Functional loss in the magnocellular and parvocellular pathways in patients with optic neuritis

Abstract

Purpose: To evaluate contrast threshold and contrast gain in patients with optic neuritis under conditions designed to favor mediation by either the inferred magnocellular (MC) or parvocellular (PC) pathway.

Methods: Achromatic and chromatic contrast discrimination was measured in 11 patients with unilateral or bilateral optic neuritis and in 18 age-matched controls with normal vision, using achromatic steady- and pulsed-pedestal paradigms to bias performance toward the MC or PC pathway, respectively. In addition, L-M chromatic discrimination at equiluminance was evaluated using the steady-pedestal paradigm. A physiologically plausible model could describe the data with parameters accounting for contrast gain and contrast sensitivity in the inferred MC or PC pathway. The fitted parameters from the eye affected by optic neuritis were compared with those from the normal eye using generalized estimation equation (GEE) models that can account for within-subject correlations.

Results: Compared with normal eyes, the affected eyes had significantly higher saturation parameters when measured with both the achromatic pulsed-pedestal paradigm (GEE: β [SE] = 0.35 [0.06]; P < 0.001) and the chromatic discrimination paradigm (β [SE] = 0.18 [0.08]; P = 0.015), suggesting that contrast gain in the inferred PC pathway is reduced; the affected eyes also had reduced absolute sensitivity in the inferred MC pathway measured with the achromatic steady-pedestal paradigm (β [SE] = 0.12 [0.04]; P = 0.005).

Conclusions: Optic neuritis produced large sensitivity losses mediated by the MC pathway and contrast gain losses in the inferred PC pathway. A clinical framework is presented for interpreting contrast sensitivity and gain loss to chromatic and achromatic stimuli in terms of retinal and postretinogeniculate loci contributions to detection and discrimination.

Figure 1.

Stimulus paradigms for the achromatic pulsed-pedestal condition (top), achromatic steady-pedestal condition (middle), and chromatic steady-pedestal condition (bottom). All three paradigms shared the same spatial stimulus configuration. A pedestal consisting of a 2 × 2 pedestal array of four 1° squares separated by 0.06° was set within a uniform 9.2° × 8.7° rectangular surround. For each trial, one square in the pedestal array was randomly chosen as the test square, which differed in luminance or chromaticity from other squares during the stimulus presentation. The observer's task was to identify which square differed from the other three. The pedestal was either pulsed simultaneously with the test square for 26.6 ms during the trial period (pulsed-pedestal condition) or presented continuously (the steady-pedestal condition). The achromatic pulsed-pedestal condition reveals PC pathway achromatic contrast gain, the achromatic steady-pedestal condition reveals steady state MC pathway sensitivity, and the chromatic steady-pedestal condition reveals PC pathway chromatic contrast gain.

Figure 2.

The luminance discrimination threshold for optic neuritis patients, in reference to the 95% CI (shaded area) defined by the normal observer data. Open symbols: data for the achromatic pulsed-pedestal paradigm; filled symbols: show data for the achromatic steady-pedestal paradigm; lines: model fits of equations 2 and 3. Arrow: the retinal illuminance of the surround.

Figure 3.

The L/M discrimination threshold in optic neuritis patients, in reference to the 95% CIs (shaded area) defined by the normal observer data. Lines: model fits of equation 4. Arrow: the retinal illuminance of the surround.

Figure 4.

Box plots for the median (50th percentile, the band inside the box) and interquartile range (25th–75th percentile, the bottom and top edges of the box) of the fitted contrast sensitivity and contrast gain parameters in normal eyes and affected eyes. Left: model parameters for achromatic paradigms (top: steady-pedestal; middle and bottom: for pulsed-pedestal). Right: model parameters for chromatic paradigm. The P values are from age-controlled GEE analyses.