Environmental Enrichment Rescues Oxidative Stress and Behavioral Impairments Induced by Maternal Care Deprivation: Sex- and Developmental-Dependent Differences.
Anxiety
Environmental enrichment
Major depressive disorder
Maternal deprivation
Memory
Oxidative stress
Journal
Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
08
04
2021
accepted:
29
09
2021
medline:
21
11
2023
pubmed:
20
10
2021
entrez:
19
10
2021
Statut:
ppublish
Résumé
Stress is related to major depressive disorder (MDD). This study investigated the action that early stress, represented by maternal deprivation (MD), has on the behavior and oxidative stress of Wistar female and male rats. Also, it was evaluated whether changes induced by MD could be reversed by environmental enrichment (EE). Male and female rats were divided into a non-MD and MD group. The MD group was subdivided into 3 groups: (1) assessed on the 31
Identifiants
pubmed: 34665408
doi: 10.1007/s12035-021-02588-3
pii: 10.1007/s12035-021-02588-3
doi:
Substances chimiques
Antioxidants
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6757-6773Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Malhi GS, Mann JJ (2018) Depression Lancet 392:2299–2312. https://doi.org/10.1016/S0140-6736(18)31948-2
doi: 10.1016/S0140-6736(18)31948-2
pubmed: 30396512
WHO (2020) Depression. https://www.who.int/news-room/fact-sheets/detail/depression . Accessed 15 Apr 2020
American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders: Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5). Arlington, VA: American Psychiatric Association
Sheehan DV, Nakagome K, Asami Y et al (2017) Restoring function in major depressive disorder: A systematic review. J Affect Disord 215:299–313
doi: 10.1016/j.jad.2017.02.029
pubmed: 28364701
Colman I, Ataullahjan A (2010) Life course perspectives on the epidemiology of depression. Can J Psychiatry 55:622–632. https://doi.org/10.1177/070674371005501002
doi: 10.1177/070674371005501002
pubmed: 20964941
Burt DB, Zembar MJ, Niederehe G (1995) Depression and Memory Impairment: A Meta-Analysis of the Association, Its Pattern, and Specificity. Psychol Bull 117:285–305. https://doi.org/10.1037/0033-2909.117.2.285
doi: 10.1037/0033-2909.117.2.285
pubmed: 7724692
Rock PL, Roiser JP, Riedel WJ, Blackwell AD (2014) Cognitive impairment in depression: A systematic review and meta-analysis. Psychol Med 44:2029–2040. https://doi.org/10.1017/S0033291713002535
doi: 10.1017/S0033291713002535
pubmed: 24168753
Jacobson NC, Newman MG (2017) Anxiety and depression as bidirectional risk factors for one another: A meta-analysis of longitudinal studies. Psychol Bull 143:1155–1200. https://doi.org/10.1037/bul0000111
doi: 10.1037/bul0000111
pubmed: 28805400
Kessler RC, Bromet EJ (2013) The epidemiology of depression across cultures. Annu Rev Public Health 34:119–138
doi: 10.1146/annurev-publhealth-031912-114409
pubmed: 23514317
pmcid: 4100461
Salk RH, Hyde JS, Abramson LY (2017) Gender differences in depression in representative national samples: Meta-analyses of diagnoses and symptoms. Psychol Bull 143:783–822. https://doi.org/10.1037/bul0000102
doi: 10.1037/bul0000102
pubmed: 28447828
pmcid: 5532074
Krishnan V, Nestler EJ (2008) The molecular neurobiology of depression. Nature 455:894–902. https://doi.org/10.1038/nature07455
doi: 10.1038/nature07455
pubmed: 18923511
pmcid: 2721780
Jeon SW, Kim YK (2017) Inflammation-induced depression: Its pathophysiology and therapeutic implications. J Neuroimmunol 313:92–98. https://doi.org/10.1016/j.jneuroim.2017.10.016
doi: 10.1016/j.jneuroim.2017.10.016
