1,465
Views
1
CrossRef citations to date
0
Altmetric
Psychiatry

Effects of bright light therapy on neuroinflammatory and neuroplasticity markers in a diurnal rodent model of Seasonal Affective Disorder

ORCID Icon, , , ORCID Icon & ORCID Icon
Article: 2249015 | Received 05 Jul 2023, Accepted 14 Aug 2023, Published online: 25 Aug 2023

References

  • Rosenthal NE, Sack DA, Gillin JC, et al. Seasonal affective disorder. A description of the syndrome and preliminary findings with light therapy. Arch Gen Psychiatry. 1984;41(1):1–11. doi: 10.1001/archpsyc.1984.01790120076010.
  • Terman M, Amira L, Terman JS, et al. Predictors of response and nonresponse to light treatment for winter depression. Am J Psychiatry. 1996;153(11):1423–1429. doi: 10.1176/ajp.153.11.1423.
  • Ruhrmann S, Kasper S, Hawellek B, et al. Effects of fluoxetine versus bright light in the treatment of seasonal affective disorder. Psychol Med. 1998;28(4):923–933. doi: 10.1017/s0033291798006813.
  • Golden RN, Gaynes BN, Ekstrom RD, et al. The efficacy of light therapy in the treatment of mood disorders: a review and meta-analysis of the evidence. Am J Psychiatry. 2005;162(4):656–662. doi: 10.1176/appi.ajp.162.4.656.
  • Özdemir PG, Boysan M, Smolensky MH, et al. Comparison of venlafaxine alone versus venlafaxine plus bright light therapy combination for severe major depressive disorder. J Clin Psychiatry. 2015;76(05):e645-54–e654. doi: 10.4088/JCP.14m09376.
  • Even C, Schröder CM, Friedman S, et al. Efficacy of light therapy in nonseasonal depression: a systematic review. J Affect Disord. 2008;108(1-2):11–23. doi: 10.1016/j.jad.2007.09.008.
  • Al-Karawi D, Jubair L. Bright light therapy for nonseasonal depression: meta-analysis of clinical trials. J Affect Disord. 2016;198:64–71. doi: 10.1016/j.jad.2016.03.016.
  • Niederhofer H, von Klitzing K. Bright light treatment as mono-therapy of non-seasonal depression for 28 adolescents. Int J Psychiatry Clin Pract. 2012;16(3):233–237. doi: 10.3109/13651501.2011.625123.
  • Wirz-Justice A, Bader A, Frisch U, et al. A randomized, double-blind, placebo-controlled study of light therapy for antepartum depression. J Clin Psychiatry. 2011;72(7):986–993. doi: 10.4088/JCP.10m06188blu.
  • Corral M, Wardrop AA, Zhang H, et al. Morning light therapy for postpartum depression. Arch Womens Ment Health. 2007;10(5):221–224. doi: 10.1007/s00737-007-0200-1.
  • Colombo C, Lucca A, Benedetti F, et al. Total sleep deprivation combined with lithium and light therapy in the treatment of bipolar depression: replication of main effects and interaction. Psychiatry Res. 2000;95(1):43–53. doi: 10.1016/s0165-1781(00)00164-5.
  • Tseng P-T, Chen Y-W, Tu K-Y, et al. Light therapy in the treatment of patients with bipolar depression: a meta-analytic study. Eur Neuropsychopharmacol. 2016;26(6):1037–1047. doi: 10.1016/j.euroneuro.2016.03.001.
  • Rybak YE, McNeely HE, Mackenzie BE, et al. An open trial of light therapy in adult attention-deficit/hyperactivity disorder. J Clin Psychiatry. 2006;67(10):1527–1535. doi: 10.4088/jcp.v67n1006.
  • Zalta AK, Bravo K, Valdespino-Hayden Z, et al. A placebo-controlled pilot study of a wearable morning bright light treatment for probable PTSD. Depress Anxiety. 2019;36(7):617–624. doi: 10.1002/da.22897.
  • Phipps-Nelson J, Redman JR, Dijk D-J, et al. Daytime exposure to bright light, as compared to dim light, decreases sleepiness and improves psychomotor vigilance performance. Sleep. 2003;26(6):695–700. doi: 10.1093/sleep/26.6.695.
  • Kohyama J. Sleep health and asynchronization. Brain Dev. 2011;33(3):252–259. doi: 10.1016/j.braindev.2010.09.006.
