that it should improve the signal-to-noise ratio at the cone terminal by about 77%.

Conclusions

We conclude that the gap junctions observed between mammalian cones, including those in human fovea, represent genuine electrical coupling. Because the space constant of the resulting neural blur is less than the optical blur, signal-to-noise ratio can be markedly improved before the nonlinear stages with little compromise to visual acuity.