pubmed: 29153615
Levy MJF, Boulle F, Steinbusch HW et al (2018) Neurotrophic factors and neuroplasticity pathways in the pathophysiology and treatment of depression. Psychopharmacology 235:2195–2220. https://doi.org/10.1007/s00213-018-4950-4
doi: 10.1007/s00213-018-4950-4
pubmed: 29961124
pmcid: 6061771
Czarny P, Wigner P, Galecki P, Sliwinski T (2018) The interplay between inflammation, oxidative stress, DNA damage, DNA repair and mitochondrial dysfunction in depression. Prog Neuro-Psychopharmacology Biol Psychiatry 80:309–321. https://doi.org/10.1016/j.pnpbp.2017.06.036
doi: 10.1016/j.pnpbp.2017.06.036
Liu T, Zhong S, Liao X et al (2015) A meta-analysis of oxidative stress markers in depression. PLoS ONE 10:e0138904. https://doi.org/10.1371/journal.pone.0138904
doi: 10.1371/journal.pone.0138904
pubmed: 26445247
pmcid: 4596519
Black CN, Bot M, Scheffer PG et al (2015) Is depression associated with increased oxidative stress? A systematic review and meta-analysis. Psychoneuroendocrinology 51:164–175. https://doi.org/10.1016/j.psyneuen.2014.09.025
doi: 10.1016/j.psyneuen.2014.09.025
pubmed: 25462890
Salim S (2017) Oxidative stress and the central nervous system. J Pharmacol Exp Ther 360:201–205. https://doi.org/10.1124/jpet.116.237503
doi: 10.1124/jpet.116.237503
pubmed: 27754930
pmcid: 5193071
Shapero BG, Black SK, Liu RT et al (2014) Stressful Life Events and Depression Symptoms: The Effect of Childhood Emotional Abuse on Stress Reactivity. J Clin Psychol 70:209–223. https://doi.org/10.1002/jclp.22011
doi: 10.1002/jclp.22011
pubmed: 23800893
Łosiak W, Blaut A, Kłosowska J, Łosiak-Pilch J (2019) Stressful Life Events, Cognitive Biases, and Symptoms of Depression in Young Adults. Front Psychol 10:2165. https://doi.org/10.3389/fpsyg.2019.02165
doi: 10.3389/fpsyg.2019.02165
pubmed: 31681059
pmcid: 6798061
Hovens JGFM, Giltay EJ, van Hemert AM, Penninx BWJH (2017) Emotional scars: impact of childhood trauma on the development of depressive and anxiety disorders later in life. Tijdschr Psychiatr 59:286–296
pubmed: 28593622
Nikkheslat N, McLaughlin AP, Hastings C et al (2020) Childhood trauma, HPA axis activity and antidepressant response in patients with depression. Brain Behav Immun 87:229–237. https://doi.org/10.1016/j.bbi.2019.11.024
doi: 10.1016/j.bbi.2019.11.024
pubmed: 31794798
pmcid: 7327513
Nanni V, Uher R, Danese A (2012) Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: A meta-analysis. Am J Psychiatry 169:141–151. https://doi.org/10.1176/appi.ajp.2011.11020335
doi: 10.1176/appi.ajp.2011.11020335
pubmed: 22420036
Réus GZ, Stringari RB, Ribeiro KF et al (2011) Maternal deprivation induces depressive-like behaviour and alters neurotrophin levels in the rat brain. Neurochem Res 36:460–466. https://doi.org/10.1007/s11064-010-0364-3
doi: 10.1007/s11064-010-0364-3
pubmed: 21161589
El Khoury A, Gruber SHM, Mørk A, Mathé AA (2006) Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog Neuro-Psychopharmacology Biol Psychiatry 30:535–540. https://doi.org/10.1016/j.pnpbp.2005.11.011
doi: 10.1016/j.pnpbp.2005.11.011
Vetulani J (2013) Early maternal separation: A rodent model of depression and a prevailing human condition. Pharmacol Reports 65:1451–1461. https://doi.org/10.1016/S1734-1140(13)71505-6
doi: 10.1016/S1734-1140(13)71505-6
Lee JH, Kim HJ, Kim JG et al (2007) Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58:32–39. https://doi.org/10.1016/j.neures.2007.01.008
doi: 10.1016/j.neures.2007.01.008
pubmed: 17298851
Sale A, Berardi N, Maffei L (2014) Environment and brain plasticity: Towards an endogenous pharmacotherapy. Physiol Rev 94:189–234. https://doi.org/10.1152/physrev.00036.2012