  • Johnson JA, Garland SN, Carlson LE, et al. Bright light therapy improves cancer-related fatigue in cancer survivors: a randomized controlled trial. J Cancer Surviv. 2018;12(2):206–215. doi: 10.1007/s11764-017-0659-3.
  • Starreveld DEJ, et al. Light therapy for cancer-related fatigue in (non-)Hodgkin lymphoma survivors: results of a randomized controlled trial. Cancers (Basel.). 2021;13(19):4948 doi: 10.3390/cancers13194948.
  • Wu H-S, Gao F, Yan L, et al. Evaluating chronotypically tailored light therapy for breast cancer survivors: preliminary findings on fatigue and disrupted sleep. Chronobiol Int. 2022;39(2):221–232. doi: 10.1080/07420528.2021.1992419.
  • Haffmans PMJ, Sival RC, Lucius SAP, et al. Bright light therapy and melatonin in motor restless behaviour in dementia: a placebo-controlled study. Int J Geriat Psychiatry. 2001;16(1):106–110. doi: 10.1002/1099-1166(200101)16:1<106::AID-GPS288>3.0.CO;2-9.
  • Ancoli-Israel S, Gehrman P, Martin JL, et al. Increased light exposure consolidates sleep and strengthens circadian rhythms in severe Alzheimer’s disease patients. Behav Sleep Med. 2003;1(1):22–36. doi: 10.1207/S15402010BSM0101_4.
  • Sloane PD, Figueiro M, Garg S, et al. Effect of home-based light treatment on persons with dementia and their caregivers. Light Res Technol. 2015;47(2):161–176. doi: 10.1177/1477153513517255.
  • Yamadera H, Ito T, Suzuki H, et al. Effects of bright light on cognitive and sleep-wake (circadian) rhythm disturbances in Alzheimer-type dementia. Psychiatry Clin Neurosci. 2000;54(3):352–353. doi: 10.1046/j.1440-1819.2000.00711.x.
  • Riemersma-van der Lek RF, Swaab DF, Twisk J, et al. Effect of bright light and melatonin on cognitive and noncognitive function in elderly residents of group care facilities: a randomized controlled trial. JAMA. 2008;299(22):2642–2655. doi: 10.1001/jama.299.22.2642.
  • Leu SJ, Shiah IS, Yatham LN, et al. Immune-inflammatory markers in patients with seasonal affective disorder: effects of light therapy. J Affect Disord. 2001;63(1-3):27–34. doi: 10.1016/s0165-0327(00)00165-8.
  • Elliott JE, McBride AA, Balba NM, et al. Feasibility and preliminary efficacy for morning bright light therapy to improve sleep and plasma biomarkers in US veterans with TBI. A prospective, open-label, single-arm trial. PLoS One. 2022;17(4):e0262955. doi: 10.1371/journal.pone.0262955.
  • Bloomfield PS, Selvaraj S, Veronese M, et al. Microglial activity in people at ultra-high risk of psychosis and in schizophrenia: an [(11)C]PBR28 PET brain imaging study. Am J Psychiatry. 2016;173(1):44–52. doi: 10.1176/appi.ajp.2015.14101358.
  • Gilhus NE, Deuschl G. Neuroinflammation – a common thread in neurological disorders. Nat Rev Neurol. 2019;15(8):429–430. doi: 10.1038/s41582-019-0227-8.
  • van Berckel BN, Bossong MG, Boellaard R, et al. Microglia activation in recent-onset schizophrenia: a quantitative (R)-[11C]PK11195 positron emission tomography study. Biol Psychiatry. 2008;64(9):820–822. doi: 10.1016/j.biopsych.2008.04.025.
  • Hinwood M, Morandini J, Day TA, et al. Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex. 2012;22(6):1442–1454. doi: 10.1093/cercor/bhr229.
  • Muller N. The role of anti-inflammatory treatment in psychiatric disorders. Psychiatr Danub. 2013;25(3):292–298.
  • Torres-Platas SG, Cruceanu C, Chen GG, et al. Evidence for increased microglial priming and macrophage recruitment in the dorsal anterior cingulate white matter of depressed suicides. Brain Behav Immun. 2014;42:50–59. doi: 10.1016/j.bbi.2014.05.007.
  • Fragale JEC, Khariv V, Gregor DM, et al. Dysfunction in amygdala-prefrontal plasticity and extinction-resistant avoidance: a model for anxiety disorder vulnerability. Exp Neurol. 2016;275(Pt 1):59–68. doi: 10.1016/j.expneurol.2015.11.002.
