Abstract
The eye drives non-visual (NV) responses to light, including circadian resetting, pupillary reflex and alerting effects. Initially thought to depend on melanopsin-expressing retinal ganglion cells (ipRGCs), classical photopigments play a modulatory role in some of these responses. As most studies have investigated only a limited number of NV functions, generally under conditions of relatively high light levels and long duration of exposure, whether NV functions share similar irradiance sensitivities and response dynamics during light exposure is unknown. We addressed this issue using light exposure paradigms spectrally and spatially tuned to target mainly cones or ipRGCs, and by measuring longitudinally (50 min) several NV responses in 28 men. We demonstrate that the response dynamics of NV functions are faster than previously thought. We find that the brain, the heart, and thermoregulation are activated within 1 to 5 min of light exposure. Further, we show that NV functions do not share the same response sensitivities. While the half-maximum response is only ∼48 s for the tonic pupil diameter, it is ∼12 min for EEG gamma activity. Most NV responses seem to be saturated by low light levels, as low as 90 melanopic lux. Our results also reveal that it is possible to maintain optimal visual performance while modulating NV responses. Our findings have real-life implications. On one hand, light therapy paradigms should be re-evaluated with lower intensities and shorter durations, with the potential of improving patients’ compliance. On the other hand, the significant impact of low intensity and short duration light exposures on NV physiology should make us reconsider the potential health consequences of light exposure before bedtime, in particular on sleep and circadian physiology.
Highlights
By processing light information via dedicated pathways, the mammalian retina can engage in vision and in light-dependent non-visual (NV) responses such as melatonin suppression, pupillary constriction, increase in body temperature and heart rate, and modulation of cortical brain activity
We have demonstrated that polychromatic lights with different spectral content and spatial distribution stimulate several NV responses with different dynamics and sensitivities
NV responses can be saturated by relatively low light levels, as low as 90 melanopic lux, for most responses
Summary
By processing light information via dedicated pathways, the mammalian retina can engage in vision and in light-dependent non-visual (NV) responses such as melatonin suppression, pupillary constriction, increase in body temperature and heart rate, and modulation of cortical brain activity. A body of evidence in human studies, including in blind individuals lacking classical visual photoreceptors (Zaidi et al, 2007), show a short wavelength sensitivity of NV functions (Cajochen et al, 2005; Revell et al, 2005; Münch et al, 2006; Lockley et al, 2006; Vandewalle et al, 2007; Mure et al, 2009; Gooley et al, 2010, 2012), with a peak around 480 nm (Brainard et al, 2001; Thapan et al, 2001; Najjar et al, 2014), close to the peak sensitivity of ipRGCs (Berson et al, 2002; Dacey et al, 2005). While the highest density of cones is in the fovea, ipRGCs and rods are totally absent from this area and are distributed over the remaining visual field (Dacey et al, 2005; Liao et al, 2016; Hannibal et al, 2017)
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