Top

Published in:

01-07-2018 | Original Article

Light rescues circadian behavior and brain dopamine abnormalities in diurnal rodents exposed to a winter-like photoperiod

Authors: Jacob Itzhacki, Daniel Clesse, Yannick Goumon, Eus J. Van Someren, Jorge Mendoza

Published in: Brain Structure and Function | Issue 6/2018

Abstract

Seasonal affective disorder (SAD), beyond mood changes, is characterized by alterations in daily rhythms of behavior and physiology. The pathophysiological conditions of SAD involve changes in day length and its first-line treatment is bright light therapy. Animal models using nocturnal rodents have been studied to elucidate the neurobiological mechanisms of depression, but might be ill suited to study the therapeutic effects of light in SAD since they exhibit light-aversive responses. Here Arvicanthis ansorgei, a diurnal rodent, was used to determine behavioral, molecular and brain dopamine changes in response to exposure to a winter-like photoperiod consisting of a light–dark cycle with 8 h of light, under diminished light intensity, and 16 h of darkness. Furthermore, we evaluated whether timed-daily bright light exposure has an effect on behavior and brain physiology of winter-like exposed animals. Arvicanthis under a winter-like condition showed alterations in the synchronization of the locomotor activity rhythm to the light–dark cycle. Moreover, alterations in day–night activity of dopaminergic neurotransmission were revealed in the nucleus accumbens and the dorsal striatum, and in the day–night clock gene expression in the suprachiasmatic nucleus. Interestingly, whereas dopamine disturbances were reversed in animals exposed to daily light at early or late day, altered phase of the daily rhythm of locomotion was reverted only in animals exposed to light at the late day. Moreover, Per2 gene expression in the SCN was also affected by light exposure at late day in winter-like exposed animals. These findings suggest that light induces effects on behavior by mechanisms that rely on both circadian and rhythm-independent pathways influencing the dopaminergic circuitry. This last point might be crucial for understanding the mechanisms of non-pharmacological treatment in SAD.

Abilio VC, Freitas FM, Dolnikoff MS, Castrucci AM, Frussa-Filho R (1999) Effects of continuous exposure to light on behavioral dopaminergic supersensitivity. Biol Psychiatry 45(12):1622–1629CrossRefPubMed

Adidharma W, Leach G, Yan L (2012) Orexinergic signaling mediates light-induced neuronal activation in the dorsal raphe nucleus. Neuroscience 220:201–207. https://doi.org/10.1016/j.neuroscience.2012.06.020 CrossRefPubMedPubMedCentral

Albrecht U (2017) Molecular mechanisms in mood regulation involving the Circadian Clock. Front Neurol 8:30. https://doi.org/10.3389/fneur.2017.00030 CrossRefPubMedPubMedCentral

Ashkenazy-Frolinger T, Kronfeld-Schor N, Juetten J, Einat H (2010) It is darkness and not light: Depression-like behaviors of diurnal unstriped Nile grass rats maintained under a short photoperiod schedule. J Neurosci Methods 186(2):165–170. https://doi.org/10.1016/j.jneumeth.2009.11.013 CrossRefPubMed

Bagchi SP (1998) Striatal and urinary DOPAC/DA ratio may indicate a long-lasting DA release enhancement by MPP + and MPTP. Neurochem Res 23(2):127–134CrossRefPubMed

Baker PM, Mizumori SJY (2017) Control of behavioral flexibility by the lateral habenula. Pharmacol Biochem Behav. https://doi.org/10.1016/j.pbb.2017.07.012 CrossRefPubMed

Berman K, Lam RW, Goldner EM (1993) Eating attitudes in seasonal affective disorder and bulimia nervosa. J Affect Disord 29(4):219–225CrossRefPubMed

Berridge KC, Kringelbach ML (2013) Neuroscience of affect: brain mechanisms of pleasure and displeasure. Curr Opin Neurobiol 23(3):294–303. https://doi.org/10.1016/j.conb.2013.01.017 CrossRefPubMedPubMedCentral

