Light Affects Mood and Learning through Distinct Retina-Brain Pathways

• Published in: Cell Vol. 175; no. 1; pp. 71 - 84.e18
• Main Authors: Fernandez, Diego Carlos, Fogerson, P. Michelle, Lazzerini Ospri, Lorenzo, Thomsen, Michael B., Layne, Robert M., Severin, Daniel, Zhan, Jesse, Singer, Joshua H., Kirkwood, Alfredo, Zhao, Haiqing, Berson, David M., Hattar, Samer
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 20-09-2018
• Subjects: aberrant light cycle; Affect - physiology; Affect - radiation effects; Animals; Brain - physiology; Circadian Rhythm; circadian rhythms; ipRGCs; learning; Learning - physiology; Learning - radiation effects; Light; Mice; Mice, Inbred C57BL; mood; perihabenular nucleus; Phototherapy - methods; Retina - metabolism; Retina - physiology; Retinal Ganglion Cells - metabolism; Retinal Ganglion Cells - physiology; Retinal Ganglion Cells - radiation effects; Signal Transduction - physiology; suprachiasmatic nucleus; Suprachiasmatic Nucleus - metabolism; ventromedial prefrontal cortex; Vision, Ocular - physiology; Visual Pathways - metabolism; Visual Perception - physiology; ipRGCs; aberrant light cycle; mood; ventromedial prefrontal cortex; perihabenular nucleus; learning; suprachiasmatic nucleus; circadian rhythms
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2018.08.004

Light exerts a range of powerful biological effects beyond image vision, including mood and learning regulation. While the source of photic information affecting mood and cognitive functions is well established, viz. intrinsically photosensitive retinal ganglion cells (ipRGCs), the central mediators are unknown. Here, we reveal that the direct effects of light on learning and mood utilize distinct ipRGC output streams. ipRGCs that project to the suprachiasmatic nucleus (SCN) mediate the effects of light on learning, independently of the SCN’s pacemaker function. Mood regulation by light, on the other hand, requires an SCN-independent pathway linking ipRGCs to a previously unrecognized thalamic region, termed perihabenular nucleus (PHb). The PHb is integrated in a distinctive circuitry with mood-regulating centers and is both necessary and sufficient for driving the effects of light on affective behavior. Together, these results provide new insights into the neural basis required for light to influence mood and learning.
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•Distinct ipRGC subpopulations drive the effects of light on learning and mood•SCN-projecting ipRGCs affect learning without disrupting the central pacemaker•The ipRGC-PHb pathway drives the light-mediated mood alterations•Thalamic PHb is integrated in a distinctive circuitry with mood-regulating centers
The effects of light on learning and mood via intrinsically photosensitive retinal ganglion cells involve a pacemaker-independent role for the suprachiasmatic nucleus as well as distinct circuitry in a region of the thalamus called the perihabenular nucleus.