Luxotonic Signals in Human Prefrontal Cortex As a Possible Substrate for Effects of Light on Mood and Cognition

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2022 Jul 22

PMID 35867740

Authors

Shai Sabbah

Michael S Worden

Dimitrios D Laniado

David M Berson

Jerome N Sanes

Affiliations

Soon will be listed here.

Abstract

Studies with experimental animals have revealed a mood-regulating neural pathway linking intrinsically photosensitive retinal ganglion cells (ipRGCs) and the prefrontal cortex (PFC), involved in the pathophysiology of mood disorders. Since humans also have light-intensity-encoding ipRGCs, we asked whether a similar pathway exists in humans. Here, functional MRI was used to identify PFC regions and other areas exhibiting light-intensity-dependent signals. We report 26 human brain regions having activation that either monotonically decreases or monotonically increases with light intensity. Luxotonic-related activation occurred across the cerebral cortex, in diverse subcortical structures, and in the cerebellum, encompassing regions with functions related to visual image formation, motor control, cognition, and emotion. Light suppressed PFC activation, which monotonically decreased with increasing light intensity. The sustained time course of light-evoked PFC responses and their susceptibility to prior light exposure resembled those of ipRGCs. These findings offer a functional link between light exposure and PFC-mediated cognitive and affective phenomena.

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References

Weiner K, Grill-Spector K . The improbable simplicity of the fusiform face area. Trends Cogn Sci. 2012; 16(5):251-4. DOI: 10.1016/j.tics.2012.03.003. View

Fernandez D, Fogerson P, Lazzerini Ospri L, Thomsen M, Layne R, Severin D . Light Affects Mood and Learning through Distinct Retina-Brain Pathways. Cell. 2018; 175(1):71-84.e18. PMC: 6190605. DOI: 10.1016/j.cell.2018.08.004. View

Vanni S, Tanskanen T, Seppa M, Uutela K, Hari R . Coinciding early activation of the human primary visual cortex and anteromedial cuneus. Proc Natl Acad Sci U S A. 2001; 98(5):2776-80. PMC: 30215. DOI: 10.1073/pnas.041600898. View

Liu J, Harris A, Kanwisher N . Perception of face parts and face configurations: an FMRI study. J Cogn Neurosci. 2009; 22(1):203-11. PMC: 2888696. DOI: 10.1162/jocn.2009.21203. View

Pang J, Gao F, Wu S . Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. J Neurosci. 2003; 23(14):6063-73. PMC: 6740343. View

Sanes J, Masland R . The types of retinal ganglion cells: current status and implications for neuronal classification. Annu Rev Neurosci. 2015; 38:221-46. DOI: 10.1146/annurev-neuro-071714-034120. View

Vandewalle G, Balteau E, Phillips C, Degueldre C, Moreau V, Sterpenich V . Daytime light exposure dynamically enhances brain responses. Curr Biol. 2006; 16(16):1616-21. DOI: 10.1016/j.cub.2006.06.031. View

Wong K . A retinal ganglion cell that can signal irradiance continuously for 10 hours. J Neurosci. 2012; 32(33):11478-85. PMC: 3432977. DOI: 10.1523/JNEUROSCI.1423-12.2012. View

Rolls E . The functions of the orbitofrontal cortex. Brain Cogn. 2004; 55(1):11-29. DOI: 10.1016/S0278-2626(03)00277-X. View

10.

Alkozei A, Smith R, Killgore W . 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. DOI: 10.1016/j.neulet.2016.01.034. View

11.

Borjigin J, Zhang L, Calinescu A . Circadian regulation of pineal gland rhythmicity. Mol Cell Endocrinol. 2011; 349(1):13-9. PMC: 3202635. DOI: 10.1016/j.mce.2011.07.009. View

12.

Vandewalle G, Gais S, Schabus M, Balteau E, Carrier J, Darsaud A . Wavelength-dependent modulation of brain responses to a working memory task by daytime light exposure. Cereb Cortex. 2007; 17(12):2788-95. DOI: 10.1093/cercor/bhm007. View

13.

Ridderinkhof K, Ullsperger M, Crone E, Nieuwenhuis S . The role of the medial frontal cortex in cognitive control. Science. 2004; 306(5695):443-7. DOI: 10.1126/science.1100301. View

14.

LeGates T, Altimus C, Wang H, Lee H, Yang S, Zhao H . Aberrant light directly impairs mood and learning through melanopsin-expressing neurons. Nature. 2012; 491(7425):594-8. PMC: 3549331. DOI: 10.1038/nature11673. View

15.

Rolls E, Cheng W, Feng J . The orbitofrontal cortex: reward, emotion and depression. Brain Commun. 2020; 2(2):fcaa196. PMC: 7749795. DOI: 10.1093/braincomms/fcaa196. View

16.

Hannibal J, Kankipati L, Strang C, Peterson B, Dacey D, Gamlin P . Central projections of intrinsically photosensitive retinal ganglion cells in the macaque monkey. J Comp Neurol. 2014; 522(10):2231-48. PMC: 3996456. DOI: 10.1002/cne.23588. View

17.

Graybiel A, Grafton S . The striatum: where skills and habits meet. Cold Spring Harb Perspect Biol. 2015; 7(8):a021691. PMC: 4526748. DOI: 10.1101/cshperspect.a021691. View

18.

Cajochen C, Frey S, Anders D, Spati J, Bues M, Pross A . Evening exposure to a light-emitting diodes (LED)-backlit computer screen affects circadian physiology and cognitive performance. J Appl Physiol (1985). 2011; 110(5):1432-8. DOI: 10.1152/japplphysiol.00165.2011. View

19.

Goffart L, Quinet J, Chavane F, Masson G . Influence of background illumination on fixation and visually guided saccades in the rhesus monkey. Vision Res. 2005; 46(1-2):149-62. DOI: 10.1016/j.visres.2005.07.026. View

20.

Haynes J, Lotto R, Rees G . Responses of human visual cortex to uniform surfaces. Proc Natl Acad Sci U S A. 2004; 101(12):4286-91. PMC: 384733. DOI: 10.1073/pnas.0307948101. View