Light Affects Mood and Learning through Distinct Retina-Brain Pathways

Abstract

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.

Blue light at night acutely impairs glucose tolerance and increases sugar intake in the diurnal rodent Arvicanthis ansorgei in a sex‐dependent manner

“…Thus, among the areas that are innervated by the ipRGCs are the SCN, the intergeniculate leaflet (IGL), and presumably the lateral hypothalamus (LH). In previous work from another group, the acute effects of light on the brain of Arvicanthis have been reported (Shuboni et al ), showing a significant number of c‐Fos activated cells in the IGL, the LH, and the lateral habenula (LHb), or the perihabenular nucleus (PHb) in mice (Fernandez et al ). It has been previously shown that the geniculohypothalamic tract (which includes the IGL), actively modulates SCN responses to retinal input (Hanna et al ) and might modulate metabolic signals to the SCN (Saderi et al ), and reward and metabolic signals of feeding to the LHb (Huang et al ).…”

Environmental light is required for maintenance of long-term memory in Drosophila

“…In nocturnal mice, an ultradian LD cycle condition induces spatial learning defects, although such an aberrant light condition does not impair the molecular clock or sleep amount (LeGates et al, 2012). The ultradian LD cycle also attenuates hippocampal long-term potentiation (Fernandez et al, 2018). In contrast, a short pulse of white light during the night before learning enhances long-lasting fear memory through the activation of hippocampal p21-activated kinase 1 (Shan et al, 2015).…”

“…Earth’s rotation generates the daily cycle of day and night, and the rhythmic light–dark (LD) cycles have a significant impact on animal behavior and physiology. In animals, light is not only essential for acquiring information for image-forming vision in nature but also acts as a powerful modulator of brain functions such as circadian entrainment, hormone secretion, sleep-wake cycles, mood, and cognitive functions (Altimus et al, 2008; Crocker and Sehgal, 2010; Fernandez et al, 2018; LeGates et al, 2012; Vandewalle et al, 2009). Using the diurnal fruitfly Drosophila melanogaster, here, we found that LTM was severely impaired in flies kept in constant darkness (DD) after memory consolidation.…”

Distinct ipRGC subpopulations mediate light's acute and circadian effects on body temperature and sleep

“…Intriguingly, a single population of retinal projections neurons—intrinsically photosensitive retinal ganglion cells (ipRGCs)—have been implicated in the circadian and acute effects of light on many functions, including activity, sleep, and mood (Göz et al, 2008; Güler et al, 2008; Hatori et al, 2008; Legates et al, 2012; Fernandez et al, 2018). ipRGCs integrate light information from rods, cones, and their endogenous melanopsin phototransduction cascade (Schmidt et al, 2011), and relay that light information to over a dozen central targets (Hattar et al, 2006; Ecker et al, 2010).…”

“…In comparison, the mechanisms by which ipRGCs mediate acute light responses remains largely a mystery. Genetic ablation of ipRGCs or their melanopsin phototransduction cascade blocks or attenuates the acute effects of light on sleep (Altimus et al, 2008; Lupi et al, 2008; Tsai et al, 2009), wheel-running activity (Mrosovsky and Hattar, 2003; Güler et al, 2008), and mood (Legates et al, 2012; Fernandez et al, 2018). This dual role of ipRGCs in circadian and acute light responses suggests they may share a common circuit mechanism.…”