Opponent melanopsin and S-cone signals in the human pupillary light response

2014 study

Manuel Spitschan, Sandeep Jain, David H. Brainard, and Geoffrey K. Aguirre. Departments of Psychology and Neurology, University of Pennsylvania, Philadelphia, PA 19104

In the human, cone photoreceptors (L, M, and S) and the melanopsincontaining, intrinsically photosensitive retinal ganglion cells (ipRGCs) are active at daytime light intensities. Signals from cones are combined both additively and in opposition to create the perception of overall light and color. Similar mechanisms seem to be at work in the control of the pupil’s response to light. Uncharacterized however, is the relative contribution of melanopsin and S cones, with their overlapping, short-wavelength spectral sensitivities. We measured the response of the human pupil to the separate stimulation of the cones and melanopsin at a range of temporal frequencies under photopic conditions. The S-cone and melanopsin photoreceptor channels were found to be low-pass, in contrast to a band-pass response of the pupil to L- and M-cone signals. An examination of the phase relationships of the evoked responses revealed that melanopsin signals add with signals from L and M cones but are opposed by signals from S cones in control of the pupil. The opposition of the S cones is revealed in a seemingly paradoxical dilation of the pupil to greater S-cone photon capture. This surprising result is explained by the neurophysiological properties of ipRGCs found in animal studies.

Results Using an infrared camera, we measured the consensual PLR of human participants while they observed sinusoidal modulations in the spectrum of a light (Fig. 1B). The stimulus modulations were designed to target specific photoreceptors. The cones and melanopsin have different but overlapping spectral sensitivities. Despite the overlap, it is possible to create sets of light spectra such that the absorption of photons is constant for all of the photoreceptor classes except one (14–16) (Fig. 1C). Modulation between a pair of these “silent substitution” spectra increases and decreases the response of (for example) melanopsin-containing ipRGCs while maintaining nominally constant stimulation of the cones. Separate modulations were designed for melanopsin, S cones, and L+M cones together (a modulation that varied luminance as well as chromaticity). An isochromatic modulation (melanopsin+S+M+L) was also used. All modulations were designed to produce 50% contrast on their targeted photoreceptor(s). Rods were silenced by modulating the spectra about a photopic background (∼800 cd/m2 ). The stimulus was wide-field (27.5°), spatially uniform, and had the central 5° obscured to avoid variation in photoreceptor spectral sensitivity across the visual field caused by the presence of the foveal macular pigment (17). Simulations and control experiments support the specificity of the photoreceptor isolation (Figs. S1–S5 and Table S1). We measured pupil responses from 16 subjects while they observed the different photoreceptor-directed modulations at two for each combination of photoreceptor target and modulation frequency. The two-filter model fits the average amplitude and phase data (Fig. 5A) with parameters similar to those found for subject 01 (Table S2). When expressed as a polar plot (Fig. 5B), the agreement between the group data and model fits is apparent. Interestingly, there is systematic “rotation” of the phase of both the pupil brightness and S-cone responses at the lower temporal frequency that is not captured by the model. This may result from individual differences in the phase of S-cone responses at low temporal frequencies, as is seen between subject 01 and subject 02 (Fig. 4), because the average data do not fully constrain the model and the fits shown are based on parameters obtained for subject 01.

Whole study on this link