Accepted Manuscripts
Back to the articles list |
Back to browse issues page
Abstract: (469 Views)
Introduction: Light-dark cycles regulate the body’s physiological activity; hence, marked changes in these cycles could lead to conditions with impaired brain functions and disrupted moods (e.g., stress). Therefore, this study compared the impact of stress due to various photoperiodic durations on anxiety-like behavior, learning, memory, locomotor activity, and memory consolidation in rats.
Methods: Thirty-five male rats were divided into five groups with different light-dark cycles: L20/D4, L16/D8, L12/D12 (control), L8/D16, and L4/D20 groups. After14 days, the elevated plus-maze (EPM) and passive avoidance (PA) tests were performed to assess the anxiety-like behaviors and brain functions.
Results: The percentage of spent time, number of entries to the open arm of the EPM test, and the entrance latency to the dark room of the PA test decreased significantly in the L20/D4 and L4/D20 groups; however, the reduction of latency to enter the dark room was particularly significant in the L20/D4 group. In addition, there were significant differences between the initial latency and latency after one day (as learning) in all experimental groups. The total dark stay (DS) time increased significantly in different photoperiods.
Conclusion: An abnormal light-dark length could disrupt certain brain functions, such as learning, memory, locomotor activity, memory consolidation and anxiety-like behavioral responses at different levels in a time-independent manner. The light-dark length (both minimum and especially the maximum day length) led to increased learning impairment and memory deficits, as well as worsened anxiety-like behaviors. The memory consolidation was also disrupted with various photoperiods.
Types of Manuscript: Experimental research article |
Subject:
Neurophysiology/Pharmacology
References
1. Arziqni N, Hadi S. The Effect of Long Photoperiod on The Visuospatial Working Memory in Wistar Rats (Rattus norvegicus)[Pengaruh Pencahayaan Panjang Terhadap Memori Kerja Visuospasial Tikus Wistar (Rattus norvegicus)]. Jurnal Biologi Indonesia 2021; 17: 127-134. [DOI:10.47349/jbi/17022021/127]
2. Atger F, Mauvoisin D, Weger B, Gobet C, Gachon F. Regulation of mammalian physiology by interconnected circadian and feeding rhythms. Frontiers in endocrinology 2017; 8: 42. [DOI:10.3389/fendo.2017.00042]
3. Barnes A K, Smith S B, Datta S J P O. Beyond emotional and spatial processes: cognitive dysfunction in a depressive phenotype produced by long photoperiod exposure. 2017; 12: e0170032. [DOI:10.1371/journal.pone.0170032]
4. Beauvalet J C, Pilz L K, Hidalgo M P L, Elisabetsky E. Is chronodisruption a vulnerability factor to stress? Behavioural Brain Research 2019; 359: 333-341. [DOI:10.1016/j.bbr.2018.11.016]
5. Bellivier F, Geoffroy P A, Etain B, Scott J. Sleep- and circadian rhythm-associated pathways as therapeutic targets in bipolar disorder. Expert Opin Ther Targets 2015; 19: 747-63. [DOI:10.1517/14728222.2015.1018822]
6. Boerngen-Lacerda R, Souza-Formigoni M L O. Does the increase in locomotion induced by ethanol indicate its stimulant or anxiolytic properties? Pharmacology Biochemistry and Behavior 2000; 67: 225-232. [DOI:10.1016/S0091-3057(00)00360-9]
7. Boonstra R, McColl C J. Contrasting stress response of male arctic ground squirrels and red squirrels. Journal of Experimental Zoology 2000; 286: 390-404. [https://doi.org/10.1002/(SICI)1097-010X(20000301)286:4<390::AID-JEZ7>3.0.CO;2-O]
8. Breuner C, Wingfield J. Rapid behavioral response to corticosterone varies with photoperiod and dose. Hormones and behavior 2000; 37: 23-30. [DOI:10.1006/hbeh.1999.1554]
9. Dastgerdi H H, Radahmadi M, Reisi P. Comparative study of the protective effects of crocin and exercise on long-term potentiation of CA1 in rats under chronic unpredictable stress. Life sciences 2020; 256: 118018. [DOI:10.1016/j.lfs.2020.118018]
10. Do Nascimento E B, Dierschnabel A L, de Macêdo Medeiros A, Suchecki D, Silva R H, Ribeiro A M. Memory impairment induced by different types of prolonged stress is dependent on the phase of the estrous cycle in female rats. Hormones and Behavior 2019; 115: 104563. [DOI:10.1016/j.yhbeh.2019.104563]
11. Emmer K M, Russart K L, Walker II W H, Nelson R J, DeVries A C. Effects of light at night on laboratory animals and research outcomes. Behavioral neuroscience 2018; 132: 302. [DOI:10.1037/bne0000252]
12. Farhud D, Aryan Z. Circadian Rhythm, Lifestyle and Health: A Narrative Review. Iran journal of public health 2018; 47: 1068-1076.