doi: 10.1152/physrev.00036.2012
pubmed: 24382886
van Praag H, Kempermann G, Gage FH (2000) Neural consequences of enviromental enrichment. Nat Rev Neurosci 1:191–198. https://doi.org/10.1038/35044558
doi: 10.1038/35044558
pubmed: 11257907
Kempermann G (2019) Environmental enrichment, new neurons and the neurobiology of individuality. Nat Rev Neurosci 20:235–245
doi: 10.1038/s41583-019-0120-x
pubmed: 30723309
Simpson J, Kelly JP (2011) The impact of environmental enrichment in laboratory rats-Behavioural and neurochemical aspects. Behav Brain Res 222:246–264. https://doi.org/10.1016/j.bbr.2011.04.002
doi: 10.1016/j.bbr.2011.04.002
pubmed: 21504762
Shilpa BM, Bhagya V, Harish G et al (2017) Environmental enrichment ameliorates chronic immobilisation stress-induced spatial learning deficits and restores the expression of BDNF, VEGF, GFAP and glucocorticoid receptors. Prog Neuro-Psychopharmacology Biol Psychiatry 76:88–100. https://doi.org/10.1016/j.pnpbp.2017.02.025
doi: 10.1016/j.pnpbp.2017.02.025
Lehmann ML, Herkenham M (2011) Environmental enrichment confers stress resiliency to social defeat through an infralimbic cortex-dependent neuroanatomical pathway. J Neurosci 31:6159–6173. https://doi.org/10.1523/JNEUROSCI.0577-11.2011
doi: 10.1523/JNEUROSCI.0577-11.2011
pubmed: 21508240
pmcid: 3094574
Ignácio ZM, Réus GZ, Abelaira HM et al (2017) Quetiapine treatment reverses depressive-like behavior and reduces DNA methyltransferase activity induced by maternal deprivation. Behav Brain Res 320:225–232. https://doi.org/10.1016/j.bbr.2016.11.044
doi: 10.1016/j.bbr.2016.11.044
pubmed: 27913254
Kosten TA, Lee HJ, Kim JJ (2007) Neonatal handling alters learning in adult male and female rats in a task-specific manner. Brain Res 1154:144–153. https://doi.org/10.1016/j.brainres.2007.03.081
doi: 10.1016/j.brainres.2007.03.081
pubmed: 17475223
Mello PB, Benetti F, Cammarota M, Izquierdo I (2009) Physical exercise can reverse the deficit in fear memory induced by maternal deprivation. Neurobiol Learn Mem 92:364–369. https://doi.org/10.1016/j.nlm.2009.04.004
doi: 10.1016/j.nlm.2009.04.004
pubmed: 19398029
Réus GZ, Fernandes GC, de Moura AB et al (2017) Early life experience contributes to the developmental programming of depressive-like behaviour, neuroinflammation and oxidative stress. J Psychiatr Res 95:196–207. https://doi.org/10.1016/j.jpsychires.2017.08.020
doi: 10.1016/j.jpsychires.2017.08.020
pubmed: 28886447
Pereira LO, Arteni NS, Petersen RC et al (2007) Effects of daily environmental enrichment on memory deficits and brain injury following neonatal hypoxia-ischemia in the rat. Neurobiol Learn Mem 87:101–108. https://doi.org/10.1016/j.nlm.2006.07.003
doi: 10.1016/j.nlm.2006.07.003
pubmed: 16931063
Rojas JJ, Deniz BF, Miguel PM et al (2013) Effects of daily environmental enrichment on behavior and dendritic spine density in hippocampus following neonatal hypoxia-ischemia in the rat. Exp Neurol 241:25–33. https://doi.org/10.1016/j.expneurol.2012.11.026
doi: 10.1016/j.expneurol.2012.11.026
pubmed: 23219882
Barichello T, Fagundes GD, Generoso JS et al (2014) Environmental enrichment restores cognitive deficits induced by experimental childhood meningitis. Rev Bras Psiquiatr 36:322–329. https://doi.org/10.1590/1516-4446-2014-1443
doi: 10.1590/1516-4446-2014-1443
pubmed: 25076170
Borba LA, Broseghini LDR, Manosso LM et al (2021) Environmental enrichment improves lifelong persistent behavioral and epigenetic changes induced by early-life stress. J Psychiatr Res 138:107–116. https://doi.org/10.1016/j.jpsychires.2021.04.008
