Abstract
Circadian rhythms are strongly associated with affective disorders and recent studies have suggested utilization of diurnal rodents as model animal for circadian rhythms-related domains of these disorders. Previous work with the diurnal fat sand rat and Nile grass rat demonstrated that short photoperiod conditions result in behavioral changes including anxiety- and depression-like behavior. The present study examined the effect of manipulating day length on activity rhythms and behavior of the diurnal degu. Animals were housed for 3 weeks under either a short photoperiod (5-h:19-h LD) or a neutral photoperiod (12-h:12-h LD) and then evaluated by sweet solution test and the forced swim test for depression-like behavior, and in the light/dark box and open field for anxiety-like behavior. Results indicate that short photoperiod induced depression-like behavior in the forced swim test and the sweet solution preference test and anxiety-like behavior in the open field compared with animals maintained in a neutral photoperiod. No effects were shown in the light/dark box. Short photoperiod-acclimated degu showed reduced total activity duration and activity was not restricted to the light phase. The present study further supports the utilization of diurnal rodents to model circadian rhythms-related affective change. Beyond the possible diversity in the mechanisms underlying diurnality in different animals, there are now evidences that in three different diurnal species, the fat sand rat, the grass Nile rat and the degu, shortening of photoperiod results in the appearance of anxiety- and depression-like behaviors.
Similar content being viewed by others
References
Abílio VC, Freitas FM, Dolnikoff MS, Castrucci AM, Frussa-Filho R (1999) Effects of continuous exposure to light on behavioral dopaminergic supersensitivity. Biol Psychiatry 45:1622–1629
Abílio VC, Vera JAR, Ferreira LSM, Duarte CRM, Martins CR, Torres-Leite D, Ribeiro Rde A, Frussa-Filho R (2003) Effects of melatonin on behavioral dopaminergic supersensitivity. Life Sci 72:3003–3015
Albrecht U (2010) Circadian clocks in mood-related behaviors. Ann Med 42:241–251
Arble DM, Bass J, Laposky AD, Vitaterna MH, Turek FW (2009) Circadian timing of food intake contributes to weight gain. Obesity. (Silver Spring) 17:2100–2102
Ashkenazy T, Einat H, Kronfeld-Schor N (2009a) Effects of bright light treatment on depression- and anxiety-like behaviors of diurnal rodents maintained on a short daylight schedule. Behav Brain Res 201:343–346
Ashkenazy T, Einat H, Kronfeld-Schor N (2009b) We are in the dark here: induction of depression- and anxiety-like behaviours in the diurnal fat sand rat, by short daylight or melatonin injections. Int J Neuropsychopharmacol 12:83–93
Ashkenazy-Frolinger T, Kronfeld-Schor N, Juetten J, Einat H (2009) It is darkness and not light: depression-like behaviors of diurnal unstriped Nile grass rats maintained under a short photoperiod schedule. J Neurosci Methods 186:165–170
Avery DH, Dahl K, Savage MV, Brengelmann GL, Larsen LH, Kenny MA, Eder DN, Vitiello MV, Prinz PN (1997) Circadian temperature and cortisol rhythms during a constant routine are phase-delayed in hypersomnic winter depression. Biol Psychiatry 41:1109–1123
Bacigalupe LD, Rezende EL (2003) Activity and space use by degus: a trade-off between thermal conditions and food availability? J Mammal 84:311–318
Barak O, Kronfeld-Schor N (2013) Activity rhythms and Masking response in the diurnal Fat Sand Rat under laboratory conditions. Chronobiol Int 30(9):1123–1134
Benedetti F, Barbini B, Campori E, Fulgosi MC, Pontiggia A, Colombo C (2001) Sleep phase advance and lithium to sustain the antidepressant effect of total sleep deprivation in bipolar depression: new findings supporting the internal coincidence model? J Psychiatr Res 35:323–329
Benedetti F, Serretti A, Colombo C, Barbini B, Lorenzi C, Campori E, Smeraldi E (2003) Influence of CLOCK gene polymorphism on circadian mood fluctuation and illness recurrence in bipolar depression. Am J Med Genet B Neuropsychiatr Genet 123B:23–26