13. Fonken L K, Finy M S, Walton J C, Weil Z M, Workman J L, Ross J, et al. Influence of light at night on murine anxiety-and depressive-like responses. Behavioural brain research 2009; 205: 349-354. [DOI:10.1016/j.bbr.2009.07.001]
14. Gu B, Tan Q, Zhao S. The association between occupational stress and psychosomatic wellbeing among Chinese nurses: a cross-sectional survey. Medicine 2019; 98. [DOI:10.1097/MD.0000000000015836]
15. Hadad-Ophir O, Albrecht A, Stork O, Richter-Levin G. Amygdala activation and GABAergic gene expression in hippocampal sub-regions at the interplay of stress and spatial learning. Frontiers in behavioral neuroscience 2014; 8: 3. [DOI:10.3389/fnbeh.2014.00003]
16. Hafez M H, Gad S B. Zinc Oxide Nanoparticles Effect on Oxidative Status, Brain Activity, Anxiety-Like Behavior and Memory in Adult and Aged Male Rats. Pakistan Veterinary Journal 2018; 38. [DOI:10.29261/pakvetj/2018.069]
17. Hosseini-Sharifabad A, Mofid M R, Moradmand M, Keimasi M. The Effect of Omega-lycotoxin on the Cognitive Impairment Induced by Kainic Acid in Rats. Iranian Journal of Toxicology 2021; 15: 49-56. [DOI:10.32598/IJT.15.1.740.1]
18. Hou Y, Wang Y, Song S, Zuo Y, Zhang H, Bai C, et al. Long-term variable photoperiod exposure impairs the mPFC and induces anxiety and depression-like behavior in male wistar rats. Experimental Neurology 2022; 347: 113908. [DOI:10.1016/j.expneurol.2021.113908]
19. Kalantarzadeh E, Radahmadi M, Reisi P. Effects of different dark chocolate diets on memory functions and brain corticosterone levels in rats under chronic stress. Physiology and Pharmacology 2020; 24. [DOI:10.32598/ppj.24.3.40]
20. Kaliyaperumal D, Elango Y, Alagesan M, Santhanakrishanan I. effects of Sleep Deprivation on the Cognitive Performance of Nurses Working in Shift. Journal of Clinical and Diagnostic Research 2017; 11. [DOI:10.7860/JCDR/2017/26029.10324]
21. Klyubin I, Ondrejcak T, Hu N-W, Rowan M J. Glucocorticoids, synaptic plasticity and Alzheimer's disease. Current Opinion in Endocrine and Metabolic Research 2022: 100365. [DOI:10.1016/j.coemr.2022.100365]
22. Knight P, Chellian R, Wilson R, Behnood-Rod A, Panunzio S, Bruijnzeel A W. Sex differences in the elevated plus-maze test and large open field test in adult Wistar rats. Pharmacology Biochemistry and Behavior 2021; 204: 173168. [DOI:10.1016/j.pbb.2021.173168]
23. Landgraf D, McCarthy M J, Welsh D K. Circadian Clock and Stress Interactions in the Molecular Biology of Psychiatric Disorders. Current Psychiatry Reports 2014; 16: 483. [DOI:10.1007/s11920-014-0483-7]
24. Leach G, Adidharm W, Yan L. Depression-Like Responses Induced by Daytime Light Deficiency in the Diurnal Grass Rat (Arvicanthis niloticus). PLoS ONE 2013; 8. [DOI:10.1371/journal.pone.0057115]
25. Lee B, Sur B, Oh S. Neuroprotective effect of Korean red ginseng against single prolonged stress-induced memory impairments and inflammation in the rat brain associated with BDNF expression. Journal of Ginseng Research 2022; 46: 435-443. [DOI:10.1016/j.jgr.2021.08.002]
26. Lee Y, Wisor J P. Multi-Modal Regulation of Circadian Physiology by Interactive Features of Biological Clocks. Biology 2021; 11: 21. [DOI:10.3390/biology11010021]
27. Logan R W, McClung C A. Rhythms of life: circadian disruption and brain disorders across the lifespan. Nature Reviews Neuroscience 2019; 20: 49-65. [DOI:10.1038/s41583-018-0088-y]
28. López-Olmeda J F, Zhao H, Reischl M, Pylatiuk C, Lucon-Xiccato T, Loosli F, et al. Long photoperiod impairs learning in male but not female medaka. Iscience 2021; 24: 102784. [DOI:10.1016/j.isci.2021.102784]
