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Research Article

Photic memory for executive brain responses

Sarah Laxhmi Chellappa, Julien Q. M. Ly, Christelle Meyer, Evelyne Balteau, Christian Degueldre, André Luxen, Christophe Phillips, Howard M. Cooper, and Gilles Vandewalle
PNAS first published March 10, 2014; https://doi.org/10.1073/pnas.1320005111
Sarah Laxhmi Chellappa
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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Julien Q. M. Ly
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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Christelle Meyer
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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Evelyne Balteau
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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Christian Degueldre
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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André Luxen
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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Christophe Phillips
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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Howard M. Cooper
bDepartment of Chronobiology, Institut National de la Santé et de la Recherche Médicale Stem Cell and Brain Research Institute, 69675 Bron Cedex, France
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  • For correspondence: gilles.vandewalle@ulg.ac.be howard.cooper@inserm.fr
Gilles Vandewalle
aCyclotron Research Center, University of Liège, 4000 Liège, Belgium; and
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  • For correspondence: gilles.vandewalle@ulg.ac.be howard.cooper@inserm.fr
  1. Edited by Bruce S. McEwen, The Rockefeller University, New York, NY, and approved February 13, 2014 (received for review October 23, 2013)

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Significance

Light is a powerful stimulant for human alertness and cognition that can be easily administered to improve performance or counteract the negative impact of sleepiness, even during the day. Here, we show that prior exposure to longer wavelength light (orange), relative to shorter wavelength (blue), enhances the subsequent impact of light on executive brain responses. These findings emphasize the importance of light for human cognitive brain function and constitute compelling evidence in favor of a cognitive role for melanopsin. This recently discovered photopigment may therefore provide a unique form of “photic memory” for human cognition and play a broader role than previously apprehended. Ultimately, these findings support the idea that the integration of light exposure over long periods of time can help optimize cognitive brain function.

Abstract

Light is a powerful stimulant for human alertness and cognition, presumably acting through a photoreception system that heavily relies on the photopigment melanopsin. In humans, evidence for melanopsin involvement in light-driven cognitive stimulation remains indirect, due to the difficulty to selectively isolate its contribution. Therefore, a role for melanopsin in human cognitive regulation remains to be established. Here, sixteen participants underwent consecutive and identical functional MRI recordings, during which they performed a simple auditory detection task and a more difficult auditory working memory task, while continuously exposed to the same test light (515 nm). We show that the impact of test light on executive brain responses depends on the wavelength of the light to which individuals were exposed prior to each recording. Test-light impact on executive responses in widespread prefrontal areas and in the pulvinar increased when the participants had been exposed to longer (589 nm), but not shorter (461 nm), wavelength light, more than 1 h before. This wavelength-dependent impact of prior light exposure is consistent with recent theories of the light-driven melanopsin dual states. Our results emphasize the critical role of light for cognitive brain responses and are, to date, the strongest evidence in favor of a cognitive role for melanopsin, which may confer a form of “photic memory” to human cognitive brain function.

  • fMRI
  • non–image-forming

Footnotes

  • ↵1S.L.C. and J.Q.M.L. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. E-mail: gilles.vandewalle{at}ulg.ac.be or howard.cooper{at}inserm.fr.
  • Author contributions: H.M.C. and G.V. designed research; S.L.C., J.Q.M.L., C.M., and G.V. performed research; E.B., C.D., A.L., and C.P. contributed new reagents/analytic tools; S.L.C. and G.V. analyzed data; S.L.C., J.Q.M.L., H.M.C., and G.V. wrote the paper; E.B. provided technical expertise for fMRI acquisitions and analysis; C.D. and A.L. provided technical expertise for data acquisitions; and C.P. provided technical expertise for data analyses.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1320005111/-/DCSupplemental.

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Prior light and brain responses
Sarah Laxhmi Chellappa, Julien Q. M. Ly, Christelle Meyer, Evelyne Balteau, Christian Degueldre, André Luxen, Christophe Phillips, Howard M. Cooper, Gilles Vandewalle
Proceedings of the National Academy of Sciences Mar 2014, 201320005; DOI: 10.1073/pnas.1320005111

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Prior light and brain responses
Sarah Laxhmi Chellappa, Julien Q. M. Ly, Christelle Meyer, Evelyne Balteau, Christian Degueldre, André Luxen, Christophe Phillips, Howard M. Cooper, Gilles Vandewalle
Proceedings of the National Academy of Sciences Mar 2014, 201320005; DOI: 10.1073/pnas.1320005111
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