Brene S, Bjornebekk A, Aberg E, Mathe AA, Olson L, Werme M (2007) Running is rewarding and antidepressive. Physiol Behav 92(1–2):136–140. https://doi.org/10.1016/j.physbeh.2007.05.015 CrossRefPubMedPubMedCentral

Burgess HJ, Fogg LF, Young MA, Eastman CI (2004) Bright light therapy for winter depression—Is phase advancing beneficial? Chronobiol Int 21(4–5):759–775CrossRefPubMed

Caldelas I, Poirel VJ, Sicard B, Pevet P, Challet E (2003) Circadian profile and photic regulation of clock genes in the suprachiasmatic nucleus of a diurnal mammal Arvicanthis ansorgei. Neuroscience 116(2):583–591CrossRefPubMed

Cawley EI, Park S, aan het Rot M, Sancton K, Benkelfat C, Young SN, Boivin DB, Leyton M (2013) Dopamine and light: dissecting effects on mood and motivational states in women with subsyndromal seasonal affective disorder. J Psychiatry Neurosci 38(6):388–397. https://doi.org/10.1503/jpn.120181 CrossRefPubMedPubMedCentral

Dahl K, Avery DH, Lewy AJ, Savage MV, Brengelmann GL, Larsen LH, Vitiello MV, Prinz PN (1993) Dim light melatonin onset and circadian temperature during a constant routine in hypersomnic winter depression. Acta Psychiatr Scand 88(1):60–66CrossRefPubMed

Deats SP, Adidharma W, Yan L (2015) Hypothalamic dopaminergic neurons in an animal model of seasonal affective disorder. Neurosci Lett 602:17–21. https://doi.org/10.1016/j.neulet.2015.06.038 CrossRefPubMedPubMedCentral

Deibel SH, Hong NS, Himmler SM, McDonald RJ (2014) The effects of chronic photoperiod shifting on the physiology of female Long-Evans rats. Brain Res Bull 103:72–81. https://doi.org/10.1016/j.brainresbull.2014.03.001 CrossRefPubMed

Diehl DJ, Mintun MA, Kupfer DJ, Moore RY (1994) A likely in vivo probe of human circadian timing system function using PET. Biol Psychiatry 36(8):562–565CrossRefPubMed

Dremencov E, El Mansari M, Blier P (2009) Effects of sustained serotonin reuptake inhibition on the firing of dopamine neurons in the rat ventral tegmental area. J Psychiatry Neurosci 34(3):223–229PubMedPubMedCentral

Eisenberg DP, Kohn PD, Baller EB, Bronstein JA, Masdeu JC, Berman KF (2010) Seasonal effects on human striatal presynaptic dopamine synthesis. J Neurosci 30(44):14691–14694. https://doi.org/10.1523/JNEUROSCI.1953-10.2010 CrossRefPubMedPubMedCentral

Gonzalez MM, Aston-Jones G (2008) Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats. Proc Natl Acad Sci USA 105(12):4898–4903. https://doi.org/10.1073/pnas.0703615105 CrossRefPubMedPubMedCentral

Grippo RM, Purohit AM, Zhang Q, Zweifel LS, Guler AD (2017) Direct midbrain dopamine input to the suprachiasmatic nucleus accelerates circadian entrainment. Curr Biol. https://doi.org/10.1016/j.cub.2017.06.084 PubMedCrossRefPubMedCentral

Hampp G, Ripperger JA, Houben T, Schmutz I, Blex C, Perreau-Lenz S, Brunk I, Spanagel R, Ahnert-Hilger G, Meijer JH, Albrecht U (2008) Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol 18(9):678–683. https://doi.org/10.1016/j.cub.2008.04.012 CrossRefPubMed

Hartikainen P, Soininen H, Reinikainen KJ, Sirvio J, Soikkeli R, Riekkinen PJ (1991) Neurotransmitter markers in the cerebrospinal fluid of normal subjects. Effects of aging and other confounding factors. J Neural Transm Gen Sect 84(1–2):103–117CrossRefPubMed

Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM (2006) Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497(3):326–349. https://doi.org/10.1002/cne.20970 CrossRefPubMedPubMedCentral

