Exposure to Blue Wavelength Light Is Associated With Increases in Bidirectional Amygdala-DLPFC Connectivity at Rest

Anna Alkozei, Natalie S Dailey, Sahil Bajaj, John R Vanuk, Adam C Raikes, William D S Killgore, Anna Alkozei, Natalie S Dailey, Sahil Bajaj, John R Vanuk, Adam C Raikes, William D S Killgore

Abstract

Blue wavelength light has been used successfully as a treatment method for certain mood disorders, but, the underlying mechanisms behind the mood enhancing effects of light remain poorly understood. We investigated the effects of a single dose of 30 min of blue wavelength light (n = 17) vs. amber wavelength light (n = 12) exposure in a sample of healthy adults on subsequent resting-state functional and directed connectivity, and associations with changes in state affect. Individuals who received blue vs. amber wavelength light showed greater positive connectivity between the right amygdala and a region within the left dorsolateral prefrontal cortex (DLPFC). In addition, using granger causality, the findings showed that individuals who received blue wavelength light displayed greater bidirectional information flow between these two regions relative to amber light. Furthermore, the strength of amygdala-DLPFC functional connectivity was associated with greater decreases in negative mood for the blue, but not the amber light condition. Blue light exposure may positively influence mood by modulating greater information flow between the amygdala and the DLPFC, which may result in greater engagement of cognitive control strategies that are needed to perceive and regulate arousal and mood.

Keywords: PFC; amygdala; depression; fMRI; light therapy; neuroimaging.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Alkozei, Dailey, Bajaj, Vanuk, Raikes and Killgore.

Figures

Figure 1
Figure 1
(A) PANAS positive affect (PANAS-P) and (B) negative affect (PANAS-N) scores from pre-light and post-light exposure for both groups.
Figure 2
Figure 2
Blue light led to increased functional connectivity between the right amygdala and a region within the left dorsolateral prefrontal cortex. Displayed is the significant cluster of voxels (x = −24, y = 46, z = 18, k = 90, volume p-FDR corrected, p < 0.001) from the seed-to-voxel analysis using the right amygdala as the seed region.
Figure 3
Figure 3
Granger Causality (GC)-frequency spectra for (A) feed-forward [right amygdala (R. AMG) to left DLPFC (L. DLPFC)] and (B) feed-backward (L. DLPFC to R. AMG) connections for the amber and blue light groups. The green dotted line here represents the threshold chosen for significant GC strength (~0.0422 at p < 0.0025, permutation test).
Figure 4
Figure 4
Here we are presenting the correlation between raw amygdala-DLPFC connectivity values and raw changes in PANAS negative affect (PANAS-N) scores from pre- to post-light exposure for the blue vs. amber groups (Greater negative values on the PANAS-N change scores indicate greater reduction in negative affect over time). We decided to present the raw scores rather than the Spearman rank order correlation for ease of interpretation, however we have included the trendlines for each group from the original analysis. The figure shows that increased functional connectivity between the amygdala and DLPFC was monotonically associated with reduced PANAS-N scores for the blue light group (ρ = −0.55, p = 0.03) but not the amber light group (ρ = −0.18, p = 0.55).

