Abstract

Melanopsin expressing intrinsically photosensitive Retinal Ganglion Cells (ipRGCs) entirely control the post-illumination pupil response (PIPR) from 6 s post-stimulus to the plateau during redilation after light offset. However, the photoreceptor contributions to the early redilation phase of the PIPR (< 6 s post-stimulus) have not been reported. Here, we evaluated the photoreceptor contributions to the early phase PIPR (0.6 s to 5.0 s) by measuring the spectral sensitivity of the criterion PIPR amplitude in response to 1 s light pulses at five narrowband stimulus wavelengths (409, 464, 508, 531 and 592 nm). The retinal irradiance producing a criterion PIPR was normalised to the peak and fitted by either a single photopigment nomogram or the combined melanopsin and rhodopsin spectral nomograms with the +L+M cone photopic luminous efficiency (Vλ) function. We show that the PIPR spectral sensitivity at times ≥ 1.7 s after light offset is best described by the melanopsin nomogram. At times < 1.7 s, the peak PIPR sensitivity shifts to longer wavelengths (range: 482 to 498 nm) and is best described by the combined photoreceptor nomogram, with major contributions from melanopsin and rhodopsin. This first report of melanopsin and rhodopsin contributions to the early phase PIPR is in line with the electrophysiological findings of ipRGC and rod signalling after the cessation of light stimuli and provides a cut-off time for isolating photoreceptor specific function in healthy and diseased eyes.

Highlights

  • In macaques, the pupil light reflex (PLR) measured during continuous light exposure and post light offset after pharmacological blockade of outer retinal rod and cone photoreceptors shows a sustained constriction that closely matches the spectral sensitivity of inner retinal melanopsin expressing intrinsically photosensitive Retinal Ganglion Cells [1]

  • For all measured times after light offset at all wavelengths, the criterion post-illumination pupil response (PIPR) amplitude could be achieved within ± 6.5% of the predefined criterion; the differences between the measured and criterion PIPR are shown in Fig 4 at two PIPR times, one that is described by the opn4 spectral nomogram (1.8 s) and the other that cannot be described by the opn4 nomogram (1.0 s)

  • When the binary and tertiary combination models were fitted to this data (> 1.7 s; Fig 6, upper two rows), the PIPR was completely described by the melanopsin nomogram (m) with zero weightings for the rhodopsin (r) and Vλ (c) contributions, and the model deviation decreased (Fig 7), the bias was lower and the limits of agreement were narrower than for the single nomograms (Fig 8)

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Summary

Introduction

The pupil light reflex (PLR) measured during continuous light exposure and post light offset after pharmacological blockade of outer retinal rod and cone photoreceptors shows a sustained constriction that closely matches the spectral sensitivity of inner retinal melanopsin expressing intrinsically photosensitive Retinal Ganglion Cells (ipRGCs) (peak ~482 nm) [1]. The spectral sensitivity of the post-illumination pupil response (PIPR) measured at PLOS ONE | DOI:10.1371/journal.pone.0161175. Spectral Sensitivity of the Early Phase PIPR The spectral sensitivity of the post-illumination pupil response (PIPR) measured at PLOS ONE | DOI:10.1371/journal.pone.0161175 August 22, 2016

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