circadian rhythms; functional magnetic resonance imaging; human cognition; light exposure; melanopsin; Cerebral Cortex/physiology/radiation effects; Cognition/physiology/radiation effects; Radiation Dosage; Sunlight
Abstract :
[en] In addition to classical visual effects, light elicits nonvisual brain responses, which profoundly influence physiology and behavior. These effects are mediated in part by melanopsin-expressing light-sensitive ganglion cells that, in contrast to the classical photopic system that is maximally sensitive to green light (550 nm), is very sensitive to blue light (470-480 nm). At present, there is no evidence that blue light exposure is effective in modulating nonvisual brain activity related to complex cognitive tasks. Using functional magnetic resonance imaging, we show that, while participants perform an auditory working memory task, a short (18 min) daytime exposure to blue (470 nm) or green (550 nm) monochromatic light (3 x 10(13) photons/cm(2)/s) differentially modulates regional brain responses. Blue light typically enhanced brain responses or at least prevented the decline otherwise observed following green light exposure in frontal and parietal cortices implicated in working memory, and in the thalamus involved in the modulation of cognition by arousal. Our results imply that monochromatic light can affect cognitive functions almost instantaneously and suggest that these effects are mediated by a melanopsin-based photoreceptor system.
Disciplines :
Neurosciences & behavior
Author, co-author :
Vandewalle, Gilles ; Université de Liège - ULiège > Centre de Recherches du Cyclotron
Gais, S.
Schabus, Manuel ; Université de Liège - ULiège > Centre de recherches du cyclotron
Balteau, Evelyne ; Université de Liège - ULiège > Centre de recherches du cyclotron
Carrier, J.
Darsaud, A.
Sterpenich, Virginie ; Université de Liège - ULiège > Centre de recherches du cyclotron
Albouy, Geneviève ; Université de Liège - ULiège > Centre de recherches du cyclotron
Dijk, D. J.
Maquet, Pierre ; Université de Liège - ULiège > Centre de recherches du cyclotron
Language :
English
Title :
Wavelength-dependent modulation of brain responses to a working memory task by daytime light exposure
Abrahamson EE, Leak RK, Moore RY. 2001. The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport. 12:435-440.
Akerstedt T, Gillberg M. 1990. Subjective and objective sleepiness in the active individual. Int J Neurosci. 52:29-37.
Aston-Jones G. 2005. Brain structures and receptors involved in alertness. Sleep Med. 6(Suppl 1):S3-S7.
Badia P, Myers B, Boecker M, Culpepper J, Harsh JR. 1991. Bright light effects on body temperature, alertness, EEG and behavior. Physiol Behav. 50:583-588.
Beck AT, Epstein N, Brown G, Steer RA. 1988. An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol. 56:893-897.
Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 295:1070-1073.
Bonnet MH, Arand DL. 1998. Sleepiness as measured by modified multiple sleep latency testing varies as a function of preceding activity. Sleep. 21:477-483.
Brainard GC, Hanifin JP, Greeson JM, Byrne B, Glickman G, Gerner E, Rollag MD. 2001. Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J Neurosci. 21:6405-6412.
Brainard GC, Rollag MD, Hanifin JP. 1997. Photic regulation of melatonin in humans: ocular and neural signal transduction. J Biol Rhythms. 12:537-546.
Braver TS, Barch DM, Kelley WM, Buckner RL, Cohen NJ, Miezin FM, Snyder AZ, Ollinger JM, Akbudak E, Conturo TE, et al. 2001. Direct comparison of prefrontal cortex regions engaged by working and long-term memory tasks. Neuroimage. 14:48-59.
Bushara KO, Grafman J, Hallett M. 2001. Neural correlates of auditory-visual stimulus onset asynchrony detection. J Neurosci. 21:300-304.
Bushara KO, Hanakawa T, Immisch I, Toma K, Kansaku K, Hallett M. 2003. Neural correlates of cross-modal binding. Nat Neurosci. 6:190-195.
Bushara KO, Weeks RA, Ishii K, Catalan MJ, Tian B, Rauschecker JP, Hallett M. 1999. Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans. Nat Neurosci. 2:759-766.
Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. 1989. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 28:193-213.
Cabeza R, Nyberg L. 2000. Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci. 12:1-47.
Cajochen C, Munch M, Kobialka S, Krauchi K, Steiner R, Oelhafen P, Orgul S, 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.
Campbell SS, Dawson D. 1990. Enhancement of nighttime alertness and performance with bright ambient light. Physiol Behav. 48:317-320.
Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE. 1997. Temporal dynamics of brain activation during a working memory task. Nature. 386:604-608.
Collette F, Hogge M, Salmon E, Van Der Linden M. 2006. Exploration of the neural substrates of executive functioning by functional neuroimaging. Neuroscience. 139(1):209-221.
Collette F, Van der Linden M, Laureys S, Delfiore G, Degueldre C, Luxen A, Salmon E. 2005. Exploring the unity and diversity of the neural substrates of executive functioning. Hum Brain Mapp. 25:409-423.