Berle JO, Hauge ER, Oedegaard KJ, Holsten F, Fasmer OB (2010) Actigraphic registration of motor activity reveals a more structured behavioural pattern in schizophrenia than in major depression. BMC Res Notes 3:149
Bilu C, Kronfeld-Schor N (2013) Effects of circadian phase and melatonin injection on anxiety-like behavior in nocturnal and diurnal rodents. Chronobiol Int 30:828–836
Bolker J (2012) Model organisms: there’s more to life than rats and flies. Nature 491:31–33
Bunney WE, Bunney BG (2000) Molecular clock genes in man and lower animals: possible implications for circadian abnormalities in depression. Neuropsychopharmacology 22:335–345
Challet E (2007) Entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. Endocrinology 148:5648–5655
Cohen R, Kronfeld-Schor N (2006) Individual variability and photic entrainment of circadian rhythms in golden spiny mice. Physiol Behav 87:563–574
Cohen R, Smale L, Kronfeld-Schor N (2009) Plasticity of circadian activity and body temperature rhythms in golden spiny mice. Chronobiol Int 26:430–446
Cohen R, Kronfeld-Schor N, Ramanathan C, Baumgras A, Smale L (2010a) The substructure of the suprachiasmatic nucleus: similarities between nocturnal and diurnal spiny mice. Brain Behav Evol 75:9–22
Cohen R, Smale L, Kronfeld-Schor N (2010b) Masking and temporal niche switches in spiny mice. J Biol Rhythms 25:47–52
Colonnello V, Iacobucci P, Anderson MP, Panksepp J (2011a) Brief periods of positive peer interactions mitigate the effects of total social isolation in young Octodon degus. Dev Psychobiol 53:280–290
Colonnello V, Iacobucci P, Fuchs T, Newberry R, Panksepp J (2011b) Octodon degus. A useful animal model for social-affective neuroscience research: basic description of separation distress, social attachment and play. Neurosci Behav Rev 35:1854–1863
Crawley JN (1981) Neuropharmacologic specificity of a simple animal model for the behavioral actions of benzodiazepines. Pharmacol Biochem Behav 15:695–699
Crawley JN (2007) Behavioral neuroscience. In: Crawley JN, McKay J (eds) Current protocols in neuroscience. Wiley Interscience, New York
Cryan JF, Holmes A (2005) The ascent of the mouse: advances in modeling human depression and anxiety. Nat Rev Drug Discov 4:77–790
Cuesta M, Mendoza J, Clesse D, Pévet P, Challet E (2008) Serotonergic activation potentiates light resetting of the main circadian clock and alters clock gene expression in a diurnal rodent. Exp Neurol 210:501–513
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 88:60–66
Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549
Dietzel M, Saletu B, Lesch OM, Sieghart W, Schjerve M (1986) Light treatment in depressive illness. Polysomnographic, psychometric and neuroendocrinological findings. Eur Neurol 25(Suppl 2):93–103
Eilam D, Dayan T, Ben-Elyahu S, Schulman II, Shefer G, Hendrie CA (1999) Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim Behav 58:1085–1093
Einat H (2010) Strategies for the development of animal models for bipolar disorder: new opportunities and new challenges. In: Zarate CA, Manji HK (eds) Behavioral neurobiology of bipolar disorder and its treatment. Current topics in behavioral neuroscience, vol 5. Springer, Berlin, pp 69–87
Einat H, Kronfeld-Schor N (2009) Utilizing diurnal model animals in the study of depression. Front Neurosci 3:242–243
Einat H, Kronfeld-Schor N, Eilam D (2006) Sand rats see the light: short photoperiod induces a depression-like response in a diurnal rodent. Behav Brain Res 173:153–157
Flaisher-Grinberg S, Overgaard S, Einat H (2009) Attenuation of high sweet solution preference by mood stabilizers: a possible mouse model for the increased reward-seeking domain of mania. J Neurosci Methods 177:44–50
Flaisher-Grinberg S, Gampetro DR, Kronfeld-Schor N, Einat H (2011) Inconsistent effects of photoperiod manipulations in tests for affective-like changes in mice: implications for the selection of appropriate model animals. Behav Pharmacol 22:23–30
Genaro G, Schmidek WR (2000) Exploratory activity of rats in three different environments. Ethology 106:849–859
Giedke H, Schwärzler F (2002) Therapeutic use of sleep deprivation in depression. Sleep Med Rev 6:361–377
Goel N, Lee TM (1995) Sex differences and effects of social cues on daily rhythms following phase advances in Octodon degus. Physiol Behav 58:205–213
