Light as a central modulator of circadian rhythms, sleep and affect

Light has profoundly influenced the evolution of life on earth. As widely appreciated, light enables us to generate images of our environment. However, light — through intrinsically photosensitive retinal ganglion cells (ipRGCs) — also influences behaviours that are essential for our health and quality of life but are independent of image formation. These include the synchronization of the circadian clock to the solar day, tracking of seasonal changes and the regulation of sleep. Irregular light environments lead to problems in circadian rhythms and sleep, which eventually cause mood and learning deficits. Recently, it was found that irregular light can also directly affect mood and learning without producing major disruptions in circadian rhythms and sleep. In this Review, we discuss the indirect and direct influence of light on mood and learning, and provide a model for how light, the circadian clock and sleep interact to influence mood and cognitive functions.

[1]  Y. Meesters,et al.  Rapid mood swings after unmonitored light exposure. , 1998, The American journal of psychiatry.

[2]  Morven A. Cameron,et al.  Evolution of Melanopsin Photoreceptors: Discovery and Characterization of a New Melanopsin in Nonmammalian Vertebrates , 2006, PLoS biology.

[3]  N. Kronfeld-Schor,et al.  It is darkness and not light: Depression-like behaviors of diurnal unstriped Nile grass rats maintained under a short photoperiod schedule , 2010, Journal of Neuroscience Methods.

[4]  Erik B. Bloss,et al.  Disruption of circadian clocks has ramifications for metabolism, brain, and behavior , 2011, Proceedings of the National Academy of Sciences.

[5]  P. Renshaw,et al.  Activation of suprachiasmatic nuclei and primary visual cortex depends upon time of day , 2009, The European journal of neuroscience.

[6]  R. McCarley,et al.  Control of sleep and wakefulness. , 2012, Physiological reviews.

[7]  L W Swanson,et al.  Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat , 1987, The Journal of comparative neurology.

[8]  Jon C. Cole,et al.  Chronic Jet Lag Produces Cognitive Deficits , 2000, The Journal of Neuroscience.

[9]  J. Harsh,et al.  Bright light effects on body temperature, alertness, EEG and behavior , 1991, Physiology & Behavior.

[10]  M. Biel,et al.  Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice , 2003, Nature.

[11]  W. Nauta,et al.  Hypothalamic regulation of sleep in rats; an experimental study. , 1946, Journal of neurophysiology.

[12]  M. Sofroniew.  Projections from vasopressin, oxytocin, and neurophysin neurons to neural targets in the rat and human. , 1980, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[13]  C. Altimus,et al.  Measuring circadian and acute light responses in mice using wheel running activity. , 2011, Journal of visualized experiments : JoVE.

[14]  M. Harrington,et al.  Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system , 2009, The European journal of neuroscience.

[15]  S. Hattar,et al.  Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation , 2008, Proceedings of the National Academy of Sciences.

[16]  F. Goodwin,et al.  Seasonal affective disorder. A description of the syndrome and preliminary findings with light therapy. , 1984, Archives of general psychiatry.

[17]  Evelyne Balteau,et al.  Nonvisual Responses to Light Exposure in the Human Brain during the Circadian Night , 2004, Current Biology.

[18]  P. Kofuji,et al.  Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse , 2011, The Journal of comparative neurology.

[19]  Russell G Foster,et al.  The acute light-induction of sleep is mediated by OPN4-based photoreception , 2008, Nature Neuroscience.

[20]  P. A. Carney,et al.  Influence of Climate on the Prevalence of Mania , 1988, British Journal of Psychiatry.

[21]  G. Aston-Jones,et al.  Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats , 2008, Proceedings of the National Academy of Sciences.

[22]  R. Silver,et al.  Resetting the brain clock: time course and localization of mPER1 and mPER2 protein expression in suprachiasmatic nuclei during phase shifts , 2004, The European journal of neuroscience.

[23]  D. Berson,et al.  Phototransduction by Retinal Ganglion Cells That Set the Circadian Clock , 2002, Science.

[24]  F. Benedetti,et al.  Chronobiological Therapy for Mood Disorders , 2015, Current Psychiatry Reports.

[25]  C. M. Singer,et al.  Treating phase typed chronobiologic sleep and mood disorders using appropriately timed bright artificial light. , 1985, Psychopharmacology bulletin.