  • Zhang JC, Yao W, Hashimoto K. Brain-derived neurotrophic factor (BDNF)-TrkB signaling in inflammation-related depression and potential therapeutic targets. Curr Neuropharmacol. 2016;14(7):721–731. doi: 10.2174/1570159x14666160119094646.
  • Guan Z, Fang J. Peripheral immune activation by lipopolysaccharide decreases neurotrophins in the cortex and hippocampus in rats. Brain Behav Immun. 2006;20(1):64–71. doi: 10.1016/j.bbi.2005.04.005.
  • Lapchak PA, Araujo DM, Hefti F. Systemic interleukin-1 beta decreases brain-derived neurotrophic factor messenger RNA expression in the rat hippocampal formation. Neuroscience. 1993;53(2):297–301. doi: 10.1016/0306-4522(93)90196-m.
  • Autry AE, Monteggia LM. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev. 2012;64(2):238–258. doi: 10.1124/pr.111.005108.
  • Lin CC, Huang TL. Brain-derived neurotrophic factor and mental disorders. Biomed J. 2020;43(2):134–142. doi: 10.1016/j.bj.2020.01.001.
  • Castren E, Monteggia LM. Brain-derived neurotrophic factor signaling in depression and antidepressant action. Biol Psychiatry. 2021;90(2):128–136. doi: 10.1016/j.biopsych.2021.05.008.
  • Bazzari AH, Bazzari FH. BDNF therapeutic mechanisms in neuropsychiatric disorders. Int J Mol Sci. 2022;23(15):8417. doi: 10.3390/ijms23158417.
  • Yan L, Lonstein JS, Nunez AA. Light as a modulator of emotion and cognition: lessons learned from studying a diurnal rodent. Horm Behav. 2019;111:78–86. doi: 10.1016/j.yhbeh.2018.09.003.
  • Leach G, Adidharma W, Yan L. Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). PLoS One. 2013;8(2):e57115. doi: 10.1371/journal.pone.0057115.
  • Leach G, Ramanathan C, Langel J, et al. Responses of brain and behavior to changing day-length in the diurnal grass rat (Arvicanthis niloticus). Neuroscience. 2013;234:31–39. doi: 10.1016/j.neuroscience.2013.01.002.
  • Ikeno T, Deats SP, Soler J, et al. Decreased daytime illumination leads to anxiety-like behaviors and HPA axis dysregulation in the diurnal grass rat (Arvicanthis niloticus). Behav Brain Res. 2016;300:77–84. doi: 10.1016/j.bbr.2015.12.004.
  • Deats SP, Adidharma W, Lonstein JS, et al. Attenuated orexinergic signaling underlies depression-like responses induced by daytime light deficiency. Neuroscience. 2014;272:252–260. doi: 10.1016/j.neuroscience.2014.04.069.
  • Soler JE, Robison AJ, Núñez AA, et al. Light modulates hippocampal function and spatial learning in a diurnal rodent species: a study using male nile grass rat (Arvicanthis niloticus). Hippocampus. 2018;28(3):189–200. doi: 10.1002/hipo.22822.
  • Soler JE, Stumpfig M, Tang Y-P, et al. Daytime light intensity modulates spatial learning and hippocampal plasticity in female nile grass rats (Arvicanthis niloticus). Neuroscience. 2019;404:175–183. doi: 10.1016/j.neuroscience.2019.01.031.
  • Lonstein JS, Linning-Duffy K, Yan L. Low daytime light intensity disrupts male copulatory behavior, and upregulates medial preoptic area steroid hormone and dopamine receptor expression, in a diurnal rodent model of seasonal affective disorder. Front Behav Neurosci. 2019;13:72. doi: 10.3389/fnbeh.2019.00072.
  • McElhinny TL, Smale L, Holekamp KE. Patterns of body temperature, activity, and reproductive behavior in a tropical murid rodent, Arvicanthis niloticus. Physiol Behav. 1997;62(1):91–96. doi: 10.1016/s0031-9384(97)00146-7.
  • Rocha FAdF, Gomes BD, Silveira LCdL, et al. Spectral sensitivity measured with electroretinogram using a constant response method. PLoS One. 2016;11(1):e0147318. doi: 10.1371/journal.pone.0147318.
  • Jacobs GH, Fenwick JA, Williams GA. Cone-based vision of rats for ultraviolet and visible lights. J Exp Biol. 2001;204(Pt 14):2439–2446. doi: 10.1242/jeb.204.14.2439.