29. Lu Q, Zhang Y, Zhao C, Zhang H, Pu Y, Yin L. Copper induces oxidative stress and apoptosis of hippocampal neuron via pCREB/BDNF/and Nrf2/HO‐1/NQO1 pathway. Journal of Applied Toxicology 2022; 42: 694-705. [DOI:10.1002/jat.4252]
30. Lunsford-Avery J R, Gonçalves B d S B, Brietzke E, Bressan R A, Gadelha A, Auerbach R P, et al. Adolescents at clinical-high risk for psychosis: Circadian rhythm disturbances predict worsened prognosis at 1-year follow-up. Schizophrenia Research 2017; 189: 37-42. [DOI:10.1016/j.schres.2017.01.051]
31. Ma L, Li Y. The effect of depression on sleep quality and the circadian rhythm of ambulatory blood pressure in older patients with hypertension. Journal of Clinical Neuroscience 2017; 39: 49-52. [DOI:10.1016/j.jocn.2017.02.039]
32. McEwen B S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005; 54: 20-23. [DOI:10.1016/j.metabol.2005.01.008]
33. Ouanes S, Popp J. High cortisol and the risk of dementia and Alzheimer's disease: a review of the literature. Frontiers in aging neuroscience 2019; 11: 43. [DOI:10.3389/fnagi.2019.00043]
34. Patki G, Solanki N, Atrooz F, Allam F, Salim S. Depression, anxiety-like behavior and memory impairment are associated with increased oxidative stress and inflammation in a rat model of social stress. Brain research 2013; 1539: 73-86. [DOI:10.1016/j.brainres.2013.09.033]
35. Phan T X, Malkani R G. Sleep and circadian rhythm disruption and stress intersect in Alzheimer's disease. Neurobiology of Stress 2019; 10: 100133. [DOI:10.1016/j.ynstr.2018.10.001]
36. Pyter L M, Reader B F, Nelson R J. Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus). Journal of Neuroscience 2005a; 25: 4521-4526. [DOI:10.1523/JNEUROSCI.0795-05.2005]
37. Pyter L M, Reader B F, Nelson R J. Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus). J Neurosci 2005b; 25: 4521-6. [DOI:10.1523/JNEUROSCI.0795-05.2005]
38. Radahmadi M, Alaei H, Sharifi M R, Hosseini N. Stress biomarker responses to different protocols of forced exercise in chronically stressed rats. Journal of bodywork movement therapies 2017; 21: 63-68.
39. Ranjbar H, Radahmadi M, Alaei H, Reisi P, Karimi S. The effect of basolateral amygdala nucleus lesion on memory under acute, mid and chronic stress in male rats. Turkish journal of medical sciences 2016; 46: 1915-1925. [DOI:10.3906/sag-1507-7]
40. Ruan W, Yuan X, Eltzschig H K. Circadian rhythm as a therapeutic target. Nature Reviews Drug Discovery 2021; 20: 287-307. [DOI:10.1038/s41573-020-00109-w]
41. Russell G, Lightman S. The human stress response. Nature reviews endocrinology 2019; 15: 525-534. [DOI:10.1038/s41574-019-0228-0]
42. Sestakova N, Puzserova A, Kluknavsky M, Bernatova I. Determination of motor activity and anxiety-related behaviour in rodents: methodological aspects and role of nitric oxide. Interdisciplinary toxicology 2013; 6: 126-135. [DOI:10.2478/intox-2013-0020]
43. Silva A L, Fry W H, Sweeney C, Trainor B C. Effects of photoperiod and experience on aggressive behavior in female California mice. Behavioural brain research 2010; 208: 528-534. [DOI:10.1016/j.bbr.2009.12.038]
44. Soler J E, Stumpfig M, Tang Y-P, Robison A J, Núñez A A, Yan L. 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]
45. Stothard E R, McHill A W, Depner C M, Birks B R, Moehlman T M, Ritchie H K, et al. Circadian Entrainment to the Natural Light-Dark Cycle across Seasons and the Weekend. Current Biology 2017; 27: 508-513. [DOI:10.1016/j.cub.2016.12.041]