Golden RN, Gaynes BN, Ekstrom RD, Hamer RM, Jacobsen FM et al (2005) The efficacy of light therapy in the treatment of mood disorders: a review and meta-analysis of the evidence. Am J Psychiatry 162(4):656–662
Gordijn MC, Beersma DG, Bouhuys AL, Reinink E, Van den Hoofdakker RH (1994) A longitudinal study of diurnal mood variation in depression; characteristics and significance. J Affect Disord 31:261–273
Gutman R, Dayan T, Levy O, Schubert I, Kronfeld-Schor N (2011) The Effect of the lunar cycle on fecal cortisol metabolite levels and foraging ecology of nocturnally and diurnally active Spiny mice. PLoS One 6:e23446
Hagenauer MH, Lee TM (2008) Circadian organization of the diurnal Caviomorph rodent, Octodon degus. Biol Rhythm Res 39:269–289
Hauge ER, Berle JØ, Oedegaard KJ, Holsten F, Fasmer OB (2011) Nonlinear analysis of motor activity shows differences between schizophrenia and depression: a study using Fourier analysis and sample entropy. PLoS One 6:e16291
Hendrie CA, Weiss SM, Eilam D (1996) Exploration and predation models of anxiety: evidence from laboratory and wild species. Pharmacol Biochem Behav 54:13–20
Hendrie CA, Weiss SM, Eilam D (1998) Behavioural response of wild rodents to the calls of an owl: a comparative study. J Zool 245:439–446
Jawed S, Kim B, Ottenhof T, Brown GM, Werstiuk ES, Niles LP (2007) Human melatonin MT1 receptor induction by valproic acid and its effects in combination with melatonin on MCF-7 breast cancer cell proliferation. Eur J Pharmacol 560:17–22
Johansson C, Willeit M, Smedh C, Ekholm J, Paunio T, Kieseppä T, Lichtermann D, Praschak-Rieder N, Neumeister A, Nilsson L-G, Kasper S, Peltonen L, Adolfsson R, Schalling M, Partonen T (2003) Circadian clock-related polymorphisms in seasonal affective disorder and their relevance to diurnal preference. Neuropsychopharmacology 28:734–739
Kara NZ, Einat H (2013) Rodent models for mania: practical considerations. Cell, tissue research. (Special issue, rodent models of psychiatric disorders: practical considerations), advance online publication. http://www.ncbi.nlm.nih.gov/pubmed/23504091
Karatsoreos IN, Bhagat S, Bloss EB, Morrison JH, McEwen BS (2011) Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci USA 108:1657–1662
Kas MJ, Edgar DM (1998) Crepuscular rhythms of EEG sleep–wake in a hystricomorph rodent, Octodon degus. J Biol Rhythms 13:9–17
Kas MJ, Edgar DM (1999) A nonphotic stimulus inverts the diurnal–nocturnal phase preference in Octodon degus. J Neurosci 19:328–333
Kenagy GJ, Vasquez RA (2004) Microstructure of summer activity bouts of degus in a thermally heterogeneous habitat. J Mammal 85:260–267
Kenagy GJ, Nespolo RF, Vasquez RA, Bozinovic F (2002a) Daily and seasonal limits of time and temperature to activity of degus. Revista Chilena Hist Nat 75:567–581
Kenagy GJ, Vásquez RA, Nespolo RF, Bozinovic F (2002b) A time–energy analysis of daytime surface activity in degus, Octodon degus. Revista Chilena Hist Nat 75:149–156
Kripke DF (1998) Light treatment for nonseasonal depression: speed, efficacy, and combined treatment. J Affect Disord 49:109–117
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 63:191–196
Krivisky K, Einat H, Kronfeld-Schor N (2012) Effects of morning compared with evening bright light administration to ameliorate short-photoperiod induced depression- and anxiety-like behaviors in a diurnal rodent model. J Neural Transm 119:1241–1248
Kronfeld-Schor N, Einat H (2012) Circadian rhythms and depression: human psychopathology and animal models. Neuropharmacology 62:101–114
Kronfeld-Schor N, Haim A, Dayan T, Zisapel N, Klingenspor M, Heldmaier G (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol Biochem Zool 73:37–44
Kronfeld-Schor N, Dayan T, Elvert R, Haim A, Zisapel N, Heldmaier G (2001) On the use of the time axis for ecological separation: diel rhythms as an evolutionary constraint. Am Nat 158:451–457
Lam RW, Levitan RD (2000) Pathophysiology of seasonal affective disorder: a review. J Psychiatry Neurosci 25:469–480
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:e57115
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