References

    1. Beecher ME, Eggett D, Erekson D, Rees LB, Bingham J, Klundt J, et al. . Sunshine on my shoulders: weather, pollution, and emotional distress. J Affect Disord. (2016) 205:234–8. 10.1016/j.jad.2016.07.021
    1. Guéguen N, Lamy L. Weather and helping: additional evidence of the effect of the sunshine Samaritan. J Soc Psychol. (2013) 153:123–6. 10.1080/00224545.2012.720618
    1. Maruani J, Geoffroy PA. Bright light as a personalized precision treatment of mood disorders. Front Psychiatry. (2019) 10:85. 10.3389/fpsyt.2019.00085
    1. Killgore WDS. Lightening the mood: evidence for blue light exposure in the treatment of post-concussion depression. Expert Rev Neurother. (2020) 20:1081–3. 10.1080/14737175.2020.1814147
    1. Aan Het Rot M, Miloserdov K, Buijze ALF, Meesters Y, Gordijn MCM. Premenstrual mood and empathy after a single light therapy session. Psychiatry Res. (2017) 256:212–8. 10.1016/j.psychres.2017.06.052
    1. Cajochen C, Munch M, Kobialka S, Kräuchi K, Steiner R, Oelhafen P, et al. . High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light. J Clin Endocrinol Metab. (2005) 90:1311–6. 10.1210/jc.2004-0957
    1. Phipps-Nelson J, Redman JR, Schlangen LJ, Rajaratnam SM. Blue light exposure reduces objective measures of sleepiness during prolonged nighttime performance testing. Chronobiol Int. (2009) 26:891–912. 10.1080/07420520903044364
    1. Alkozei A, Smith R, Pisner D, Vanuk JR, Markowski SM, Fridman A, et al. . Exposure to blue light increases subsequent functional activation of the prefrontal cortex during performance of a working memory task. Sleep. (2016) 39:1671–80. 10.5665/sleep.6090
    1. Alkozei A, Smith R, Dailey NS, Bajaj S, Killgore WDS. Acute exposure to blue wavelength light during memory consolidation improves verbal memory performance. PLoS ONE. (2017) 12:e0184884. 10.1371/journal.pone.0184884
    1. Even C, Schröder CM, Friedman S, Rouillon F. Efficacy of light therapy in nonseasonal depression: a systematic review. J Affect Disord. (2008) 108:11–23. 10.1016/j.jad.2007.09.008
    1. Glickman G, Byrne B, Pineda C, Hauck WW, Brainard GC. Light therapy for seasonal affective disorder with blue narrow-band light-emitting diodes (LEDs). Biol Psychiatry. (2006) 59:502–7. 10.1016/j.biopsych.2005.07.006
    1. Perera S, Eisen R, Bhatt M, Bhatnagar N, de Souza R, Thabane L, et al. . Light therapy for non-seasonal depression: systematic review and meta-analysis. Br J Psychiatry Open. (2016) 2:116–26. 10.1192/bjpo.bp.115.001610
    1. Strong RE, Marchant BK, Reimherr FW, Williams E, Soni P, Mestas R. Narrow-band blue-light treatment of seasonal affective disorder in adults and the influence of additional nonseasonal symptoms. Depress Anxiety. (2009) 26:273–8. 10.1002/da.20538
    1. Lack L, Bramwell T, Wright H, Kemp K. Morning blue light can advance the melatonin rhythm in mild delayed sleep phase syndrome. Sleep Biol Rhythms. (2007) 5:78–80. 10.1111/j.1479-8425.2006.00250.x
    1. Killgore WDS, Vanuk JR, Shane BR, Weber M, Bajaj S. A randomized, double-blind, placebo-controlled trial of blue wavelength light exposure on sleep and recovery of brain structure, function, and cognition following mild traumatic brain injury. Neurobiol Dis. (2020) 134:104679. 10.1016/j.nbd.2019.104679
    1. Raikes AC, Dailey NS, Shane BR, Forbeck B, Alkozei A, Killgore WDS. Daily morning blue light therapy improves daytime sleepiness, sleep quality, and quality of life following a mild traumatic brain injury. J Head Trauma Rehabil. (2020) 35:E405–21. 10.1097/HTR.0000000000000579
    1. Raikes AC, Dailey NS, Forbeck B, Alkozei A, Killgore WDS. Daily morning blue light therapy for post-mTBI sleep disruption: effects on brain structure and function. Front Neurol. (2021) 12:625431. 10.3389/fneur.2021.625431
    1. Sinclair KL, Ponsford JL, Taffe J, Lockley SW, Rajaratnam SM. Randomized controlled trial of light therapy for fatigue following traumatic brain injury. Neurorehabil Neural Repair. (2014) 28:303–13. 10.1177/1545968313508472
    1. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. (2002) 295:1070–3. 10.1126/science.1067262
    1. Dijk DJ, Archer SN. Light, sleep, and circadian rhythms: together again. PLoS Biol. (2009) 7:1221. 10.1371/journal.pbio.1000145