46. Subhadeep D, Srikumar B, Rao S, Kutty B M. Exposure to Short Photoperiod Regime Restores Spatial Cognition in Ventral Subicular Lesioned Rats: Potential Role of Hippocampal Plasticity, Glucocorticoid Receptors, and Neurogenesis. Molecular Neurobiology 2021; 58: 4437-4459. [DOI:10.1007/s12035-021-02409-7]
47. Subhadeep D, Srikumar B N, Shankaranarayana Rao B S, Kutty B M. Short photoperiod restores ventral subicular lesion‐induced deficits in affective and socio‐cognitive behavior in male Wistar rats. Journal of Neuroscience Research 2020; 98: 1114-1136. [DOI:10.1002/jnr.24601]
48. Tahara Y, Aoyama S, Shibata S. The mammalian circadian clock and its entrainment by stress and exercise. The Journal of Physiological Sciences 2016; 67. [DOI:10.1007/s12576-016-0450-7]
49. Takahashi L. Olfactory systems and neural circuits that modulate predator odor fear. Frontiers in Behavioral Neuroscience 2014; 8. [DOI:10.3389/fnbeh.2014.00072]
50. Tamminga C A, Southcott S, Sacco C, Wagner A D, Ghose S. Glutamate dysfunction in hippocampus: relevance of dentate gyrus and CA3 signaling. Schizophrenia bulletin 2012; 38: 927-935. [DOI:10.1093/schbul/sbs062]
51. Thangwong P, Jearjaroen P, Govitrapong P, Tocharus C, Tocharus J. Melatonin improves cognitive function by suppressing endoplasmic reticulum stress and promoting synaptic plasticity during chronic cerebral hypoperfusion in rats. Biochemical Pharmacology 2022; 198: 114980. [DOI:10.1016/j.bcp.2022.114980]
52. Valdés‐Tovar M, Estrada‐Reyes R, Solís‐Chagoyán H, Argueta J, Dorantes‐Barrón A M, Quero‐Chávez D, et al. Circadian modulation of neuroplasticity by melatonin: a target in the treatment of depression. British journal of pharmacology 2018; 175: 3200-3208. [DOI:10.1111/bph.14197]
53. Walton J C, Chen Z, Weil Z M, Pyter L M, Travers J B, Nelson R J. Photoperiod-mediated impairment of long-term potention and learning and memory in male white-footed mice. Neuroscience 2011a; 175: 127-32. [DOI:10.1016/j.neuroscience.2010.12.004]
54. Walton J C, Chen Z, Weil Z M, Pyter L M, Travers J B, Nelson R J J N. Photoperiod-mediated impairment of long-term potention and learning and memory in male white-footed mice. 2011b; 175: 127-132. [DOI:10.1016/j.neuroscience.2010.12.004]
55. Weiss I C, Di Iorio L, Feldon J, Domeney A M. Strain differences in the isolation-induced effects on prepulse inhibition of the acoustic startle response and on locomotor activity. Behavioral neuroscience 2000; 114: 364. [DOI:10.1037/0735-7044.114.2.364]
56. Workman J L, Manny N, Walton J C, Nelson R J. Short day lengths alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters. Horm Behav 2011; 60: 520-8. [DOI:10.1016/j.yhbeh.2011.07.021]
57. Yang J, Hou C, Ma N, Liu J, Zhang Y, Zhou J, et al. Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiology of learning and memory 2007; 87: 257-263. [DOI:10.1016/j.nlm.2006.09.001]
58. Youngstedt S D, Elliott J A, Kripke D F. Human circadian phase-response curves for exercise. The Journal of Physiology 2019; 597: 2253-2268. [DOI:10.1113/JP276943]
59. Zelinski E L, Hong N S, McDonald R J J A c. Persistent impairments in hippocampal function following a brief series of photoperiod shifts in rats. 2014; 17: 127-141. [DOI:10.1007/s10071-013-0645-8]
60. Zhang I. The Impact of Emotional Arousal on Amygdala Activity, Memory Consolidation, and Long-Term Potentiation in the Hippocampus. Journal of Student Research 2022; 11. [DOI:10.47611/jsr.v11i2.1614]
61. Zoeram S B, Salmani M E, Lashkarbolouki T, Goudarzi I. Hippocampal orexin receptor blocking prevented the stress induced social learning and memory deficits. Neurobiology of Learning and Memory 2019; 157: 12-23. [DOI:10.1016/j.nlm.2018.11.009]
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
