functional magnetic resonance imaging; melanopic equivalent daylight illuminance; melanopsin; non-image-forming effect of light; pupil light reflex
Abstract :
[en] Light triggers numerous non-image-forming, or non-visual, biological effects. The brain correlates of these non-image-forming effects have been investigated, notably using magnetic resonance imaging and short light exposures varying in irradiance and spectral quality. However, it is not clear whether non-image-forming responses estimation may be biased by having light in sequential blocks, for example, through a potential carryover effect of one light onto the next. We reasoned that pupil light reflex was an easy readout of one of the non-image-forming effects of light that could be used to address this issue. We characterised the sustained pupil light reflex in 13-16 healthy young individuals under short light exposures during three distinct cognitive processes (executive, emotional and attentional). Light conditions pseudo-randomly alternated between monochromatic orange light (0.16 melanopic equivalent daylight illuminance lux) and polychromatic blue-enriched white light of three different levels (37, 92, 190 melanopic equivalent daylight illuminance lux). As expected, higher melanopic irradiance was associated with larger sustained pupil light reflex in each cognitive domain. This result was stable over the light sequence under higher melanopic irradiance levels compared with lower ones. Exploratory frequency-domain analyses further revealed that sustained pupil light reflex was more variable under lower melanopic irradiance levels. Importantly, sustained pupil light reflex varied across tasks independently of the light condition, pointing to a potential impact of light history and/or cognitive context on sustained pupil light reflex. Together, our results emphasise that the distinct contribution and adaptation of the different retinal photoreceptors influence the non-image-forming effects of light and therefore potentially their brain correlates.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Beckers, Elise ; Université de Liège - ULiège > GIGA ; Faculty of Health, Medicine and Life Sciences, School for Mental Health and Neuroscience, Alzheimer Centre Limburg, Maastricht University, Maastricht, the Netherlands
Sharifpour, Roya ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Paparella, Ilenia ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Sleep and chronobiology
Berger, Alexandre ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Sleep and chronobiology ; Institute of Neuroscience (IoNS), Université Catholique de Louvain (UCLouvain), Woluwe-Saint-Lambert, Belgium ; Synergia Medical SA, Mont-Saint-Guibert, Belgium
Talwar, Puneet ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Sherif, Siya ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Sleep and chronobiology
Jacobs, Heidi I L; Faculty of Health, Medicine and Life Sciences, School for Mental Health and Neuroscience, Alzheimer Centre Limburg, Maastricht University, Maastricht, the Netherlands ; Gordon Center for Medical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA
Vandewalle, Gilles ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Language :
English
Title :
Impact of repeated short light exposures on sustained pupil responses in an fMRI environment.
Aston-Jones, G., & Bloom, F. E. (1981). Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. The Journal of Neuroscience, 1(8), 887–900. https://doi.org/10.1523/jneurosci.01-08-00887.1981
Banse, R., & Scherer, K. R. (1996). Acoustic profiles in vocal emotion expression. Journal of Personality and Social Psychology, 70(3), 614–636. https://doi.org/10.1037//0022-3514.70.3.614
Beck, A. T., Epstein, N., Brown, G., & Steer, R. A. (1988). An inventory for measuring clinical anxiety: Psychometric properties. Journal of Consulting and Clinical Psychology, 56(6), 893–897. https://doi.org/10.1037//0022-006x.56.6.893
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561–571. https://doi.org/10.1001/archpsyc.1961.01710120031004
Berson, D. M., Dunn, F. A., & Takao, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295(5557), 1070–1073. https://doi.org/10.1126/science.1067262
Brainard, G. C., Hanifin, J. P., Greeson, J. M., Byrne, B., Glickman, G., Gerner, E., & Rollag, M. D. (2001). Action spectrum for melatonin regulation in humans: Evidence for a novel circadian photoreceptor. The Journal of Neuroscience, 21(16), 6405–6412. https://doi.org/10.1523/jneurosci.21-16-06405.2001
Buysse, D. J., Reynolds, C. F., 3rd, Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989). The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Research, 28(2), 193–213. https://doi.org/10.1016/0165-1781(89)90047-4
Cajochen, C., Münch, M., Kobialka, S., Kräuchi, K., Steiner, R., Oelhafen, P., Orgül, S., & Wirz-Justice, A. (2005). High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light. The Journal of Clinical Endocrinology and Metabolism, 90(3), 1311–1316. https://doi.org/10.1210/jc.2004-0957
Campbell, I., Beckers, E., Sharifpour, R., Berger, A., Paparella, I., Aizpurua, J. F. B., Koshmanova, E., Mortazavi, N., Sherif, S., & Vandewalle, G. (2023). Impact of light on task-evoked pupil responses during cognitive tasks. bioRxiv, 2023.2004.2012.536570. https://doi.org/10.1101/2023.04.12.536570
Campbell, I., Sharifpour, R., & Vandewalle, G. (2023). Light as a modulator of non-image-forming brain functions—positive and negative impacts of increasing light availability. Clocks & Sleep, 5(1), 116–140.