    1. Cajochen C. Alerting effects of light. Sleep Med Rev. (2007) 11:453–64. 10.1016/j.smrv.2007.07.009
    1. Chellappa SL, Steiner R, Blattner P, Oelhafen P, Götz T, Cajochen C. Non-visual effects of light on melatonin, alertness and cognitive performance: can blue-enriched light keep us alert. PLoS ONE. (2011) 6:e16429. 10.1371/journal.pone.0016429
    1. Pandi-Perumal SR, Smits M, Spence W, Srinivasan V, Cardinali DP, Lowe AD, et al. . Dim light melatonin onset (DLMO): a tool for the analysis of circadian phase in human sleep and chronobiological disorders. Prog Neuropsychopharmacol Biol Psychiatry. (2007) 31:1–11. 10.1016/j.pnpbp.2006.06.020
    1. Chesson AL, Jr, Littner M, Davila D, Anderson WM, Grigg-Damberger M, et al. . Practice parameters for the use of light therapy in the treatment of sleep disorders. Standards of Practice Committee, American Academy of Sleep Medicine. Sleep. (1999) 22:641–60. 10.1093/sleep/22.5.641
    1. Pail G, Huf W, Pjrek E, Winkler D, Willeit M, Praschak-Rieder N, et al. . Bright-light therapy in the treatment of mood disorders. Neuropsychobiology. (2011) 64:152–62. 10.1159/000328950
    1. Rautkyä E, Puolakka M, Halonen L. Alerting effects of daytime light exposure–a proposed link between light exposure and brain mechanisms. Light Res Technol. (2011) 44:238–52. 10.1177/1477153511409294
    1. Mick G, Cooper H, Magnin M. Retinal projection to the olfactory tubercle and basal telencephalon in primates. J Compar Neurol. (1993) 327:205–19. 10.1002/cne.903270204
    1. Johnson RF, Morin LP, Moore RY. Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res. (1988) 462:301–12. 10.1016/0006-8993(88)90558-6
    1. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, et al. . Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol. (2006) 497:326–49. 10.1002/cne.20970
    1. Morin LP, Studholme KM. Retinofugal projections in the mouse. J Compar Neurol. (2014) 522:3733–53. 10.1002/cne.23635
    1. Vandewalle G, Schmidt C, Albouy G, Sterpenich V, Darsaud A, Rauchs G, et al. . Brain responses to violet, blue, and green monochromatic light exposures in humans: prominent role of blue light and the brainstem. PLoS ONE. (2007) 2:e1247. 10.1371/journal.pone.0001247
    1. Vandewalle G, Schwartz S, Grandjean D, Wuillaume C, Balteau E, Degueldre C, et al. . Spectral quality of light modulates emotional brain responses in humans. Proc Natl Acad Sci USA. (2010) 107:19549–54. 10.1073/pnas.1010180107
    1. Fisher PM, Madsen MK, Mc Mahon B, Holst KK, Andersen SB, Laursen HR, et al. . Three-week bright-light intervention has dose-related effects on threat-related corticolimbic reactivity and functional coupling. Biol Psychiatry. (2014) 76:332–9. 10.1016/j.biopsych.2013.11.031
    1. Tang Y, Kong L, Wu F, Womer F, Jiang W, Cao Y, et al. . Decreased functional connectivity between the amygdala and the left ventral prefrontal cortex in treatment-naive patients with major depressive disorder: a resting-state functional magnetic resonance imaging study. Psychol Med. (2013) 43:1921–7. 10.1017/S0033291712002759
    1. Cullen KR, Westlund MK, Klimes-Dougan B, Mueller BA, Houri A, Eberly LE, et al. . Abnormal amygdala resting-state functional connectivity in adolescent depression. JAMA Psychiatry. (2014) 71:1138–47. 10.1001/jamapsychiatry.2014.1087
    1. Kaiser RH, Andrews-Hanna JR, Wager TD, Pizzagalli DA. Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry. (2015) 72:603–11. 10.1001/jamapsychiatry.2015.0071
    1. Alkozei A, Smith R, Killgore WD. Exposure to blue wavelength light modulates anterior cingulate cortex activation in response to ‘uncertain' versus ‘certain' anticipation of positive stimuli. Neurosci Lett. (2016) 616:5–10. 10.1016/j.neulet.2016.01.034
    1. Killgore WDS, Dailey NS, Raikes AC, Vanuk JR, Taylor E, Alkozei A. Blue light exposure enhances neural efficiency of the task positive network during a cognitive interference task. Neurosci Lett. (2020) 735:135242. 10.1016/j.neulet.2020.135242
    1. Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol. (1988) 54:1063. 10.1037/0022-3514.54.6.1063
    1. Crawford JR, Henry JD. The Positive and Negative Affect Schedule (PANAS): Construct validity, measurement properties and normative data in a large non-clinical sample. Br J Clin Psychol. (2004) 43:245–65. 10.1348/0144665031752934
