Photic memory for executive brain responses

Abstract

Light is a powerful stimulant for human alertness and cognition, presumably acting through a photoreception system that heavily relies on the photopigment melanopsin. In humans, evidence for melanopsin involvement in light-driven cognitive stimulation remains indirect, due to the difficulty to selectively isolate its contribution. Therefore, a role for melanopsin in human cognitive regulation remains to be established. Here, sixteen participants underwent consecutive and identical functional MRI recordings, during which they performed a simple auditory detection task and a more difficult auditory working memory task, while continuously exposed to the same test light (515 nm). We show that the impact of test light on executive brain responses depends on the wavelength of the light to which individuals were exposed prior to each recording. Test-light impact on executive responses in widespread prefrontal areas and in the pulvinar increased when the participants had been exposed to longer (589 nm), but not shorter (461 nm), wavelength light, more than 1 h before. This wavelength-dependent impact of prior light exposure is consistent with recent theories of the light-driven melanopsin dual states. Our results emphasize the critical role of light for cognitive brain responses and are, to date, the strongest evidence in favor of a cognitive role for melanopsin, which may confer a form of "photic memory" to human cognitive brain function.

Keywords: fMRI; non–image-forming.

Fig. 1.

Experimental protocol. (A) Enlarged view of an experimental run, which started with 10-min exposure to an adaptation light, which could be of shorter (blue, 461 nm), intermediate (green, 515 nm), or longer (orange, 589 nm) wavelength (balanced order across subjects; constant irradiance, 6 × 10¹³ photons⋅cm⁻²⋅s⁻¹). Adaptation light was administered in the MR scanner, while participants performed auditory n-back tasks (0-back and 3-back) to modulate subsequent impact of the test light on brain activity. Afterwards, participants were kept in darkness (blindfolded outside the MR scanner) for 70 min to allow for complete readaptation of rods and cones. Test light (515 nm; constantly changing irradiance) (see Materials and Methods and SI Materials and Methods) was then administered for 15 min in the MR scanner, while participants performed auditory n-back tasks (0-back and 3-back). (B) Schematic diagram of the entire study protocol (time relative to clock time, in hours). Order of adaptation-light wavelength was balanced across subjects. The white arrows indicate the predicted impact of the adaptation light on the subsequent impact of the test light.

Fig. 2.

Impact of the test light on executive brain responses depends on prior light. Orange blobs represent brain areas showing increased test-light impact after prior orange-light relative to prior blue-light exposure. Green blobs represent brain areas showing increased test-light impact after prior green-light relative to prior blue-light exposure (green arrows highlight these areas). Yellow blobs represent brain areas showing increased test-light impact after prior orange-light relative to prior green-light exposure (yellow arrows highlight these areas). Graphs show activity estimates of test-light impact on executive responses [3-back to 0-back; arbitrary units (a.u.); mean ± SEM] in the different brain areas after exposure to blue, green, and orange light. The numbers of the graphs correspond to brain locations on the central panels (as in Table 1). Graphs 1 and 2, left and right DLPFC; graph 3, left VLPFC; graph 4, left amygdala; graphs 5 and 6, left and right pulvinar; graph 7, substantia nigra; graphs 8 and 9, left and right fusiform gyrus; graph 10, cerebellum. *P < 0.05 corrected for multiple comparisons.