Lee TM (2004) Octodon degus: a diurnal, social, and long-lived rodent. ILAR J 45:14–24
Le-Niculescu H, McFarland MJ, Ogden CA, Balaraman Y, Patel S, Tan J, Rodd ZA, Paulus M, Geyer MA, Edenberg HJ, Glatt SJ, Faraone SV, Nurnberger JI, Kuczenski R, Tsuang MT, Niculescu AB (2008) Phenomic, convergent functional genomic, and biomarker studies in a stress-reactive genetic animal model of bipolar disorder and co-morbid alcoholism. Am J Med Genet B Neuropsychiatr Genet 147B:134–166
Lenox RH, Gould TD, Manji HK (2002) Endophenotypes in bipolar disorder. Am J Med Genet 114:391–406
Lewy AJ, Bauer VK, Cutler NL, Sack RL, Ahmed S et al (1998) Morning vs evening light treatment of patients with winter depression. Arch Gen Psychiatry 55(10):890–896
Li JZ, Bunney BG, Meng F, Hagenauer MH, Walsh DM, Vawter MP, Evans SJ, Choudary PV, Cartagena P, Barchas JD, Schatzberg AF, Jones EG, Myers RM, Watson SJ Jr, Akil H, Bunney WE (2013) Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc Natl Acad Sci USA 110:9950–9955
Mandelik YT, Dayan (2000) Foraging activity of Acomys cahirinus under different illumination levels: comparing giving-up densities to direct behavioral observations. Isr J Zool 46:167–168
Martijena ID, Tapia M, Molina VA (1996) Altered behavioral and neurochemical response to stress in benzodiazepine-withdrawn rats. Brain Res 712:239–244
McClung CA (2007) Circadian genes, rhythms and the biology of mood disorders. Pharmacol Ther 114:222–232
Molina hernandez M, Téllez-Alcántara P (2000) Long photoperiod regimen may produce antidepressant actions in the male rat. Prog Neuropsychopharmacol Biol Psychiatry 24:105–116
Moscovici L, Kotler M (2009) A multistage chronobiologic intervention for the treatment of depression: a pilot study. J Affect Disord 116:201–207
Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34:13–25
Nowak JZ, Zawilska JB (1998) Melatonin and its physiological and therapeutic properties. Pharm World Sci 20:18–27
Papp M, Willner P, Muscat R (1991) An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berl) 104:255–259
Partonen T et al (2007) Three circadian clock genes Per2, Arntl, and Npas2 contribute to winter depression. Ann Med 39:229–238
Porsolt RD, Bertin A, Jalfre M (1978) “Behavioural despair” in rats and mice: strain differences and the effects of imipramine. Eur J Pharmacol 51:291–294
Prendergast BJ, Kay LM (2008) Affective and adrenocorticotrophic responses to photoperiod in Wistar rats. J Neuroendocrinol 20:261–267
Prendergast BJ, Nelson RJ (2005) Affective responses to changes in day length in Siberian hamsters. (Phodopus sungorus). Psychoneuroendocrinology 30:438–452
Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463:3–33
Pyter LM, Nelson RJ (2006) Enduring effects of photoperiod on affective behaviors in Siberian hamsters. (Phodopus sungorus). Behav Neurosci 120:125–134
Raoux N, Benoit O, Dantchev N, Denise P, Franc B, Allilaire JF, Widlöcher D (1994) Circadian pattern of motor activity in major depressed patients undergoing antidepressant therapy: relationship between actigraphic measures and clinical course. Psychiatry Res 52:85–98
Refinetti R (1996) Rhythms of body temperature and temperature selection are out of phase in a diurnal rodent, Octodon degus. Physiol Behav 60:959–961
Refinetti R (2004) Daily activity patterns of a nocturnal and a diurnal rodent in a seminatural environment. Physiol Behav 82:285–294
Roll U, Dayan T, Kronfeld-Schor N (2006) On the role of phylogeny in determining activity patterns of rodents. Evol Ecol 20:479–490
Rotics S, Dayan T, Levy O, Kronfeld-Schor N (2011) Light masking in the field: an experiment with nocturnal and diurnal spiny mice under semi-natural field conditions. Chronobiol Int 28:70–75
Roybal K, Theobold D, Graham A, DiNieri JA, Russo SJ, Krishnan V, Chakravarty S, Peevey J, Oehrlein N, Birnbaum S, Vitaterna MH, Orsulak P, Takahashi JS, Nestler EJ, Carlezon WA, McClung CA (2007) Mania-like behavior induced by disruption of CLOCK. Proc Natl Acad Sci USA 104:6406–6411
Sadock VA, Kaplan HI (2007) Kaplan and Sadock’s synopsis of psychiatry. Lippincott Williams, Wilkins