[26]  K. Deisseroth,et al.  Rapid regulation of depression-related behaviors by control of midbrain dopamine neurons , 2012, Nature.

[27]  Kwoon Y. Wong,et al.  Induction of photosensitivity by heterologous expression of melanopsin , 2005, Nature.

[28]  A. Wirz-Justice,et al.  High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light. , 2005, The Journal of clinical endocrinology and metabolism.

[29]  G. Vandewalle,et al.  Abnormal Hypothalamic Response to Light in Seasonal Affective Disorder , 2011, Biological Psychiatry.

[30]  D. Dijk,et al.  Dynamics of EEG slow-wave activity and core body temperature in human sleep after exposure to bright light. , 1992, Sleep.

[31]  R. Foster,et al.  The rhythm of rest and excess , 2005, Nature Reviews Neuroscience.

[32]  C. Allen,et al.  Intrinsic light responses of retinal ganglion cells projecting to the circadian system , 2003, The European journal of neuroscience.

[33]  Aaron S. Andalman,et al.  Dopamine neurons modulate neural encoding and expression of depression-related behaviour , 2012, Nature.

[34]  R. Nelson,et al.  Chronic dim light at night provokes reversible depression-like phenotype: possible role for TNF , 2013, Molecular Psychiatry.

[35]  Dennis McGinty,et al.  Sleep–waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats , 1998, Brain Research.

[36]  D. Berson,et al.  Morphology and mosaics of melanopsin‐expressing retinal ganglion cell types in mice , 2010, The Journal of comparative neurology.

[37]  J. M. Ree,et al.  Disrupting circadian rhythms in rats induces retrograde amnesia , 1985, Physiology & Behavior.

[38]  R. Nelson,et al.  Photoperiod-mediated impairment of long-term potention and learning and memory in male white-footed mice , 2011, Neuroscience.

[39]  D. Dijk,et al.  Dose-response relationship for light intensity and ocular and electroencephalographic correlates of human alertness , 2000, Behavioural Brain Research.

[40]  L W Swanson,et al.  Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat , 1987, The Journal of comparative neurology.

[41]  W. Drevets.  Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders , 2001, Current Opinion in Neurobiology.

[42]  Randy J. Nelson,et al.  Dim light at night provokes depression-like behaviors and reduces CA1 dendritic spine density in female hamsters , 2011, Psychoneuroendocrinology.

[43]  Thomas Götz,et al.  Acute exposure to evening blue‐enriched light impacts on human sleep , 2013, Journal of sleep research.

[44]  C. Escobar,et al.  Disruption of circadian rhythms due to chronic constant light leads to depressive and anxiety-like behaviors in the rat , 2013, Behavioural Brain Research.

[45]  C. Colwell,et al.  Rapid Changes in the Light/Dark Cycle Disrupt Memory of Conditioned Fear in Mice , 2010, PloS one.

[46]  Nanxin Li,et al.  Glutamate N-methyl-D-aspartate Receptor Antagonists Rapidly Reverse Behavioral and Synaptic Deficits Caused by Chronic Stress Exposure , 2011, Biological Psychiatry.

[47]  T. Badea,et al.  Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs , 2011, Nature.

[48]  Krzysztof Palczewski,et al.  Chemistry and Biology of Vision* , 2011, The Journal of Biological Chemistry.

[49]  Jun Lu,et al.  A Broad Role for Melanopsin in Nonvisual Photoreception , 2003, The Journal of Neuroscience.

[50]  K. Yau,et al.  Melanopsin-Containing Retinal Ganglion Cells: Architecture, Projections, and Intrinsic Photosensitivity , 2002, Science.

[51]  D. Cardinali,et al.  Circadian urinary 6‐sulphatoxymelatonin, cortisol excretion and locomotor activity in airline pilots during transmeridian flights , 2001, Journal of pineal research.

[52]  R. Bauman,et al.  Effects of controllable vs. uncontrollable stress on circadian temperature rhythms , 1991, Physiology & Behavior.

[53]  P. Willner,et al.  The validity of animal models of predisposition to depression. , 2002, Behavioural pharmacology.

[54]  R. Moore,et al.  Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections , 2001, Brain Research.

[55]  B. Roska,et al.  Local Retinal Circuits of Melanopsin-Containing Ganglion Cells Identified by Transsynaptic Viral Tracing , 2007, Current Biology.

