Spectral quality of light modulates emotional brain responses in humans

Abstract

Light therapy can be an effective treatment for mood disorders, suggesting that light is able to affect mood state in the long term. As a first step to understand this effect, we hypothesized that light might also acutely influence emotion and tested whether short exposures to light modulate emotional brain responses. During functional magnetic resonance imaging, 17 healthy volunteers listened to emotional and neutral vocal stimuli while being exposed to alternating 40-s periods of blue or green ambient light. Blue (relative to green) light increased responses to emotional stimuli in the voice area of the temporal cortex and in the hippocampus. During emotional processing, the functional connectivity between the voice area, the amygdala, and the hypothalamus was selectively enhanced in the context of blue illumination, which shows that responses to emotional stimulation in the hypothalamus and amygdala are influenced by both the decoding of vocal information in the voice area and the spectral quality of ambient light. These results demonstrate the acute influence of light and its spectral quality on emotional brain processing and identify a unique network merging affective and ambient light information.

Fig. 1.

Experimental design. (A) General protocol. Arrow indicates pupil dilator administration. Time relative to scheduled wake time (h). T1 (task 1): first fMRI task, consisting of a gender discrimination of auditory vocalizations while exposed to alternating blue and green monochromatic ambient light (see B for details). T2 (task 2): second fMRI task (voice localizer); its main aim was to identify the voice-sensitive area of the temporal cortex. Participants performed a 1-back task with the voice stimuli from task 1 (anger and neutral pseudoword) and nonvoice white-noise auditory stimuli replicating the envelope (EN) or the mean of the fundamental (F0) of the original voice stimuli from task 1. T3 (task 3): emotional judgment task performed outside the MRI scanner, in which the emotions of all of the auditory stimuli presented in T1 were evaluated by the participants on a five-item Likert scale. (B) Detailed experimental procedures of the gender discrimination task (T1). Time (s) relative to t0, a time point arbitrarily chosen as a blue light onset of the session. Monochromatic [blue (473 nm) or green (427 nm)] ambient light exposures lasted 40 s and were separated by 15- to 25-s periods of darkness (mean duration, 20 s). Anger (red bars) and neutral (white bars) prosody vocalizations (meaningless word-like sounds; half neutral, half anger) were pseudorandomly and evenly administered in each light condition throughout the entire session (interstimuli interval, 3–11 s; mean, 4.8 s).

Fig. 2.

Behavioral results. (A) Accuracy for the gender discrimination task (task 1) (mean ± SD). (B) Reaction times during the gender discrimination task (task 1) (mean ± SD). (C) Emotional judgment of the neutral and anger voice stimuli made by the subjects during task 3 (i.e., after the fMRI procedure and outside the MRI scanner) (mean ± SD). *P ≤ 0.001.

Fig. 3.

Differences in responses to blue and green light onsets in the right amygdala. (A) Statistical results for the blue > green onset contrast modulated by time, overlaid on the population mean structural image (P_uncorrected < 0.001). (B) Mean activity estimates [arbitrary units (a.u.) ± SEM] of the constant component of the brain responses associated with blue and green light onsets across the entire session; difference between conditions is nonsignificant (ns). (C) Estimates of the linear change component (a.u. ± SEM) of the brain responses associated with blue and green light onsets across the entire session, showing a significant (*) negative component for blue light onsets, suggesting an adaptation of amygdala responses with time. (D) Composite of both components showing the evolution of the responses to the 12 blue and green light onsets of the session.

Fig. 4.

Impact of the the wavelength of the ambient illumination context on the brain processing of emotional auditory stimuli. (A) Significant differences between blue and green monochromatic ambient light exposures in the modulation of the brain responses associated with anger prosody stimuli. Yellow lines indicate voice-sensitive regions activated during the voice localizer (task 2). Dotted lines refer to the functional connectivity analysis (see C). Statistical results are overlaid to the population mean structural image (P_uncorrected < 0.001). 1, left hippocampus; 2, right hippocampus; 3, left superior temporal gyrus; 4, right superior temporal gyrus. (B) Mean activity estimates [arbitrary units (a.u.) ± SEM] of the brain responses associated with anger prosody during blue and green ambient illumination contexts. (C) Increased functional connectivity with voice-sensitive regions for anger prosody under blue vs. green monochromatic ambient light exposure. Dashed lines/circles indicate higher functional connectivity between left superior temporal gyrus and (5) the left amygdala and (6) the hypothalamus (anterior to the mammilary bodies, posterior to the infundibulum) under blue relative to green ambient light exposure, and increased functional connectivity between the right superior temporal gyrus and (6) the hypothalamus (anterior to the mammillary bodies, posterior to the infundibulum) under blue but not under green ambient light.