  • Costello A, Linning-Duffy K, Vandenbrook C, et al. Effects of light therapy on sleep/wakefulness, daily rhythms, and the Central orexin system in a diurnal rodent model of seasonal affective disorder. J Affect Disord. 2023;332:299–308. doi: 10.1016/j.jad.2023.04.012.
  • Toh H, Yang C, Formenti G, et al. A haplotype-resolved genome assembly of the nile rat facilitates exploration of the genetic basis of diabetes. BMC Biol. 2022;20(1):245. doi: 10.1186/s12915-022-01427-8.
  • Costello A, Linning-Duffy K, Vandenbrook C, et al. Daytime light deficiency leads to sex- and brain region-specific neuroinflammatory responses in a diurnal rodent. Cell Mol Neurobiol. 2023;43(3):1369–1384. doi: 10.1007/s10571-022-01256-x.
  • Demirkol ME, Namlı Z, Tamam L. Efficacy of light therapy on non-seasonal depression and inflammatory markers. European J Psych. 2019;33(3):104–111. doi: 10.1016/j.ejpsy.2019.03.002.
  • Kikusui T, Ichikawa S, Mori Y. Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology. 2009;34(5):762–772. doi: 10.1016/j.psyneuen.2008.12.009.
  • Viveros M-P, Díaz F, Mateos B, et al. Maternal deprivation induces a rapid decline in circulating leptin levels and sexually dimorphic modifications in hypothalamic trophic factors and cell turnover. Horm Behav. 2010;57(4-5):405–414. doi: 10.1016/j.yhbeh.2010.01.009.
  • Weintraub A, Singaravelu J, Bhatnagar S. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res. 2010;1343:83–92. doi: 10.1016/j.brainres.2010.04.068.
  • Bakos J, Hlavacova N, Rajman M, et al. Enriched environment influences hormonal status and hippocampal brain derived neurotrophic factor in a sex dependent manner. Neuroscience. 2009;164(2):788–797. doi: 10.1016/j.neuroscience.2009.08.054.
  • Zhu S-W, Yee BK, Nyffeler M, et al. Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behav Brain Res. 2006;169(1):10–20. doi: 10.1016/j.bbr.2005.11.024.
  • Hill RA, van den Buuse M. Sex-dependent and region-specific changes in TrkB signaling in BDNF heterozygous mice. Brain Res. 2011;1384:51–60. doi: 10.1016/j.brainres.2011.01.060.
  • Sohrabji F, Miranda RC, Toran-Allerand CD. Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci USA. 1995;92(24):11110–11114. doi: 10.1073/pnas.92.24.11110.
  • Harte-Hargrove LC, Maclusky NJ, Scharfman HE. Brain-derived neurotrophic factor-estrogen interactions in the hippocampal mossy fiber pathway: implications for normal brain function and disease. Neuroscience. 2013;239:46–66. doi: 10.1016/j.neuroscience.2012.12.029.
  • Scharfman HE, MacLusky NJ. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front Neuroendocrinol. 2006;27(4):415–435. doi: 10.1016/j.yfrne.2006.09.004.
  • Tang YP, Wade J. 17beta-estradiol regulates the sexually dimorphic expression of BDNF and TrkB proteins in the song system of juvenile zebra finches. PLoS One. 2012;7(8):e43687. doi: 10.1371/journal.pone.0043687.
  • Hayley S, Du L, Litteljohn D, et al. Gender and brain regions specific differences in brain derived neurotrophic factor protein levels of depressed individuals who died through suicide. Neurosci Lett. 2015;600:12–16. doi: 10.1016/j.neulet.2015.05.052.
  • Zhu B, Dong Y, Xu Z, et al. Sleep disturbance induces neuroinflammation and impairment of learning and memory. Neurobiol Dis. 2012;48(3):348–355. doi: 10.1016/j.nbd.2012.06.022.
  • Manchanda S, Singh H, Kaur T, et al. Low-grade neuroinflammation due to chronic sleep deprivation results in anxiety and learning and memory impairments. Mol Cell Biochem. 2018;449(1-2):63–72. doi: 10.1007/s11010-018-3343-7.
  • Patel SR, Zhu X, Storfer-Isser A, et al. Sleep duration and biomarkers of inflammation. Sleep. 2009;32(2):200–204. doi: 10.1093/sleep/32.2.200.
  • Irwin MR, Carrillo C, Olmstead R. Sleep loss activates cellular markers of inflammation: sex differences. Brain Behav Immun. 2010;24(1):54–57. doi: 10.1016/j.bbi.2009.06.001.