[56]  Torbjörn Akerstedt,et al.  Psychosocial stress and impaired sleep. , 2006, Scandinavian journal of work, environment & health.

[57]  H. Heller,et al.  Melanopsin as a Sleep Modulator: Circadian Gating of the Direct Effects of Light on Sleep and Altered Sleep Homeostasis in Opn4−/− Mice , 2009, PLoS biology.

[58]  A. Yilmaz,et al.  Effect of lesioning the suprachiasmatic nuclei on behavioral despair in rats , 2004, Brain Research.

[59]  T. Holy,et al.  Physiologic Diversity and Development of Intrinsically Photosensitive Retinal Ganglion Cells , 2005, Neuron.

[60]  O. Hikosaka,et al.  Lateral habenula as a source of negative reward signals in dopamine neurons , 2007, Nature.

[61]  D B Boivin,et al.  Influence of sleep-wake and circadian rhythm disturbances in psychiatric disorders. , 2000, Journal of psychiatry & neuroscience : JPN.

[62]  A. B. Reddy,et al.  A clockwork web: circadian timing in brain and periphery, in health and disease , 2003, Nature Reviews Neuroscience.

[63]  Randy J. Nelson,et al.  Light at night increases body mass by shifting the time of food intake , 2010, Proceedings of the National Academy of Sciences.

[64]  T. Wehr.  Sleep loss: a preventable cause of mania and other excited states. , 1989, The Journal of clinical psychiatry.

[65]  D. Hellhammer,et al.  Associations between jet lag and cortisol diurnal rhythms after domestic travel. , 2010, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[66]  T. Fujioka,et al.  Effects of a constant light environment on hippocampal neurogenesis and memory in mice , 2011, Neuroscience Letters.

[67]  M. Rollag,et al.  A missense variant (P10L) of the melanopsin (OPN4) gene in seasonal affective disorder. , 2009, Journal of affective disorders.

[68]  Martin H. Teicher,et al.  24-h Monitoring of plasma norepinephrine, MHPG, cortisol, growth hormone and prolactin in depression. , 2004, Journal of psychiatric research.

[69]  M Terman,et al.  Circadian time of morning light administration and therapeutic response in winter depression. , 2001, Archives of general psychiatry.

[70]  Lance J. Kriegsfeld,et al.  Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters , 2010, PloS one.

[71]  F. Scheer,et al.  Short-wavelength sensitivity for the direct effects of light on alertness, vigilance, and the waking electroencephalogram in humans. , 2006, Sleep.

[72]  T. Miller.  The Impact of Cognitive Performance of , 2011 .

[73]  Samer Hattar,et al.  Central projections of melanopsin‐expressing retinal ganglion cells in the mouse , 2006, The Journal of comparative neurology.

[74]  Philippe Denis,et al.  Melanopsin Bistability: A Fly's Eye Technology in the Human Retina , 2009, PloS one.

[75]  Wen-pei Ma,et al.  Exposure to chronic constant light impairs spatial memory and influences long-term depression in rats , 2007, Neuroscience Research.

[76]  R. Lam,et al.  Evidence of a Biological Effect of Light Therapy on the Retina of Patients with Seasonal Affective Disorder , 2009, Biological Psychiatry.

[77]  M. Papp,et al.  Effect of chronic mild stress on circadian rhythms in the locomotor activity in rats , 1996, Pharmacology Biochemistry and Behavior.

[78]  Samer Hattar,et al.  Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions , 2011, Trends in Neurosciences.

[79]  G. Vandewalle,et al.  Light as a modulator of cognitive brain function , 2009, Trends in Cognitive Sciences.

[80]  P. Linkowski,et al.  The 24-hour profile of adrenocorticotropin and cortisol in major depressive illness. , 1985, The Journal of clinical endocrinology and metabolism.

[81]  M. Terman,et al.  Light Therapy for Seasonal and Nonseasonal Depression: Efficacy, Protocol, Safety, and Side Effects , 2005, CNS Spectrums.

[82]  Jun Lu,et al.  Afferents to the Ventrolateral Preoptic Nucleus , 2002, The Journal of Neuroscience.

[83]  A. Pack,et al.  Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4-5 hours per night. , 1997, Sleep.

[84]  R. Nelson,et al.  Nocturnal Light Exposure Impairs Affective Responses in a Wavelength-Dependent Manner , 2013, The Journal of Neuroscience.

