Quantitative relations between color-opponent response of horizontal cells and action spectra of cones

Abstract

1. Relations between cones and chromatic-type horizontal cells (C-cells) were investigated by intracellular recording in the retina of the walleye (Stizostedion vitreum). 2. The retina contains two classes of cones, midwave (M) and long wave (L). Their action spectra have maximum sensitivity at 533 and 605 nm, respectively, and have been measured with good precision from 400 to 750 nm. 3. C-cells generate relatively sustained depolarizing and hyperpolarizing responses to deep red (680 nm) and green (530 nm) test flashes, respectively, but prominent on and off transients are evoked by intermediate wavelengths. To minimize these temporal interactions, quantitative analysis was restricted to measurements of the apparent steady-state response amplitude. 4. Response amplitude was linearly related to flash intensity for responses that did not exceed 20% of their respective maxima. This is called the linear range. At higher levels, the nonlinear region of the Naka-Rushton relation holds approximately if input is largely confined to the hyperpolarizing or depolarizing mechanism. 5. Tests with red/green mixture flashes show that the hyperpolarizing and depolarizing inputs interact by simple summation for responses in the linear range. At higher levels, the interaction is complex. 6. Spectral-response curves (response amplitude versus wavelength for flashes of equal photon level) were determined for 16 C-cells in the linear range. The exact form of these curves varied considerably from cell to cell, reflecting differences in the relative strength of the hyperpolarizing and depolarizing mechanisms. 7. The spectral-response curves were analyzed by a simple linear model based on the action spectra of the L and M cones. Measured and predicted spectral-response curves agree closely. The only free parameter in the analysis is a scaling factor that specifies the strength of the L cone input relative to the M cone input. 8. Triphasic spectral-response curves, as predicted by the model, were found in the sauger (Stizostedion canadense). These C-cells have short-wavelength responses due to input from long-wave cones, resemble certain triphasic cells in primate retina, and differ sharply from other triphasic C-cells found in other fish retinas. 9. Although the precise synaptic mechanisms must still be identified, the present results show that the functional information transfer from cones to C-cells in the linear range can be closely approximated by simple operations of scaling, sign inversion, and simple summation. The C-cell thus effectively subtracts one cone action spectrum from the other and displays the difference in the form of the spectral-response curve.