doi: 10.1016/j.jpsychires.2021.04.008
pubmed: 33848966
pmcid: 10494235
Ohlsson AL, Johansson BB (1995) Environment influences functional outcome of cerebral infarction in rats. Stroke 26:644–649. https://doi.org/10.1161/01.STR.26.4.644
doi: 10.1161/01.STR.26.4.644
pubmed: 7709412
Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709. https://doi.org/10.1038/nrn1970
doi: 10.1038/nrn1970
pubmed: 16924259
Brown RE, Corey SC, Moore AK (1999) Differences in measures of exploration and fear in MHC-congenic C57BL/6J and B6-H-2K mice. Behav Genet 29:263–271. https://doi.org/10.1023/A:1021694307672
doi: 10.1023/A:1021694307672
Vianna MRM, Alonso M, Viola H et al (2000) Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem 7:333–340. https://doi.org/10.1101/lm.34600
doi: 10.1101/lm.34600
pubmed: 11040265
pmcid: 311352
Gomes KM, Souza RP, Inácio CG et al (2011) Evaluation of light/dark cycle in anxiety- and depressive-like behaviors after regular treatment with methylphenidate hydrochloride in rats of different ages. Braz J Psychiatry 33:55–58. https://doi.org/10.1590/S1516-44462010005000018
doi: 10.1590/S1516-44462010005000018
pubmed: 20602012
Levine RL, Garland D, Oliver CN et al (1990) Determination of Carbonyl Content in Oxidatively Modified Proteins. Methods Enzymol 186:464–478. https://doi.org/10.1016/0076-6879(90)86141-H
doi: 10.1016/0076-6879(90)86141-H
pubmed: 1978225
Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407–421. https://doi.org/10.1016/0076-6879(90)86134-H
doi: 10.1016/0076-6879(90)86134-H
pubmed: 2233308
Green LC, Wagner DA, Glogowski J et al (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126:131–138. https://doi.org/10.1016/0003-2697(82)90118-X
doi: 10.1016/0003-2697(82)90118-X
pubmed: 7181105
Aebi H (1984) [13] Catalase in Vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
doi: 10.1016/S0076-6879(84)05016-3
pubmed: 6727660
Bannister JV, Calabrese L (1987) Assays for superoxide dismutase. Methods Biochem Anal 32:279–312
doi: 10.1002/9780470110539.ch5
pubmed: 3033431
Miragaia AS, de Oliveira Wertheimer GS, Consoli AC et al (2018) Maternal deprivation increases anxiety-and depressive-like behaviors in an age-dependent fashion and reduces neuropeptide y expression in the amygdala and hippocampus of male and female young adult rats. Front Behav Neurosci 12:159. https://doi.org/10.3389/fnbeh.2018.00159
doi: 10.3389/fnbeh.2018.00159
pubmed: 30131681
pmcid: 6090069
Wigger A, Neumann ID (1999) Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 66:293–302. https://doi.org/10.1016/S0031-9384(98)00300-X
doi: 10.1016/S0031-9384(98)00300-X
pubmed: 10336157
Llorente-Berzal A, Fuentes S, Gagliano H et al (2011) Sex-dependent effects of maternal deprivation and adolescent cannabinoid treatment on adult rat behaviour. Addict Biol 16:624–637. https://doi.org/10.1111/j.1369-1600.2011.00318.x
doi: 10.1111/j.1369-1600.2011.00318.x
pubmed: 21521421
Andersen SL (2015) Exposure to early adversity: Points of cross-species translation that can lead to improved understanding of depression. Dev Psychopathol 27:477–491. https://doi.org/10.1017/S0954579415000103
doi: 10.1017/S0954579415000103
pubmed: 25997766
pmcid: 5237807
Ahmad F, Salahuddin M, Alsamman K et al (2018) Neonatal maternal deprivation impairs localized de novo activity-induced protein translation at the synapse in the rat hippocampus. Biosci Rep 38(3):BSR20180118. https://doi.org/10.1042/BSR20180118
doi: 10.1042/BSR20180118
pubmed: 29700212
pmcid: 5997792