[85]  N. Kronfeld-Schor,et al.  Antidepressants Reverse Short-Photoperiod-Induced, Forced Swim Test Depression-Like Behavior in the Diurnal Fat Sand Rat: Further Support for the Utilization of Diurnal Rodents for Modeling Affective Disorders , 2011, Neuropsychobiology.

[86]  Yasufumi Shigeyoshi,et al.  An Abrupt Shift in the Day/Night Cycle Causes Desynchrony in the Mammalian Circadian Center , 2003, The Journal of Neuroscience.

[87]  J. Bellingham,et al.  Addition of human melanopsin renders mammalian cells photoresponsive , 2005, Nature.

[88]  Charles A Czeisler,et al.  High sensitivity of the human circadian melatonin rhythm to resetting by short wavelength light. , 2003, The Journal of clinical endocrinology and metabolism.

[89]  Charles A Czeisler,et al.  Melanopsin and Rod–Cone Photoreceptors Play Different Roles in Mediating Pupillary Light Responses during Exposure to Continuous Light in Humans , 2012, The Journal of Neuroscience.

[90]  E. Kavalali,et al.  NMDA Receptor Blockade at Rest Triggers Rapid Behavioural Antidepressant Responses , 2011, Nature.

[91]  Randy J. Nelson,et al.  Dim Nighttime Light Impairs Cognition and Provokes Depressive-Like Responses in a Diurnal Rodent , 2012, Journal of biological rhythms.

[92]  T. Åkerstedt.  Shift work and disturbed sleep/wakefulness. , 1998, Occupational medicine.

[93]  T. Badea,et al.  Melanopsin cells are the principal conduits for rod–cone input to non-image-forming vision , 2008, Nature.

[94]  G. Groos,et al.  Vertebrate circadian rhythms: Retinal and extraretinal photoreception , 1982, Experientia.

[95]  Satchidananda Panda,et al.  Melanopsin (Opn4) Requirement for Normal Light-Induced Circadian Phase Shifting , 2002, Science.

[96]  A. Kalsbeek,et al.  Output pathways of the mammalian suprachiasmatic nucleus: coding circadian time by transmitter selection and specific targeting , 2002, Cell and Tissue Research.

[97]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[98]  J. Gillin,et al.  REM architecture changes in bipolar and unipolar depression. , 1979, The American journal of psychiatry.

[99]  Pierre Maquet,et al.  Cerebral Cortex doi:10.1093/cercor/bhm007 Wavelength-Dependent Modulation of Brain Responses to a Working Memory Task by Daytime Light Exposure , 2007 .

[100]  D. M. White,et al.  Morning vs evening light treatment for winter depression. Evidence that the therapeutic effects of light are mediated by circadian phase shifts. , 1990, Archives of general psychiatry.

[101]  R. Foster,et al.  Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[102]  Okihide Hikosaka,et al.  Habenula: Crossroad between the Basal Ganglia and the Limbic System , 2008, The Journal of Neuroscience.

[103]  R. Nelson,et al.  Influence of light at night on murine anxiety- and depressive-like responses , 2009, Behavioural Brain Research.

[104]  Walter W. Hauck,et al.  Light Therapy for Seasonal Affective Disorder with Blue Narrow-Band Light-Emitting Diodes (LEDs) , 2006, Biological Psychiatry.

[105]  G. E. Pickard,et al.  Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses , 2003, The Journal of comparative neurology.

[106]  Iain M McIntyre,et al.  Human Melatonin Suppression by Light is Intensity Dependent , 1989, Journal of pineal research.

[107]  Manuel Schabus,et al.  Spectral quality of light modulates emotional brain responses in humans , 2010, Proceedings of the National Academy of Sciences.

[108]  Arcady A. Putilov,et al.  Diurnal and seasonal variations of melatonin and serotonin in women with seasonal affective disorder. , 1994, Arctic medical research.

[109]  M. Terman.  Evolving applications of light therapy. , 2007, Sleep medicine reviews.

[110]  Richard T. Marrocco,et al.  Arousal systems , 1994, Current Opinion in Neurobiology.

[111]  D. Dijk,et al.  Melatonin and the Circadian Regulation of Sleep Initiation, Consolidation, Structure, and the Sleep EEG , 1997, Journal of biological rhythms.