Cole, L., Lightman, S., Clark, R., & Gilchrist, I. D. (2022). Tonic and phasic effects of reward on the pupil: Implications for locus coeruleus function. Proceedings of the Biological Sciences, 289(1982), 20221545. https://doi.org/10.1098/rspb.2022.1545
Collette, F., Hogge, M., Salmon, E., & Van der Linden, M. (2005). Exploration of the neural substrates of executive functioning by functional neuroimaging. Neuroscience, 139(1), 209–221. https://doi.org/10.1016/j.neuroscience.2005.05.035
Daneault, V., Hébert, M., Albouy, G., Doyon, J., Dumont, M., Carrier, J., & Vandewalle, G. (2014). Aging reduces the stimulating effect of blue light on cognitive brain functions. Sleep, 37(1), 85–96. https://doi.org/10.5665/sleep.3314
Daneault, V., Vandewalle, G., Hébert, M., Teikari, P., Mure, L. S., Doyon, J., Gronfier, C., Cooper, H. M., Dumont, M., & Carrier, J. (2012, Jun). Does pupil constriction under blue and green monochromatic light exposure change with age? Journal of Biological Rhythms, 27(3), 257–264. https://doi.org/10.1177/0748730412441172
Do, M. T., Kang, S. H., Xue, T., Zhong, H., Liao, H. W., Bergles, D. E., & Yau, K. W. (2009). Photon capture and signalling by melanopsin retinal ganglion cells. Nature, 457(7227), 281–287. https://doi.org/10.1038/nature07682
Fisk, A. S., Tam, S. K. E., Brown, L. A., Vyazovskiy, V. V., Bannerman, D. M., & Peirson, S. N. (2018). Light and cognition: Roles for circadian rhythms, sleep, and arousal. Frontiers in Neurology, 9, 56. https://doi.org/10.3389/fneur.2018.00056
Gaggioni, G., Maquet, P., Schmidt, C., Dijk, D. J., & Vandewalle, G. (2014). Neuroimaging, cognition, light and circadian rhythms. Frontiers in Systems Neuroscience, 8, 126. https://doi.org/10.3389/fnsys.2014.00126
Gamlin, P. D., McDougal, D. H., Pokorny, J., Smith, V. C., Yau, K. W., & Dacey, D. M. (2007). Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Research, 47(7), 946–954. https://doi.org/10.1016/j.visres.2006.12.015
Gooley, J. J., Ho Mien, I., St Hilaire, M. A., Yeo, S. C., Chua, E. C., van Reen, E., Hanley, C. J., Hull, J. T., Czeisler, C. A., & Lockley, S. W. (2012, Oct 10). Melanopsin and rod-cone photoreceptors play different roles in mediating pupillary light responses during exposure to continuous light in humans. The Journal of Neuroscience, 32(41), 14242–14253. https://doi.org/10.1523/jneurosci.1321-12.2012
Güler, A. D., Ecker, J. L., Lall, G. S., Haq, S., Altimus, C. M., Liao, H. W., Barnard, A. R., Cahill, H., Badea, T. C., Zhao, H., Hankins, M. W., Berson, D. M., Lucas, R. J., Yau, K. W., & Hattar, S. (2008). Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature, 453(7191), 102–105. https://doi.org/10.1038/nature06829
Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K. W., & Berson, D. M. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. The Journal of Comparative Neurology, 497(3), 326–349. https://doi.org/10.1002/cne.20970
Horne, J. A., & Ostberg, O. (1976). A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. International Journal of Chronobiology, 4(2), 97–110.
