Plasticity in the Sensitivity to Light in Aging: Decreased Non-visual Impact of Light on Cognitive Brain Activity in Older Individuals but No Impact of Lens Replacement

Abstract

Beyond its essential visual role, light, and particularly blue light, has numerous non-visual effects, including stimulating cognitive functions and alertness. Non-visual effects of light may decrease with aging and contribute to cognitive and sleepiness complaints in aging. However, both the brain and the eye profoundly change in aging. Whether the stimulating effects light on cognitive brain functions varies in aging and how ocular changes may be involved is not established. We compared the impact of blue and orange lights on non-visual cognitive brain activity in younger (23.6 ± 2.5 years), and older individuals with their natural lenses (NL; 66.7 ± 5.1 years) or with intraocular lens (IOL) replacement following cataract surgery (69.6 ± 4.9 years). Analyses reveal that blue light modulates executive brain responses in both young and older individuals. Light effects were, however, stronger in young individuals including in the hippocampus and frontal and cingular cortices. Light effects did not significantly differ between older-IOL and older-NL while regression analyses indicated that differential brain engagement was not underlying age-related differences in light effects. These findings show that, although its impact decreases, light can stimulate cognitive brain activity in aging. Since lens replacement did not affect light impact, the brain seems to adapt to the progressive decrease in retinal light exposure in aging.

Keywords: aging; circadian; cognition; lens; light; melanopsin; non-visual impact of light.

FIGURE 1

Experimental protocol. Upper panel: participants were maintained in dim light after admission (1.5 h after their habitual waketime). They completed two fMRI sessions under light exposure in a counterbalanced order (blue light 480 nm, 3 × 10ˆ13 ph/cm/s² – orange light 620 nm, 3 × 10ˆ13 ph/cm/s²). The total duration of each session was 40 min during which participants performed an auditory n-back task. Upon arrival (baseline) and after each fMRI session, the pupils were measured. Pupils were dilated before, and right after, the first fMRI session (e.g., before second fMRI session). Subjective sleepiness and anxiety levels were also collected. Participants were exposed for 5 min to a bright polychromatic white light (1000 lux) before each fMRI session. Lower panels: within an fMRI session (i.e., including either blue or orange light), light was administered in block of 30 s and coincided with the 30 s task blocks (either 0b or 2b) or were administered alone. All blocks were separated by at least 15 s in complete darkness without task, which was either followed by a 30 s light exposure or a 30 s period in darkness. A total of 48 blocks of auditory 0b task (n = 18), 2b task (n = 20), and rest under light exposure (n = 10) were performed in each fMRI session. Half of n-back task blocks were executed under light exposure and the other half in darkness.

FIGURE 2

Behavioral results. For each panel (A–E), results represent mean ± standard error of the mean (SEM) for both light conditions. (A) Score on the Karolinska (KSS) sleepiness scale before the fMRI session. (B) Score on the State Anxiety questionnaire (STAI-S) after each fMRI session. (C) Dilated absolute pupil size (mm) after each fMRI session. (D) Accuracy on the 2b and 0b tasks when all subjects are pooled together. (E) Response time to 2b and 0b tasks when all subjects are pooled together;^∗ indicates significant differences between groups or light conditions.

FIGURE 3

Brain responses to the n-back tasks [2b-0b] irrespective of the light conditions. Statistical results (P < 0.05 FWE-whole brain) overlay the mean structural image of all participants. Significant responses to the task common to all groups are displayed in green while group differences (older-nl and older-iol > younger; younger > older-nl and older-iol) are in yellow. See Table 2 for brain regions corresponding to the letters and abbreviations. Right panels show activity estimates (arbitrary unit – a.u. ± SEM) for each brain region. ^∗ Significant group differences P < 0.05 corrected FWE-whole brain.

FIGURE 4

Effect of [(2b-0b)blue – (2b-0b)orange] on brain responses in young, older-nl, and older-iol subjects. Statistical results (P < 0.001 uncorrected) overlay the mean structural image of all participants. Responses to light are displayed in green for all subjects pooled together, whereas group differences (young > older-nl and older-iol) are displayed in yellow. Right panels show activity estimates (a.u. ± SEM) for each brain region. See Table 3 for brain regions corresponding to the letters and abbreviations. ^∗ Significant group differences P < 0.05 corrected for multiple comparisons over small volumes of interest taken a priori location based on the literature.