[en] Light is a powerful modulator of cognition through its long-term effects on circadian rhythmicity and direct effects on brain function as identified by neuroimaging. How the direct impact of light on brain function varies with wavelength of light, circadian phase, and sleep homeostasis, and how this differs between individuals, is a largely unexplored area. Using functional MRI, we compared the effects of 1 minute of low-intensity blue (473 nm) and green light (527 nm) exposures on brain responses to an auditory working memory task while varying circadian phase and status of the sleep homeostat. Data were collected in 27 subjects genotyped for the PER3 VNTR (12 PER3(5/5) and 15 PER3(4/4) ) in whom it was previously shown that the brain responses to this task, when conducted in darkness, depend on circadian phase, sleep homeostasis, and genotype. In the morning after sleep, blue light, relative to green light, increased brain responses primarily in the ventrolateral and dorsolateral prefrontal cortex and in the intraparietal sulcus, but only in PER3(4/4) individuals. By contrast, in the morning after sleep loss, blue light increased brain responses in a left thalamofrontoparietal circuit to a larger extent than green light, and only so in PER3(5/5) individuals. In the evening wake maintenance zone following a normal waking day, no differential effect of 1 minute of blue versus green light was observed in either genotype. Comparison of the current results with the findings observed in darkness indicates that light acts as an activating agent particularly under those circumstances in which and in those individuals in whom brain function is jeopardized by an adverse circadian phase and high homeostatic sleep pressure.
Research center :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurology
Author, co-author :
Vandewalle, Gilles ; Université de Liège - ULiège > Centre de recherches du cyclotron
Archer, Simon N
Wuillaume, Catherine
Balteau, Evelyne ; Université de Liège - ULiège > Centre de recherches du cyclotron
Degueldre, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron
Luxen, André ; Université de Liège - ULiège > Centre de Recherches du Cyclotron > Chimie organique de synthèse
Dijk, Derk*-Jan
Maquet, Pierre ; Université de Liège - ULiège > Centre de recherches du cyclotron
Language :
English
Title :
Effects of light on cognitive brain responses depend on circadian phase and sleep homeostasis.
Publication date :
2011
Journal title :
Journal of Biological Rhythms
ISSN :
0748-7304
eISSN :
1552-4531
Publisher :
SAGE Science Press, United States - California
Volume :
26
Issue :
3
Pages :
249-59
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
GR069714MA; Inter-university Attraction Poles (PAI/IAP) P6/29
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] FMRE - Fondation Médicale Reine Elisabeth [BE] Wellcome Trust [GB] BBSRC - Biotechnology and Biological Sciences Research Council [GB]
Altimus CM, Guler AD, Alam NM, Arman AC, Prusky GT, Sampath AP, and Hattar S. (2010) Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci 13: 1107-1112.
Altimus CM, Guler AD, Villa KL, McNeill DS, Legates TA, and Hattar S. (2008) Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc Natl Acad Sci U S A 105: 19998-20003.
Archer SN, Robilliard DL, Skene DJ, Smits M., Williams A., Arendt J., and von Schantz M. (2003) A length polymorphism in the circadian clock gene Per3 is linked to delayed sleep phase syndrome and extreme diurnal preference. Sleep 26: 413-415. (Pubitemid 39610658)
Badia P., Myers B., Boecker M., Culpepper J., and Harsh JR (1991) Bright light effects on body temperature, alertness, EEG and behavior. Physiol Behav 50: 583-588.
Burgess HJ (2010) Partial sleep deprivation reduces phase advances to light in humans. J Biol Rhythms 25: 460-468.
Cabeza R. and Nyberg L. (2000) Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12: 1-47. (Pubitemid 30142782)
Cajochen C. (2007) Alerting effects of light. Sleep Med Rev 11: 453-464. (Pubitemid 350087714)
Cajochen C., Munch M., Kobialka S., Krauchi K., Steiner R., Oelhafen P., Orgul S., and Wirz-Justice A. (2005) High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light. J Clin Endocrinol Metab 90: 1311-1316. (Pubitemid 40463981)
Chee MW and Chuah LY (2008) Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Curr Opin Neurol 21: 417-423.
Cohen DA, Wang W., Wyatt JK, Kronauer RE, Dijk DJ, Czeisler CA, and Klerman EB (2010) Uncovering residual effects of chronic sleep loss on human performance. Sci Transl Med 2: 14ra13.
Conway BR (2009) Color vision, cones, and color-coding in the cortex. Neuroscientist 15: 274-290.
Corbetta M. and Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3: 201-215. (Pubitemid 135706590)
Dijk DJ and Archer SN (2010) PERIOD3, circadian phenotypes, and sleep homeostasis. Sleep Med Rev 14: 151-160.
Dijk DJ, Duffy JF, and Czeisler CA (1992) Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res 1: 112-117.
Drummond SP and Brown GG (2001) The effects of total sleep deprivation on cerebral responses to cognitive performance. Neuropsychopharmacology 25: S68 - S73.
Duffy JF and Czeisler CA (2009) Effect of light on human circadian physiology. Sleep Med Clin 4: 165-177.
Gooley JJ, Rajaratnam SM, Brainard GC, Kronauer RE, Czeisler CA, and Lockley SW (2010) Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci Transl Med 2: 31ra33.