Hood S, Cassidy P, Cossette MP, Weigl Y, Verwey M, Robinson B, Stewart J, Amir S (2010) Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J Neurosci 30(42):14046–14058. https://doi.org/10.1523/JNEUROSCI.2128-10.2010 CrossRefPubMed

Krivisky K, Ashkenazy T, Kronfeld-Schor N, Einat H (2011) 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. Neuropsychobiology 63(3):191–196. https://doi.org/10.1159/000321805 CrossRefPubMed

Lam RW, Levitan RD (2000) Pathophysiology of seasonal affective disorder: a review. J Psychiatry Neurosci 25(5):469–480PubMedPubMedCentral

Lazzerini Ospri L, Prusky G, Hattar S (2017) Mood, the circadian system, and melanopsin retinal ganglion cells. Annu Rev Neurosci 40:539–556. https://doi.org/10.1146/annurev-neuro-072116-031324 CrossRefPubMed

Leach G, Adidharma W, Yan L (2013a) Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). PLoS One 8(2):e57115. https://doi.org/10.1371/journal.pone.0057115 CrossRefPubMedPubMedCentral

Leach G, Ramanathan C, Langel J, Yan L (2013b) Responses of brain and behavior to changing day-length in the diurnal grass rat (Arvicanthis niloticus). Neuroscience 234:31–39. https://doi.org/10.1016/j.neuroscience.2013.01.002 CrossRefPubMedPubMedCentral

LeGates TA, Fernandez DC, Hattar S (2014) Light as a central modulator of circadian rhythms, sleep and affect. Nat Rev Neurosci 15(7):443–454. https://doi.org/10.1038/nrn3743 CrossRefPubMedPubMedCentral

Lewy AJ, Bauer VK, Cutler NL, Sack RL, Ahmed S, Thomas KH, Blood ML, Jackson JM (1998) Morning vs evening light treatment of patients with winter depression. Arch Gen Psychiatry 55(10):890–896CrossRefPubMed

Lewy AJ, Lefler BJ, Emens JS, Bauer VK (2006) The circadian basis of winter depression. Proc Natl Acad Sci USA 103(19):7414–7419. https://doi.org/10.1073/pnas.0602425103 CrossRefPubMedPubMedCentral

Lieverse R, Van Someren EJ, Nielen MM, Uitdehaag BM, Smit JH, Hoogendijk WJ (2011) Bright light treatment in elderly patients with nonseasonal major depressive disorder: a randomized placebo-controlled trial. Arch Gen Psychiatry 68(1):61–70. https://doi.org/10.1001/archgenpsychiatry.2010.183 CrossRefPubMed

Logan RW, Edgar N, Gillman AG, Hoffman D, Zhu X, McClung CA (2015) Chronic stress induces brain region-specific alterations of molecular rhythms that correlate with depression-like behavior in mice. Biol Psychiatry 78(4):249–258. https://doi.org/10.1016/j.biopsych.2015.01.011 CrossRefPubMedPubMedCentral

Luo AH, Aston-Jones G (2009) Circuit projection from suprachiasmatic nucleus to ventral tegmental area: a novel circadian output pathway. Eur J Neurosci 29(4):748–760. https://doi.org/10.1111/j.1460-9568.2008.06606.x CrossRefPubMed

McCune AM, Lundgren JD (2015) Bright light therapy for the treatment of night eating syndrome: A pilot study. Psychiatry Res 229(1–2):577–579. https://doi.org/10.1016/j.psychres.2015.07.079 CrossRefPubMed

Mendoza J (2017) Circadian neurons in the lateral habenula: clocking motivated behaviors. Pharmacol Biochem Behav. https://doi.org/10.1016/j.pbb.2017.06.013 CrossRefPubMed

Mendoza J, Challet E (2014) Circadian insights into dopamine mechanisms. Neuroscience 282:230–242. https://doi.org/10.1016/j.neuroscience.2014.07.081 CrossRefPubMed

Mendoza J, Gourmelen S, Dumont S, Sage-Ciocca D, Pevet P, Challet E (2012) Setting the main circadian clock of a diurnal mammal by hypocaloric feeding. J Physiol 590(13):3155–3168. https://doi.org/10.1113/jphysiol.2012.230300 CrossRefPubMedPubMedCentral

Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359(2):221–238. https://doi.org/10.1002/cne.903590204 CrossRefPubMed

Moorman DE, Aston-Jones G (2010) Orexin/hypocretin modulates response of ventral tegmental dopamine neurons to prefrontal activation: diurnal influences. J Neurosci 30(46):15585–15599. https://doi.org/10.1523/JNEUROSCI.2871-10.2010 CrossRefPubMedPubMedCentral

Neumeister A, Konstantinidis A, Praschak-Rieder N, Willeit M, Hilger E, Stastny J, Kasper S (2001) Monoaminergic function in the pathogenesis of seasonal affective disorder. Int J Neuropsychopharmacol 4(4):409–420. https://doi.org/10.1017/S1461145701002644 CrossRefPubMed

Opmeer EM, Kortekaas R, Aleman A (2010) Depression and the role of genes involved in dopamine metabolism and signalling. Prog Neurobiol 92(2):112–133. https://doi.org/10.1016/j.pneurobio.2010.06.003 CrossRefPubMed

Partonen T, Treutlein J, Alpman A, Frank J, Johansson C, Depner M, Aron L, Rietschel M, Wellek S, Soronen P, Paunio T, Koch A, Chen P, Lathrop M, Adolfsson R, Persson ML, Kasper S, Schalling M, Peltonen L, Schumann G (2007) Three circadian clock genes Per2, Arntl, and Npas2 contribute to winter depression. Ann Med 39(3):229–238. https://doi.org/10.1080/07853890701278795 CrossRefPubMed

Pinchasov BB, Shurgaja AM, Grischin OV, Putilov AA (2000) Mood and energy regulation in seasonal and non-seasonal depression before and after midday treatment with physical exercise or bright light. Psychiatry Res 94(1):29–42CrossRefPubMed

Raoux N, Benoit O, Dantchev N, Denise P, Franc B, Allilaire JF, Widlocher D (1994) Circadian pattern of motor activity in major depressed patients undergoing antidepressant therapy: relationship between actigraphic measures and clinical course. Psychiatry Res 52(1):85–98CrossRefPubMed

Rosenthal NE, Sack DA, Gillin JC, Lewy AJ, Goodwin FK, Davenport Y, Mueller PS, Newsome DA, Wehr TA (1984) Seasonal affective disorder. A description of the syndrome and preliminary findings with light therapy. Arch Gen Psychiatry 41(1):72–80CrossRefPubMed

Ruger M, St Hilaire MA, Brainard GC, Khalsa SB, Kronauer RE, Czeisler CA, Lockley SW (2013) Human phase response curve to a single 6.5 h pulse of short-wavelength light. J Physiol 591(1):353–363. https://doi.org/10.1113/jphysiol.2012.239046 CrossRefPubMed

Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14(9):609–625. https://doi.org/10.1038/nrn3381 CrossRefPubMed

Salaberry NL, Mendoza J (2015) Insights into the role of the habenular circadian clock in addiction. Front Psychiatry 6:179. https://doi.org/10.3389/fpsyt.2015.00179 PubMedCrossRef

Shuboni DD, Cramm S, Yan L, Nunez AA, Smale L (2012) Acute behavioral responses to light and darkness in nocturnal Mus musculus and diurnal Arvicanthis niloticus. J Biol Rhythms 27(4):299–307. https://doi.org/10.1177/0748730412449723 CrossRefPubMed

Shuboni DD, Cramm SL, Yan L, Ramanathan C, Cavanaugh BL, Nunez AA, Smale L (2015) Acute effects of light on the brain and behavior of diurnal Arvicanthis niloticus and nocturnal Mus musculus. Physiol Behav 138:75–86. https://doi.org/10.1016/j.physbeh.2014.09.006 CrossRefPubMed

St Hilaire MA, Gooley JJ, Khalsa SB, Kronauer RE, Czeisler CA, Lockley SW (2012) Human phase response curve to a 1 h pulse of bright white light. J Physiol 590(13):3035–3045. https://doi.org/10.1113/jphysiol.2012.227892 CrossRefPubMedPubMedCentral

