Latency characteristics of the short-wavelength-sensitive cones and their associated pathways

Abstract

There are many distinct types of retinal ganglion and LGN cells that have opponent cone inputs and which may carry chromatic information. Of interest are the asymmetries in those LGN cells that carry S-cone signals: in S-ON cells, S+ signals are opposed by (L + M) whereas, in many S-OFF cells, L+ signals are opposed by (S + M), giving -S + L - M (C. Tailby, S. G. Solomon, & P. Lennie, 2008). However, the S-opponent pathway is traditionally modeled as +/-[S - (L + M)]. A phase lag of the S-cone signal has been inferred from psychophysical thresholds for discriminating combinations of simultaneous sinusoidal modulations along +/-[L - M] and +/-[S - (L + M)] directions (C. F. Stromeyer, R. T. Eskew, R. E. Kronauer, & L. Spillmann, 1991). We extend this experiment, measuring discrimination thresholds as a function of the phase delay between pairs of orthogonal component modulations. When one of the components isolates the tritan axis, there are phase delays at which discrimination is impossible; when neither component is aligned with the tritan axis, discrimination is possible at all delays. The data imply that the S-cone signal is delayed by approximately 12 ms relative to (L - M) responses. Given that post-receptoral mechanisms show diverse tuning around the tritan axis, we suggest that the delay arises before the S-opponent channels are constructed, possibly in the S-cones themselves.

Figure 1

The sequences of chromaticities produced by sinusoidal Δ[L − M] and ΔS modulations in different phase relationships. The plots on the left show modulations as a function of time; the plots on the right show the loci of chromaticities that are visited. In the plots on the left, the Δ[L − M] signal is used as a reference (thin black solid line). When this is combined with a ΔS modulation with a 3π/2 phase shift (top-left panel, thick blue solid line), the resulting sequence of chromaticities follows a circular clockwise (CW) trajectory in the equiluminant plane of DKL color space (top-right plot, thick blue solid line). If the ΔS modulation has a phase of π/2 relative to the Δ[L − M] signal (lower left panel, thick red solid line), the sequence of chromaticities plots out a circular counterclockwise (CCW) trajectory (bottom-right panel, thick red solid line). If the phase of the ΔS modulation is delayed from 3π/2 (dashed curves in upper panels), then the chromaticities follow elliptical trajectories in color space. These ellipses are oriented with their major axis along the positive diagonal, becoming more eccentric with larger phase differences, up to a phase difference of π. For delays from π/2 (dashed curves in lower panels), the ellipses are oriented with their major axis along the negative diagonal. Importantly, inverting the S-cone modulation by introducing a phase difference of π reverses the sense of procession and the orientation of the ellipse (and defines the difference between upper and lower panels).

Figure 2

Simulated chromatic loci reaching a central site when the stimuli are composed of sinusoidal modulations (upper panel, A) along the cardinal directions of color space or (bottom panel, B) along our intermediate axes. Each square represents the equiluminant plane of DKL color space. CW stimulus loci (where the component modulations have a phase difference of θ) are shown in blue, and CCW loci (where the component modulations have a phase difference of θ − π) are shown in red. Each column of plots represents a different value of θ and each row represents a different simulated neural phase shift φ introduced by the S-cones or the putative ±[S − (L + M)] mechanism. Note how, in the cardinal axes condition, increasing φ translates the pattern of ellipses to the right but in the intermediate axes condition, increasing φ rotates the ellipses and the patterns remain symmetrical around θ = 0.5π.

Figure 3

Measured thresholds for discriminating CW and CCW processions, as a function of θ, the phase difference between component modulations. Panels A–D represent results from observer RJL and panels E–H are for observer HES. Panels A, B, E, and F show data from the experimental conditions when component modulations were along the cardinal axes. Panels C, D, G, and H show data from conditions in which component modulations were along intermediate axes. The left-hand column of panels represents conditions in which the ΔS modulation or the Δ[S + L − M] modulation was adjusted by the staircase. The right-hand column of panels represents conditions in which the Δ[L − M] modulation or the Δ[S − L + M] modulation was adjusted by the staircase. Data points are the geometric mean of at least four staircases. Error bars indicate one geometric standard deviation above and below the geometric mean of several staircase results. Arrows along the top edges of each panel indicate that we failed to measure thresholds at the corresponding phase difference on some attempts (small orange arrows) or on all attempts (large red arrows). The green and blue lines represent predictions of the model described in the text and shown in Figure 4, with parameters adjusted to obtain least-squares best fits to the data. The faint lines in panels C and D represent the simple version of the intermediate axes model in which the rotation of the axes is fixed, and darker blue lines represent the model in which the axis rotation can vary. The gray shaded areas represent the range of values of θ at which the peaks of the predicted thresholds may occur, based on a 95% confidence interval on the neural phase delay variable.

Figure 4

Predicted thresholds for discriminating between a stimulus in which component sinusoidal modulations have a phase difference of θ and a stimulus in which the phase difference is θ − π, as a function of θ. Green lines show predictions when component modulations aligned with the cardinal axes, and blue lines show predictions for the intermediate axes. The uppermost panel assumes no neural delay between the response to ΔS and Δ[L − M], and each subsequent panel shows predictions for successive small increases in the phase delay of the ΔS response, denoted by φ.