Groeger JA, Viola AU, Lo JC, von Schantz M., Archer SN, and Dijk DJ (2008) Early morning executive functioning during sleep deprivation is compromised by a PERIOD3 polymorphism. Sleep 31: 1159-1167.
Hatori M. and Panda S. (2010) The emerging roles of melanopsin in behavioral adaptation to light. Trends Mol Med 16: 435-446.
Hill S., Tononi G., and Ghilardi MF (2008) Sleep improves the variability of motor performance. Brain Res Bull 76: 605-611.
Koechlin E. and Hyafil A. (2007) Anterior prefrontal function and the limits of human decision-making. Science 318: 594-598. (Pubitemid 350014799)
Lall GS, Revell VL, Momiji H., Al Enezi J., Altimus CM, Guler AD, Aguilar C., Cameron MA, Allender S., Hankins MW, and Lucas RJ (2010) Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 66: 417-428.
Lockley SW, Evans EE, Scheer Fajl, Brainard GC, Czeisler CA, and Aeschbach D. (2006) Short-wavelength sensitivity for the direct effects of light on alertness, vigilance, and the waking electroencephalogram in humans. Sleep 29: 161-168. (Pubitemid 44019969)
Lupi D., Oster H., Thompson S., and Foster RG (2008) The acute light-induction of sleep is mediated by OPN4-based photoreception. Nat Neurosci 11: 1068-1073.
Mu Q., Mishory A., Johnson KA, Nahas Z., Kozel FA, Yamanaka K., Bohning DE, and George MS (2005) Decreased brain activation during a working memory task at rested baseline is associated with vulnerability to sleep deprivation. Sleep 28: 433-446. (Pubitemid 40489838)
Palmer SE and Schloss KB (2010) An ecological valence theory of human color preference. Proc Natl Acad Sci U S A 107: 8877-8882.
Ruger M., Gordijn MC, Beersma DG, de Vries B., and Daan S. (2006) Time-of-day-dependent effects of bright light exposure on human psychophysiology: comparison of daytime and nighttime exposure. Am J Physiol Regul Integr Comp Physiol 290: R1413 - R1420.
Schmidt C., Collette F., Cajochen C., and Peigneux P. (2007) A time to think: circadian rhythms in human cognition. Cogn Neuropsychol 24: 755-789. (Pubitemid 350239082)
Shipp S. (2004) The brain circuitry of attention. Trends Cogn Sci 8: 223-230. (Pubitemid 38543252)
Tsai JW, Hannibal J., Hagiwara G., Colas D., Ruppert E., Ruby NF, Heller HC, Franken P., and Bourgin P. (2009) Melanopsin as a sleep modulator: circadian gating of the direct effects of light on sleep and altered sleep homeostasis in Opn4(-/-) mice. PLoS Biol 7: e1000125.
van der Veen DR and Archer SN (2010) Light-dependent behavioral phenotypes in PER3-deficient mice. J Biol Rhythms 25: 3-8.
Van Dongen HP, Baynard MD, Maislin G., and Dinges DF (2004) Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep 27: 423-433. (Pubitemid 44138802)
Vandewalle G., Archer SN, Wuillaume C., Balteau E., Degueldre C., Luxen A., Maquet P., and Dijk DJ (2009 a) Functional magnetic resonance imaging-assessed brain responses during an executive task depend on interaction of sleep homeostasis, circadian phase, and PER3 genotype. J Neurosci 29: 7948-7956.
Vandewalle G., Balteau E., Phillips C., Degueldre C., Moreau V., Sterpenich V., Albouy G., Darsaud A., Desseilles M., Dang-Vu TT, et al. (2006) Daytime light exposure dynamically enhances brain responses. Curr Biol 16: 1616-1621. (Pubitemid 44233267)
Vandewalle G., Gais S., Schabus M., Balteau E., Carrier J., Darsaud A., Sterpenich V., Albouy G., Dijk DJ, and Maquet P. (2007 a) Wavelength-dependent modulation of brain responses to a working memory task by daytime light exposure. Cereb Cortex 17: 2788-2795. (Pubitemid 350129439)
Vandewalle G., Maquet P., and Dijk DJ (2009 b) Light as a modulator of cognitive brain function. Trends Cogn Sci 13: 429-438.
Vandewalle G., Schmidt C., Albouy G., Sterpenich V., Darsaud A., Rauchs G., Berken PY, Balteau E., Degueldre C., Luxen A., et al. (2007 b) Brain responses to violet, blue, and green monochromatic light exposures in humans: prominent role of blue light and the brainstem. PLoS One 2: e1247.
Vandewalle G., Schwartz S., Grandjean D., Wuillaume C., Balteau E., Degueldre C., Schabus M., Phillips C., Luxen A., Dijk DJ, and Maquet P. (2010) Spectral quality of light modulates emotional brain responses in humans. Proc Natl Acad Sci U S A 107: 19549-19554.
Viola AU, Archer SN, James LM, Groeger JA, Lo JC, Skene DJ, von Schantz M., and Dijk DJ (2007) PER3 polymorphism predicts sleep structure and waking performance. Curr Biol 17: 613-618. (Pubitemid 46497792)
Wyatt JK, Ritz-De Cecco A., Czeisler CA, and Dijk DJ (1999) Circadian temperature and melatonin rhythms, sleep, and neurobehavioral function in humans living on a 20-h day. Am J Physiol 277: R1152 - R1163.