  • Irwin MR, Wang M, Campomayor CO, et al. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch Intern Med. 2006;166(16):1756–1762. doi: 10.1001/archinte.166.16.1756.
  • McAlpine CS, et al. Sleep exerts lasting effects on hematopoietic stem cell function and diversity. J Exp Med. 2022;219(11):e20220081. doi:10.1084/jem.20220081.
  • Pak VM, Onen S-H, Bliwise DL, et al. Sleep disturbances in MCI and AD: neuroinflammation as a possible mediating pathway. Front Aging Neurosci. 2020;12:69. doi: 10.3389/fnagi.2020.00069.
  • Benington JH, Frank MG. Cellular and molecular connections between sleep and synaptic plasticity. Prog Neurobiol. 2003;69(2):71–101. doi: 10.1016/s0301-0082(03)00018-2.
  • Wang G, Grone B, Colas D, et al. Synaptic plasticity in sleep: learning, homeostasis and disease. Trends Neurosci. 2011;34(9):452–463. doi: 10.1016/j.tins.2011.07.005.
  • Tononi G, Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron. 2014;81(1):12–34. doi: 10.1016/j.neuron.2013.12.025.
  • da Costa Souza A, Ribeiro S. Sleep deprivation and gene expression. Curr Top Behav Neurosci. 2015;25:65–90.
  • Ardeshiri MR, Hosseinmardi N, Akbari E. Orexin 1 and orexin 2 receptor antagonism in the basolateral amygdala modulate long-term potentiation of the population spike in the perforant path-dentate gyrus-evoked field potential in rats. Neurobiol Learn Mem. 2018;149:98–106. doi: 10.1016/j.nlm.2018.02.024.
  • Chen XY, Chen L, Du YF. Orexin-A increases the firing activity of hippocampal CA1 neurons through orexin-1 receptors. J Neurosci Res. 2017;95(7):1415–1426. doi: 10.1002/jnr.23975.
  • Gao XB, Wang AH. Experience-dependent plasticity in hypocretin/orexin neurones: re-setting arousal threshold. Acta Physiol. 2010;198(3):251–262. doi: 10.1111/j.1748-1716.2009.02047.x.
  • Gotter AL, et al. Orexin receptors as therapeutic drug targets. Prog Brain Res. 2012;198:163–188.
  • Butterick TA, Nixon JP, Billington CJ, et al. Orexin a decreases lipid peroxidation and apoptosis in a novel hypothalamic cell model. Neurosci Lett. 2012;524(1):30–34. doi: 10.1016/j.neulet.2012.07.002.
  • Kooshki R, Abbasnejad M, Esmaeili-Mahani S, et al. The effect of CA1 administration of orexin-A on hippocampal expression of COX-2 and BDNF in a rat model of orofacial pain. Arq Neuropsiquiatr. 2018;76(9):603–608. doi: 10.1590/0004-282X20180099.
  • Xiong X, White RE, Xu L, et al. Mitigation of murine focal cerebral ischemia by the hypocretin/orexin system is associated with reduced inflammation. Stroke. 2013;44(3):764–770. doi: 10.1161/STROKEAHA.112.681700.
  • Duffy CM, Yuan C, Wisdorf LE, et al. Role of orexin a signaling in dietary palmitic acid-activated microglial cells. Neurosci Lett. 2015;606:140–144. doi: 10.1016/j.neulet.2015.08.033.
  • Modi HR, Wang Q, Gd S, et al. Intranasal post-cardiac arrest treatment with orexin-A facilitates arousal from coma and ameliorates neuroinflammation. PLoS One. 2017;12(9):e0182707. doi: 10.1371/journal.pone.0182707.
  • Cohen S, Matar MA, Vainer E, et al. Significance of the orexinergic system in modulating stress-related responses in an animal model of post-traumatic stress disorder. Transl Psychiatry. 2020;10(1):10. doi: 10.1038/s41398-020-0698-9.
  • Yamada N, Katsuura G, Tatsuno I, et al. Orexins increase mRNA expressions of neurotrophin-3 in rat primary cortical neuron cultures. Neurosci Lett. 2009;450(2):132–135. doi: 10.1016/j.neulet.2008.11.028.
  • Toor B, et al. Sleep, orexin and cognition. Front Neurol Neurosci. 2021;45:38–51.
  • Lonstein JS, Linning-Duffy K, Tang Y, et al. Impact of daytime light intensity on the Central orexin (hypocretin) system of a diurnal rodent (Arvicanthis niloticus). Eur J Neurosci. 2021;54:4167–4181. doi: 10.1111/ejn.15248.