Light modulates task-dependent thalamo-cortical connectivity during an auditory attentional task

Abstract

Exposure to blue wavelength light stimulates alertness and performance by modulating a widespread set of task-dependent cortical and subcortical areas. How light affects the crosstalk between brain areas to trigger this stimulating effect is not established. Here we record the brain activity of 19 healthy young participants (24.05±2.63; 12 women) while they complete an auditory attentional task in darkness or under an active (blue-enriched) or a control (orange) light, in an ultra-high-field 7 Tesla MRI scanner. We test if light modulates the effective connectivity between an area of the posterior associative thalamus, encompassing the pulvinar, and the intraparietal sulcus (IPS), key areas in the regulation of attention. We find that only the blue-enriched light strengthens the connection from the posterior thalamus to the IPS. To the best of our knowledge, our results provide the first empirical data supporting that blue wavelength light affects ongoing non-visual cognitive activity by modulating task-dependent information flow from subcortical to cortical areas.

Fig. 1. Activation and eigenvariate extraction from the two regions of interest (ROIs).

a The intraparietal sulcus (IPS). b The thalamus. Left: axial or coronal view showing brain areas activated during the appearance of deviant tones. The upper legend shows the t-values associated with the color map. Results are thresholded at p < 0.05 FDR-corrected. The blue arrow is pointing at either the bilateral intraparietal sulcus (peak MNI coordinates left hemisphere: [−40 −46 50], Z_score = 4.16, P_FDR-corr = 0.002; right hemisphere: [45 −30 51], Z_score = 3.47, P_FDR-corr = 0.008) or at the bilateral thalamus (peak MNI coordinates left hemisphere: [−16 −21 11], Z_score = 4.61, P_FDR-corr = 0.001; right hemisphere: [17 −20 12], Z_score = 4.45, P_FDR-corr = 0.002). Center: probabilistic ROIs across subjects overlapped onto the activation map for both ROIs. The color scale showed in the lower legend represents the proportion of subjects whose ROI included that node: the redder the color the higher the probability that the node is common across the subjects. Right: an example of the adjusted eigenvariate in both ROIs. c Thalamic probability maps on parcellation. Left: Zoom in of the thalamic probability maps overlapped onto an MRI-based parcellation of the thalamus in all three views. Right: Parcellation alone to fully show the nuclei encompassing our thalamic activation.

Fig. 2. Effective connectivity results and their relationship with pupillary response.

a–c PEB results of the DCM analysis at baseline, and under blue-enriched or orange light modulation, respectively. Left: matrices of the effective connectivity either at baseline (a) or with modulatory effects exerted by the active blue-enriched (b) or the control orange (c) light for either the left or the right hemisphere. Right: schematic representation of the corresponding matrices where IPS and the thalamus are showed in green and yellow respectively. On all panels, only suprathreshold parameters are shown (Pp > 0.95) whereas subthreshold parameters are marked as “n.s” (i.e., non-suprathreshold). Connections strengths are represented on a scale from turquoise to yellow, if excitatory, and from light to dark blue if inhibitory. Non modeled direct effects (i.e., whose priors were set to 0) are displayed in white. In the schematic representation, the line patterns denote whether the connection was significantly modulated compared to baseline: solid and dashed lines represent connections that were significantly modulated or not, respectively; red lines denote excitatory connections whereas black ones denote inhibitory connections. d Spearman correlation results. Spearman correlation between modulation exerted by blue-enriched light over the TH-IPS connection (referenced to baseline) across both hemispheres and the difference in pupil constriction in both lights exposures (r[9] = −0.82; p = 0.0037). Density plots for both variables are also provided in orange and red respectively.

Fig. 3. Graphical representation of the experimental protocol.

Participants came to the lab once for a structural MRI and then again, 7 days after, to perform a functional scan. During the 7 days, participants followed a loose sleep-wake schedule which was verified using wrist actigraphy. For the functional scan, participants were exposed to bright polychromatic light (~1000 lux) for 5 min prior to being maintained in dim light (<10 lux) for 45 min while they also trained for the auditory tasks to perform in the MRI. The tasks probed executive (n-back task), emotion processing and attention (oddball task) and were performed in the MRI for about 1 h 30 min. The present paper only discusses the oddball task where participants had to detect rare (25%) deviant tones (100 Hz; 500 ms, here represented as red) presented pseudo-randomly within a stream of more frequent (75%) standard (500 Hz; 500 ms, here represented as black) tones (interstimulus interval: 2 s). While performing the task, participants were exposed to 30s-blocks of active, blue-enriched cool polychromatic light (6500 K; 92 melanopic EDI lux) or control orange monochromatic light (5.28 × 10¹² photons/cm²/s; 590 nm, 10 nm at full width half maximum; 0.16 melanopic EDI lux) separated by ~15 s darkness periods (<0.01 lux). All icons in the figure were taken from Microsoft PowerPoint (https://www.microsoft.com) except the brain icon, which was taken from Wikimedia Commons freely licensed (https://en.wikipedia.org/wiki/File:Human_Brain_sketch_with_eyes_and_cerebrellum.svg).