Jaeger, B. C., Edwards, L. J., Das, K., & Sen, P. K. (2017). An R2 statistic for fixed effects in the generalized linear mixed model. Journal of Applied Statistics, 44(6), 1086–1105. https://doi.org/10.1080/02664763.2016.1193725
Johns, M. W. (1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14(6), 540–545. https://doi.org/10.1093/sleep/14.6.540
Joshi, S., & Gold, J. I. (2020). Pupil size as a window on neural substrates of cognition. Trends in Cognitive Sciences, 24(6), 466–480. https://doi.org/10.1016/j.tics.2020.03.005
Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus Coeruleus, colliculi, and cingulate cortex. Neuron, 89(1), 221–234. https://doi.org/10.1016/j.neuron.2015.11.028
Lok, R., Smolders, K., Beersma, D. G. M., & de Kort, Y. A. W. (2018). Light, alertness, and alerting effects of white light: A literature overview. Journal of Biological Rhythms, 33(6), 589–601. https://doi.org/10.1177/0748730418796443
Lucas, R. J., Hattar, S., Takao, M., Berson, D. M., Foster, R. G., & Yau, K. W. (2003). Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science, 299(5604), 245–247. https://doi.org/10.1126/science.1077293
Lucas, R. J., Lall, G. S., Allen, A. E., & Brown, T. M. (2012). Chapter 1-how rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock. In A. Kalsbeek, M. Merrow, T. Roenneberg, & R. G. Foster (Eds.), Progress in brain research (Vol. 199, pp. 1–18). Elsevier.
Lucas, R. J., Peirson, S. N., Berson, D. M., Brown, T. M., Cooper, H. M., Czeisler, C. A., Figueiro, M. G., Gamlin, P. D., Lockley, S. W., O'Hagan, J. B., Price, L. L. A., Provencio, I., Skene, D. J., & Brainard, G. C. (2014). Measuring and using light in the melanopsin age. Trends in Neurosciences, 37(1), 1–9. https://doi.org/10.1016/j.tins.2013.10.004
Mathôt, S., Schreij, D., & Theeuwes, J. (2012). OpenSesame: An open-source, graphical experiment builder for the social sciences. Behavior Research Methods, 44(2), 314–324. https://doi.org/10.3758/s13428-011-0168-7
McDougal, D. H., & Gamlin, P. D. (2010). The influence of intrinsically-photosensitive retinal ganglion cells on the spectral sensitivity and response dynamics of the human pupillary light reflex. Vision Research, 50(1), 72–87. https://doi.org/10.1016/j.visres.2009.10.012
McGlashan, E. M., Poudel, G. R., Jamadar, S. D., Phillips, A. J. K., & Cain, S. W. (2021). Afraid of the dark: Light acutely suppresses activity in the human amygdala. PLoS One, 16(6), e0252350. https://doi.org/10.1371/journal.pone.0252350
Megemont, M., McBurney-Lin, J., & Yang, H. (2022). Pupil diameter is not an accurate real-time readout of locus coeruleus activity. eLife, 11, e70510. https://doi.org/10.7554/eLife.70510
Mure, L. S. (2021). Intrinsically photosensitive retinal ganglion cells of the human retina. Frontiers in Neurology, 12, 636330. https://doi.org/10.3389/fneur.2021.636330
Murphy, P. R., O'Connell, R. G., O'Sullivan, M., Robertson, I. H., & Balsters, J. H. (2014). Pupil diameter covaries with BOLD activity in human locus coeruleus. Human Brain Mapping, 35(8), 4140–4154. https://doi.org/10.1002/hbm.22466
Nakayama, M., & Shimizu, Y. (2021). Frequency analysis of task evoked pupillary response and eye movement. In M. Nakayama & Y. Shimizu (Eds.), Pupil reactions in response to human mental activity (pp. 89–103). Springer Singapore.