[112]  Evelyne Balteau,et al.  Effects of Light on Cognitive Brain Responses Depend on Circadian Phase and Sleep Homeostasis , 2011, Journal of biological rhythms.

[113]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[114]  R. Nelson,et al.  Short day lengths alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters , 2011, Hormones and Behavior.

[115]  Shin Yamazaki,et al.  Constant light desynchronizes mammalian clock neurons , 2005, Nature Neuroscience.

[116]  Kole T. Roybal,et al.  Mania-like behavior induced by disruption of CLOCK , 2007, Proceedings of the National Academy of Sciences.

[117]  A. Wirz-Justice,et al.  Chronotherapeutics (light and wake therapy) as a class of interventions for affective disorders. , 2012, Handbook of clinical neurology.

[118]  R. J. McDonald,et al.  Circadian Phase-Shifted Rats Show Normal Acquisition but Impaired Long-Term Retention of Place Information in the Water Task , 2001, Neurobiology of Learning and Memory.

[119]  R. Canbeyli,et al.  Blue but not red light stimulation in the dark has antidepressant effect in behavioral despair , 2009, Behavioural Brain Research.

[120]  J. Nauta.  HYPOTHALAMIC REGULATION OF SLEEP IN RATS , 2004 .

[121]  E. Smeraldi,et al.  Morning light treatment hastens the antidepressant effect of citalopram: a placebo-controlled trial. , 2003, The Journal of clinical psychiatry.

[122]  S. Reppert,et al.  Coordination of circadian timing in mammals , 2002, Nature.

[123]  Sharon C. Lyter,et al.  Diagnostic and Statistical Manual of Mental Disorders: Making it Work for Social Work , 2012 .

[124]  B. McEwen,et al.  Effects of stress throughout the lifespan on the brain, behaviour and cognition , 2009, Nature Reviews Neuroscience.

[125]  F. Holloway,et al.  Phase shifting circadian rhythms produces retrograde amnesia. , 1981, Science.

[126]  G. Vandewalle,et al.  Brain Responses to Violet, Blue, and Green Monochromatic Light Exposures in Humans: Prominent Role of Blue Light and the Brainstem , 2007, PloS one.

[127]  N. Kronfeld-Schor,et al.  Effects of bright light treatment on depression- and anxiety-like behaviors of diurnal rodents maintained on a short daylight schedule , 2009, Behavioural Brain Research.

[128]  Martin H. Teicher,et al.  Seasonal mood disorders. Patterns of seasonal recurrence in mania and depression. , 1993, Archives of general psychiatry.

[129]  S. Deurveilher,et al.  Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: Implications for the circadian control of behavioural state , 2005, Neuroscience.

[130]  F. Goodwin,et al.  48-hour sleep-wake cycles in manic-depressive illness: naturalistic observations and sleep deprivation experiments. , 1982, Archives of general psychiatry.

[131]  G. E. Pickard,et al.  Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus , 2008, The European journal of neuroscience.

[132]  Arcady A. Putilov,et al.  Phase of melatonin rhythm in winter depression. , 1999, Advances in experimental medicine and biology.

[133]  R. Sapolsky,et al.  Hippocampal-dependent learning requires a functional circadian system , 2008, Proceedings of the National Academy of Sciences.

[134]  F. Goodwin.  Manic-Depressive Illness , 1990 .

[135]  Glen T. Prusky,et al.  Melanopsin-Expressing Retinal Ganglion-Cell Photoreceptors: Cellular Diversity and Role in Pattern Vision , 2010, Neuron.

[136]  T. Scammell,et al.  Afferents to the orexin neurons of the rat brain , 2006, The Journal of comparative neurology.

[137]  F. Holsboer,et al.  Stress and the brain: from adaptation to disease , 2005, Nature Reviews Neuroscience.

[138]  D J Kupfer,et al.  Self-reported sleep disturbance as a prodromal symptom in recurrent depression. , 1997, Journal of affective disorders.

[139]  G. Aston-Jones,et al.  Circuit projection from suprachiasmatic nucleus to ventral tegmental area: a novel circadian output pathway , 2009, The European journal of neuroscience.

[140]  W. P. Hayes,et al.  Melanopsin: An opsin in melanophores, brain, and eye. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[141]  Izzo,et al.  SUPPRESSION OF MELATONIN SECRETION IN SOME BLIND PATIENTS BY EXPOSURE TO BRIGHT LIGHT , 2001 .

