Abstract
Purpose: :
To investigate the coupling resistance between rods, and resting membrane resistance of isolated rods in order to develop a model of coupled rod photoreceptors. With the model, we examine how rod-rod coupling in the salamander retina leads to a decrease in noise at the expense of spatial resolution.
Methods: :
Dual patch voltage clamp experiments of adjacent rods were performed in the whole salamander retina in order to evaluate the coupling resistance between cells. One cell, designated the follower, was held at -40 mV while the other was pulsed between -120 and +20 mV. The current in the follower cell was used to calculate the apparent network coupling resistance. We also use a bar light stimulus projected onto the retina from a modified consumer LCOS video projector to estimate the network length constant. Resulting estimates were used as parameters in a linear model of the rod network which was solved numerically using MATLAB.
Results: :
Dual voltage-clamp measurements demonstrate an average initial apparent coupling resistance of 890 ± 10 MΩ (SEM) in the network, and an apparent steady-state coupling resistance of 1120 ± 13 MΩ (SEM). Using light stimuli, we estimate a one-dimensional length constant of 25 microns in rods and 12 microns in cones. With the known whole field response-intensity relationship for the cone, we estimate the profile of scattered light in the retina. From this data we calculate the ideal electrical length constant of the rod to be 9.8 microns. These results translate into a coupling resistance of approximately 930 MΩ between two isolated rods, and a membrane resistance of 300 MΩ, which we use as parameters in a linear model describing the rod network.
Conclusions: :
With parameters for coupling and membrane resistance defined, we demonstrate that electrical coupling results in a twofold increase in the signal-to-noise ratio for whole field stimuli in comparison with uncoupled rods. When stimuli of increasing spatial frequencies are considered, this advantage is reduced. However, for most perceptible spatial frequencies, electrical coupling offers an advantageous signal-to-noise ratio over an uncoupled network. Photoreceptor coupling may be a disadvantage in perceiving high contrast fine image features such as text, but it is well suited to perceiving noisy, low intensity stimuli with the low spatial frequency image components that are characteristic of natural scenes. In this way, rod-rod coupling provides an advantage in the representation of visual scenes that the rod pathways have presumably evolved to perceive: natural environments dimly lit by starlight or moonlight.
Keywords: photoreceptors: visual performance • gap junctions/coupling • electrophysiology: non-clinical