Nguyen, K. T., Liang, W. K., Juan, C. H., & Wang, C. A. (2022). Time-frequency analysis of pupil size modulated by global luminance, arousal, and saccade preparation signals using Hilbert-Huang transform. International Journal of Psychophysiology, 176, 89–99. https://doi.org/10.1016/j.ijpsycho.2022.03.011
Partala, T., & Surakka, V. (2003). Pupil size variation as an indication of affective processing. International Journal of Human-Computer Studies, 59(1), 185–198. https://doi.org/10.1016/S1071-5819(03)00017-X
Peysakhovich, V., Causse, M., Scannella, S., & Dehais, F. (2015). Frequency analysis of a task-evoked pupillary response: Luminance-independent measure of mental effort. International Journal of Psychophysiology, 97(1), 30–37. https://doi.org/10.1016/j.ijpsycho.2015.04.019
Prayag, A., Jost-Boissard, S., Avouac, P., Dumortier, D., & Gronfier, C. (2019). Dynamics of non-visual responses in humans: As fast as lightning? Frontiers in Neuroscience, 13, 126. https://doi.org/10.3389/fnins.2019.00126
Paparella, I., Campbell, I., Sharifpour, R., Beckers, E., Berger, A., Aizpurua, J. F. B., Koshmanova, E., Mortazavi, N., Talwar, P., Degueldre, C., Lamalle, L., Sherif, S., Phillips, C., Maquet, P., & Vandewalle, G. (2023). Light modulates task-dependent thalamo-cortical connectivity during an auditory attentional task. Communications Biology, 6(1). https://doi.org/10.1038/s42003-023-05337-5
Rosenthal, N. (1984). Seasonal pattern assessment questionnaire. Journal of Affective Disorders, 41(3), 193–1999.
Rukmini, A. V., Milea, D., Aung, T., & Gooley, J. J. (2017). Pupillary responses to short-wavelength light are preserved in aging. Scientific Reports, 7, 43832. https://doi.org/10.1038/srep43832
Stevens, A. A., Skudlarski, P., Gatenby, J. C., & Gore, J. C. (2000). Event-related fMRI of auditory and visual oddball tasks. Magnetic Resonance Imaging, 18(5), 495–502. https://doi.org/10.1016/s0730-725x(00)00128-4
Thapan, K., Arendt, J., & Skene, D. J. (2001, Aug 15). An action spectrum for melatonin suppression: Evidence for a novel non-rod, non-cone photoreceptor system in humans. The Journal of Physiology, 535(Pt 1), 261–267. https://doi.org/10.1111/j.1469-7793.2001.t01-1-00261.x
Vandewalle, G., Archer, S. N., Wuillaume, C., Balteau, E., Degueldre, C., Luxen, A., Dijk, D. J., & Maquet, P. (2011). Effects of light on cognitive brain responses depend on circadian phase and sleep homeostasis. Journal of Biological Rhythms, 26(3), 249–259. https://doi.org/10.1177/0748730411401736
Vandewalle, G., Maquet, P., & Dijk, D. J. (2009). Light as a modulator of cognitive brain function. Trends in Cognitive Sciences, 13(10), 429–438. https://doi.org/10.1016/j.tics.2009.07.004
Vandewalle, G., Schmidt, C., Albouy, G., Sterpenich, V., Darsaud, A., Rauchs, G., Berken, P. Y., Balteau, E., Degueldre, C., Luxen, A., Maquet, P., & Dijk, D. J. (2007). Brain responses to violet, blue, and green monochromatic light exposures in humans: Prominent role of blue light and the brainstem. PLoS One, 2(11), e1247. https://doi.org/10.1371/journal.pone.0001247
Vandewalle, G., Schwartz, S., Grandjean, D., Wuillaume, C., Balteau, E., Degueldre, C., Schabus, M., Phillips, C., Luxen, A., Dijk, D. J., & Maquet, P. (2010). Spectral quality of light modulates emotional brain responses in humans. Proceedings of the National Academy of Sciences of the United States of America, 107(45), 19549–19554. https://doi.org/10.1073/pnas.1010180107