[142]  D. Dijk,et al.  Daytime exposure to bright light, as compared to dim light, decreases sleepiness and improves psychomotor vigilance performance. , 2003, Sleep.

[143]  J. Eagles.  The relationship between mood and daily hours of sunlight in rapid cycling bipolar illness , 1994, Biological Psychiatry.

[144]  Gregor Eichele,et al.  Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. , 2010, The Journal of clinical investigation.

[145]  J. Takahashi,et al.  Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms , 1984, Nature.

[146]  T. Dang-Vu,et al.  Supplemental Results , 2022 .

[147]  K. Yau,et al.  Diminished Pupillary Light Reflex at High Irradiances in Melanopsin-Knockout Mice , 2003, Science.

[148]  M. Ikeda,et al.  Continuous exposure to dim illumination uncouples temporal patterns of sleep, body temperature, locomotion and drinking behavior in the rat , 2000, Neuroscience Letters.

[149]  D. Cardinali,et al.  Melatonin in mood disorders , 2006, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[150]  A. Wirz-Justice,et al.  Light therapy in seasonal affective disorder is independent of time of day or circadian phase. , 1993, Archives of general psychiatry.

[151]  W. P. Hayes,et al.  A Novel Human Opsin in the Inner Retina , 2000, The Journal of Neuroscience.

[152]  S. Lockley,et al.  Lux vs. wavelength in light treatment of Seasonal Affective Disorder , 2009, Acta psychiatrica Scandinavica.

[153]  D. Eilam,et al.  Sand rats see the light: Short photoperiod induces a depression-like response in a diurnal rodent , 2006, Behavioural Brain Research.

[154]  Kwoon Y. Wong,et al.  Intrinsic physiological properties of the five types of mouse ganglion-cell photoreceptors. , 2013, Journal of neurophysiology.

[155]  Sunggu Yang,et al.  Aberrant light directly impairs mood and learning through melanopsin-expressing neurons , 2012, Nature.

[156]  Thomas E. Scammell,et al.  The sleep switch: hypothalamic control of sleep and wakefulness , 2001, Trends in Neurosciences.

[157]  Scott J. Russo,et al.  The brain reward circuitry in mood disorders , 2013, Nature Reviews Neuroscience.

[158]  A. Borbély.  A two process model of sleep regulation. , 1982, Human neurobiology.

[159]  Brian J. Wiltgen,et al.  Light enhances learned fear , 2011, Proceedings of the National Academy of Sciences.

[160]  Clifford M. Singer,et al.  Winter Depression and the Phase-Shift Hypothesis for Bright Light's Therapeutic Effects: History, Theory, and Experimental Evidence , 1988, Journal of biological rhythms.

[161]  Franco Lepore,et al.  Blue Light Stimulates Cognitive Brain Activity in Visually Blind Individuals , 2013, Journal of Cognitive Neuroscience.

[162]  A. Wirz-Justice,et al.  Morning or night-time melatonin is ineffective in seasonal affective disorder. , 1990, Journal of psychiatric research.

[163]  P. Kofuji,et al.  Functional and Morphological Differences among Intrinsically Photosensitive Retinal Ganglion Cells , 2009, The Journal of Neuroscience.

[164]  R. Nelson,et al.  Light at Night Alters Daily Patterns of Cortisol and Clock Proteins in Female Siberian Hamsters , 2013, Journal of neuroendocrinology.

[165]  J. Emens,et al.  The circadian basis of winter depression. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[166]  M. Thase,et al.  Seasonal changes in clinical status in bipolar disorder: a prospective study in 1000 STEP‐BD patients , 2006, Acta psychiatrica Scandinavica.

[167]  Robert J. McDonald,et al.  Neuroscience and Biobehavioral Reviews the Trouble with Circadian Clock Dysfunction: Multiple Deleterious Effects on the Brain and Body , 2022 .

[168]  R. Nelson,et al.  Dim light at night increases depressive-like responses in male C3H/HeNHsd mice , 2013, Behavioural Brain Research.

[169]  R. Parker,et al.  Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species , 2002, Neuroscience.

[170]  P. Polo-Kantola,et al.  Sleep deprivation: Impact on cognitive performance , 2007, Neuropsychiatric disease and treatment.