    1. Whitfield-Gabrieli S, Nieto-Castanon A. Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. (2012) 2:125–41. 10.1089/brain.2012.0073
    1. Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage. (2007) 37:90–101. 10.1016/j.neuroimage.2007.04.042
    1. Chai XJ, Castañón AN, Öngür D, Whitfield-Gabrieli S. Anticorrelations in resting state networks without global signal regression. Neuroimage. (2012) 59:1420–8. 10.1016/j.neuroimage.2011.08.048
    1. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. . Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. (2002) 15:273–89. 10.1006/nimg.2001.0978
    1. Dhamala M, Rangarajan G, Ding M. Analyzing information flow in brain networks with nonparametric Granger causality. Neuroimage. (2008) 41:354–62. 10.1016/j.neuroimage.2008.02.020
    1. Dhamala M, Rangarajan G, Ding M. Estimating Granger causality from fourier and wavelet transforms of time series data. Phys Rev Lett. (2008) 100:018701. 10.1103/PhysRevLett.100.018701
    1. Vandewalle G, Maquet P, Dijk DJ. Light as a modulator of cognitive brain function. Trends Cogn Sci. (2009) 13:429–38. 10.1016/j.tics.2009.07.004
    1. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception II: implications for major psychiatric disorders. Biol Psychiatry. (2003) 54:515–28. 10.1016/S0006-3223(03)00171-9
    1. Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ. Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci. (2007) 27:8877–84. 10.1523/JNEUROSCI.2063-07.2007
    1. Cheng W, Rolls ET, Qiu J, Xie X, Lyu W, Li Y, et al. . Functional connectivity of the human amygdala in health and in depression. Soc Cogn Affect Neurosci. (2018) 13:557–68. 10.1093/scan/nsy032
    1. Connolly CG, Ho TC, Blom EH, LeWinn KZ, Sacchet MD, Tymofiyeva O, et al. . Resting-state functional connectivity of the amygdala and longitudinal changes in depression severity in adolescent depression. J Affect Disord. (2017) 207:86–94. 10.1016/j.jad.2016.09.026
    1. Ramasubbu R, Konduru N, Cortese F, Bray S, Gaxiola I, Goodyear B. Reduced intrinsic connectivity of amygdala in adults with major depressive disorder. Front Psychiatry. (2014) 5:17. 10.3389/fpsyt.2014.00017
    1. Liu J, Fang J, Wang Z, Rong P, Hong Y, Fan Y, et al. . Transcutaneous vagus nerve stimulation modulates amygdala functional connectivity in patients with depression. J Affect Disord. (2016) 205:319–26. 10.1016/j.jad.2016.08.003
    1. Woody ML, Gibb BE. Integrating NIMH research domain criteria (RDoC) into depression research. Curr Opin Psychol. (2015) 4:6–12. 10.1016/j.copsyc.2015.01.004
    1. Kawamura A, Yoshiike T, Yoshimura A, Koizumi H, Nagao K, Fujii Y, et al. . Bright light exposure augments cognitive behavioral therapy for panic and posttraumatic stress disorders: a pilot randomized control trial. Sleep Biol Rhythms. (2019) 18:1–7. 10.1007/s41105-019-00248-7
    1. Yoshiike T, Honma M, Yamada N, Kim Y, Kuriyama K. Effects of bright light exposure on human fear conditioning, extinction, and associated prefrontal activation. Physiol Behav. (2018) 194:268–76. 10.1016/j.physbeh.2018.06.015
    1. Do MTH, Yau KW. Intrinsically photosensitive retinal ganglion cells. Physiol Rev. (2010) 162:59–90. 10.1152/physrev.00013.2010
    1. Lawson RP, Nord CL, Seymour B, Thomas DL, Dayan P, Pilling S, et al. . Disrupted habenula function in major depression. Mol Psychiatry. (2017) 22:202–8. 10.1038/mp.2016.81
    1. Huang LU, Xi Y, Peng Y, Yang Y, Huang X, Fu Y, et al. . A visual circuit related to habenula underlies the antidepressive effects of light therapy. Neuron. (2019) 102:128–42. 10.1016/j.neuron.2019.01.037
    1. Vandewalle G, Hébert M, Beaulieu C, Richard L, Daneault V, Garon ML, et al. . Abnormal hypothalamic response to light in seasonal affective disorder. Biol Psychiatry. (2011) 70:954–61. 10.1016/j.biopsych.2011.06.022
    1. Willeit M, Sitte HH, Thierry N, Michalek K, Praschak-Rieder N, Zill P, et al. . Enhanced serotonin transporter function during depression in seasonal affective disorder. Neuropsychopharmacology. (2008) 33:1503. 10.1038/sj.npp.1301560
    1. Eklund A, Nichols TE, Knutsson H. Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci USA. (2016) 113:7900–5. 10.1073/pnas.1602413113

Source: PubMed

3
Sottoscrivi