Scheer FAJL, Hilton MF, Mantzoros CS, Shea SA (2009) Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci USA 106:4453–4458
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 27:299–307
Sinitskaya N, Schuster-Klein C, Guardiola-Lemaitre B, Gourmelen S, Pévet P, Challet E (2008) Short day-length increases sucrose consumption and adiposity in rats fed a high-fat diet. Psychoneuroendocrinology 33:1269–1278
Smale L, Heideman PD, French JA (2005) Behavioral neuroendocrinology in nontraditional species of mammals: things the “knockout” mouse CAN’T tell us. Horm Behav 48:474–483
Smale L, Nunez AA, Schwartz MD (2008) Rhythms in a diurnal brain. Biol Rhythm Res 39:305–318
Sonntag A, Rothe B, Guldner J, Yassouridis A, Holsboer F, Steiger A (1996) Trimipramine and imipramine exert different effects on the sleep EEG and on nocturnal hormone secretion during treatment of major depression. Depression 4:1–13
Tallman JF (1999) Neuropsychopharmacology at the new millennium: new industry directions. Neuropsychopharmacology 20:99–105
Tan Z-L, Bao A-M, Tao M, Liu Y-J, Zhou J-N (2007) Circadian rhythm of salivary serotonin in patients with major depressive disorder. Neuro Endocrinol Lett 28:395–400
Tecott LH, Nestler EJ (2004) Neurobehavioral assessment in the information age. Nat Neurosci 7:462–466
Teicher MH, Glod CA, Magnus E, Harper D, Benson GE, Krueger K, McGreenery CE (1997) Circadian rest–activity disturbances in seasonal affective disorder. Arch Gen Psychiatry 54:124–130
Todder D, Caliskan S, Baune BT (2006) Night locomotor activity and quality of sleep in quetiapine-treated patients with depression. J Clin Psychopharmacol 26:638–642
Volkers AC, Tulen JHM, van den Broek WW, Bruijn JA, Passchier J, Pepplinkhuizen L (2003) Motor activity and autonomic cardiac functioning in major depressive disorder. J Affect Disord 76:23–30
Wallace-Boone TL, Newton AE, Wright RN, Lodge NJ, McElroy JF (2008) Behavioral and pharmacological validation of the gerbil forced-swim test: effects of neurokinin-1 receptor antagonists. Neuropsychopharmacology 33:1919–1928
Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504
Wehr TA, Wirz-Justice A, Goodwin FK, Duncan W, Gillin JC (1979) Phase advance of the circadian sleep–wake cycle as an antidepressant. Science 206:710–713
Wehr TA, Jacobsen FM, Sack DA, Arendt J, Tamarkin L et al (1986) Phototherapy of seasonal affective disorder. Time of day and suppression of melatonin are not critical for antidepressant effects. Arch Gen Psychiatry 43(9):870–875
Wirz-Justice A, Van den Hoofdakker RH (1999) Sleep deprivation in depression: what do we know, where do we go? Biol Psychiatry 46:445–453
Wirz-Justice A, Wehr TA, Goodwin FK, Kafka MS, Naber D, Marangos PJ, Campbell IC (1980) Antidepressant drugs slow circadian rhythms in behavior and brain neurotransmitter receptors (proceedings). Psychopharmacol Bull 16:45–47
Woods CA, Boraker DK (1975) Octodon degus. American Society of Mammalogists. Mammalian Species 67:1-5
Wu JC, Kelsoe JR, Schachat C, Bunney BG, DeModena A, Golshan S, Gillin JC, Potkin SG, Bunney WE (2009) Rapid and sustained antidepressant response with sleep deprivation and chronotherapy in bipolar disorder. Biol Psychiatry 66:298–301
Yamada N, Martin-Iverson MT, Daimon K, Tsujimoto T, Takahashi S (1995) Clinical and chronobiological effects of light therapy on nonseasonal affective disorders. Biol Psychiatry 37:866–873
Zawilska JB, Derbiszewska T, Nowak JZ (1997) Prolonged exposure of chicks to light or darkness differentially affects the quinpirole-evoked suppression of serotonin N-acetyltransferase activity in chick retina: an impact on dopamine D4-like receptor. J Pineal Res 22:59–64
Zubidat AE, Ben-Shlomo R, Haim A (2007) Thermoregulatory and endocrine responses to light pulses in short-day acclimated social voles. (Microtus socialis). Chronobiol Int 24:269–288
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ashkenazy-Frolinger, T., Einat, H. & Kronfeld-Schor, N. Diurnal rodents as an advantageous model for affective disorders: novel data from diurnal degu (Octodon degus). J Neural Transm 122 (Suppl 1), 35–45 (2015). https://doi.org/10.1007/s00702-013-1137-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-013-1137-3