Stahl SM, Lee-Zimmerman C, Cartwright S, Morrissette DA (2013) Serotonergic drugs for depression and beyond. Curr Drug Targets 14(5):578–585CrossRefPubMed

Tavolaro FM, Thomson LM, Ross AW, Morgan PJ, Helfer G (2015) Photoperiodic effects on seasonal physiology, reproductive status and hypothalamic gene expression in young male F344 rats. J Neuroendocrinol 27(2):79–87. https://doi.org/10.1111/jne.12241 CrossRefPubMedPubMedCentral

Teicher MH, Glod CA, Magnus E, Harper D, Benson G, Krueger K, McGreenery CE (1997) Circadian rest-activity disturbances in seasonal affective disorder. Arch Gen Psychiatry 54(2):124–130CrossRefPubMed

Terman M, Terman JS (2005) Light therapy for seasonal and nonseasonal depression: efficacy, protocol, safety, and side effects. CNS Spectr 10(8):647–663 (quiz 672)CrossRefPubMed

Terman M, Terman JS, Quitkin FM, Cooper TB, Lo ES, Gorman JM, Stewart JW, McGrath PJ (1988) Response of the melatonin cycle to phototherapy for seasonal affective disorder. Short note. J Neural Transm 72(2):147–165CrossRefPubMed

Tsai HY, Chen KC, Yang YK, Chen PS, Yeh TL, Chiu NT, Lee IH (2011) Sunshine-exposure variation of human striatal dopamine D(2)/D(3) receptor availability in healthy volunteers. Prog Neuropsychopharmacol Biol Psychiatry 35(1):107–110. https://doi.org/10.1016/j.pnpbp.2010.09.014 CrossRefPubMed

Verwey M, Dhir S, Amir S (2016) Circadian influences on dopamine circuits of the brain: regulation of striatal rhythms of clock gene expression and implications for psychopathology and disease. F1000Res. https://doi.org/10.12688/f1000research.9180.1 PubMedPubMedCentralCrossRef

Volkers AC, Tulen JH, Van Den Broek WW, Bruijn JA, Passchier J, Pepplinkhuizen L (2002) 24-Hour motor activity after treatment with imipramine or fluvoxamine in major depressive disorder. Eur Neuropsychopharmacol 12(4):273–278CrossRefPubMed

Willeit M, Sitte HH, Thierry N, Michalek K, Praschak-Rieder N, Zill P, Winkler D, Brannath W, Fischer MB, Bondy B, Kasper S, Singer EA (2008) Enhanced serotonin transporter function during depression in seasonal affective disorder. Neuropsychopharmacology 33(7):1503–1513. https://doi.org/10.1038/sj.npp.1301560 CrossRefPubMed

Wirz-Justice A, Graw P, Krauchi K, Gisin B, Jochum A, Arendt J, Fisch HU, Buddeberg C, Poldinger W (1993) Light therapy in seasonal affective disorder is independent of time of day or circadian phase. Arch Gen Psychiatry 50(12):929–937CrossRefPubMed

Title: Light rescues circadian behavior and brain dopamine abnormalities in diurnal rodents exposed to a winter-like photoperiod
Authors: Jacob Itzhacki
Daniel Clesse
Yannick Goumon
Eus J. Van Someren
Jorge Mendoza
Publication date: 01-07-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1655-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Light rescues circadian behavior and brain dopamine abnormalities in diurnal rodents exposed to a winter-like photoperiod

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2018

The neural correlates of arithmetic difficulty depend on mathematical ability: evidence from combined fNIRS and ERP

Influence of the DRD2/ANKK1 Taq1A polymorphism on caudate volume in older adults without dementia

Paraventricular hypothalamic and amygdalar CRF neurons synapse in the external globus pallidus

Circuit-selective properties of glutamatergic inputs to the rat prelimbic cortex and their alterations in neuropathic pain

Linguistic and motor representations of everyday complex actions: an fNIRS investigation

How do cortico-striatal projections impact on downstream pallidal circuitry?