Coull JT, Jones ME, Egan TD, Frith CD, Maze M. 2004. Attentional effects of noradrenaline vary with arousal level: selective activation of thalamic pulvinar in humans. Neuroimage. 22:315-322.
Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin PD. 2005. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 433:749-754.
Deurveilher S, Semba K. 2005. Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience. 130:165-183.
Dijk DJ, Lockley SW. 2002. Integration of human sleep-wake regulation and circadian rhythmicity. J Appl Physiol. 92:852-862.
Dkhissi-Benyahya O, Rieux C, Hut RA, Cooper HM. 2006. Immunohistochemical evidence of a melanopsin cone in human retina. Investig Ophthalmol Vis Sci. 47:1636-1641.
Dkhissi-Benyahya O, Sicard B, Cooper HM. 2000. Effects of irradiance and stimulus duration on early gene expression (Fos) in the suprachiasmatic nucleus: temporal summation and reciprocity. J Neurosci. 20:7790-7797.
Downar J, Crawley AP, Mikulis DJ, Davis KD. 2000. A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci. 3:277-283.
Duffy JF, Kronauer RE, Czeisler CA. 1996. Phase-shifting human circadian rhythms: influence of sleep timing, social contact and light exposure. J Physiol. 495(Pt 1):289-297.
Foucher JR, Otzenberger H, Gounot D. 2004. Where arousal meets attention: a simultaneous fMRI and EEG recording study. Neuroimage. 22:688-697.
French J, Hannon P, Brainard GC. 1990. Effects of bright illuminance on body temperature and human performance. Annu Rev Chronopharmacol. 7:37-40.
Friston KJ, Penny W. 2003. Posterior probability maps and SPMs. Neuroimage. 19:1240-1249.
Glaser DE, Friston KJ. 2004. Variance components. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Price CJ, Zeki S, Ashburner J, Penny W, editors. Human brain function. San Diego (CA): Academic Press. p. 781-791.
Gooley JJ, Lu J, Fischer D, Saper CB. 2003. A broad role for melanopsin in nonvisual photoreception. J Neurosci. 23:7093-7106.
Grandjean D, Sander D, Pourtois G, Schwartz S, Seghier ML, Scherer KR, Vuilleumier P. 2005. The voices of wrath: brain responses to angry prosody in meaningless speech. Nat Neurosci. 8:145-146.
Hankins MW, Lucas RJ. 2002. The primary visual pathway in humans is regulated according to long-term light exposure through the action of a nonclassical photopigment. Curr Biol. 12:191-198.
Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol. 497:326-349.
Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, et al. 2003. Melanopsin and rodcone photoreceptive systems account for all major accessory visual functions in mice. Nature. 424:76-81.
Horne JA, Ostberg O. 1976. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 4:97-110.
Johns MW. 1991. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 14:540-545.
Lockley SW, Brainard GC, Czeisler CA. 2003. High sensitivity of the human circadian melatonin rhythm to resetting by short wavelength light. J Clin Endocrinol Metab. 88:4502-4505.
Lockley SW, Evans EE, Scheer FAJL, Brainard GC, Czeisler CA, 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.
Lucas RJ, Douglas RH, Foster RG. 2001. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci. 4:621-626.
Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW. 2005. Addition of human melanopsin renders mammalian cells photoresponsive. Nature. 433:741-745.
Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. 2005. Illumination of the melanopsin signaling pathway. Science. 307:600-604.
Perrin F, Peigneux P, Fuchs S, Verhaeghe S, Laureys S, Middleton B, Degueldre C, Del Fiore G, Vandewalle G, Balteau E, et al. 2004. Nonvisual responses to light exposure in the human brain during the circadian night. Curr Biol 14:1842-1846.
Phipps-Nelson J, Redman JR, Dijk DJ, Rajaratnam SMW. 2003. Daytime exposure to bright light, as compared to dim light, decreases sleepiness and improves psychomotor vigilance performance. Sleep. 26:695-700.
Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. 2000. A novel human opsin in the inner retina. J Neurosci. 20:600-605.
Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM. 2005. Induction of photosensitivity by heterologous expression of melanopsin. Nature. 433:745-749.
Ruger M, Gordijn MC, Beersma DG, de Vries B, Daan S. 2005. Timeof-day-dependent effects of bright light exposure on human psychophysiology: comparison of daytime and nighttime exposure. Am J Physiol Regul Integr Comp Physiol.
Saper CB, Lu J, Chou TC, Gooley J. 2005. The hypothalamic integrator for circadian rhythms. Trends Neurosci. 28:152-157.
Steer RA, Ball R, Ranieri WF, Beck AT. 1997. Further evidence for the construct validity of the Beck depression Inventory-II with psychiatric outpatients. Psychol Rep. 80:443-446.
Talairach J, Tournoux P. 1988. Co-planar steriotaxic atlas of the human brain. New-York: Thieme.
Thapan K, Arendt J, Skene DJ. 2001. An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J Physiol. 535:261-267.
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.
Wager TD, Jonides J, Reading S. 2004. Neuroimaging studies of shifting attention: a meta-analysis. Neuroimage. 22:1679-1693.
Wager TD, Smith EE. 2003. Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci. 3:255-274.