Janetsian-Fritz SS, Timme NM, McCane AM et al (2018) Maternal deprivation induces alterations in cognitive and cortical function in adulthood. Transl Psychiatry 8:71. https://doi.org/10.1038/s41398-018-0119-5
doi: 10.1038/s41398-018-0119-5
pubmed: 29581432
pmcid: 5913289
Seong HH, Park JM, Kim YJ (2018) Antidepressive Effects of Environmental Enrichment in Chronic Stress-Induced Depression in Rats. Biol Res Nurs 20:40–48. https://doi.org/10.1177/1099800417730400
doi: 10.1177/1099800417730400
pubmed: 28931312
Koe AS, Ashokan A, Mitra R (2016) Short environmental enrichment in adulthood reverses anxiety and basolateral amygdala hypertrophy induced by maternal separation. Transl Psychiatry 6:e729. https://doi.org/10.1038/tp.2015.217
doi: 10.1038/tp.2015.217
pubmed: 26836417
pmcid: 4872421
Francis DD, Diorio J, Plotsky PM, Meaney MJ (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840–7843. https://doi.org/10.1523/jneurosci.22-18-07840.2002
doi: 10.1523/jneurosci.22-18-07840.2002
pubmed: 12223535
pmcid: 6758090
Sampedro-Piquero P, Begega A (2016) Environmental Enrichment as a Positive Behavioral Intervention Across the Lifespan. Curr Neuropharmacol 15:459–470. https://doi.org/10.2174/1570159x14666160325115909
doi: 10.2174/1570159x14666160325115909
Lin EJD, Choi E, Liu X et al (2011) Environmental enrichment exerts sex-specific effects on emotionality in C57BL/6J mice. Behav Brain Res 216:349–357. https://doi.org/10.1016/j.bbr.2010.08.019
doi: 10.1016/j.bbr.2010.08.019
pubmed: 20732356
Chourbaji S, Hörtnagl H, Molteni R et al (2012) The impact of environmental enrichment on sex-specific neurochemical circuitries - Effects on brain-derived neurotrophic factor and the serotonergic system. Neuroscience 220:267–276. https://doi.org/10.1016/j.neuroscience.2012.06.016
doi: 10.1016/j.neuroscience.2012.06.016
pubmed: 22710068
Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
doi: 10.1146/annurev.arplant.55.031903.141701
pubmed: 15377225
Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13
doi: 10.1042/BJ20081386
pubmed: 19061483
Birben E, Sahiner UM, Sackesen C et al (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19
doi: 10.1097/WOX.0b013e3182439613
pubmed: 23268465
pmcid: 3488923
Guevara I, Iwanejko J, Dembińska-Kieć A et al (1998) Determination of nitrite/nitrate in human biological material by the simple Griess reaction. Clin Chim Acta 274:177–188. https://doi.org/10.1016/S0009-8981(98)00060-6
doi: 10.1016/S0009-8981(98)00060-6
pubmed: 9694586
Frijhoff J, Winyard PG, Zarkovic N et al (2015) Clinical Relevance of Biomarkers of Oxidative Stress. Antioxidants Redox Signal 23:1144–1170
doi: 10.1089/ars.2015.6317
Siwek M, Sowa-Kuaema M, Dudek D et al (2013) Oxidative stress markers in affective disorders. Pharmacol Reports 65:1558–1571. https://doi.org/10.1016/S1734-1140(13)71517-2
doi: 10.1016/S1734-1140(13)71517-2
Llorente R, Gallardo ML, Berzal AL et al (2009) Early maternal deprivation in rats induces gender-dependent effects on developing hippocampal and cerebellar cells. Int J Dev Neurosci 27:233–241. https://doi.org/10.1016/j.ijdevneu.2009.01.002
doi: 10.1016/j.ijdevneu.2009.01.002
pubmed: 19429388
Burke NN, Llorente R, Marco EM et al (2013) Maternal deprivation is associated with sex-dependent alterations in nociceptive behavior and neuroinflammatory mediators in the rat following peripheral nerve injury. J Pain 14:1173–1184. https://doi.org/10.1016/j.jpain.2013.05.003
doi: 10.1016/j.jpain.2013.05.003
pubmed: 23850096
Réus GZ, Carlessi AS, Titus SE et al (2015) A single dose of S-ketamine induces long-term antidepressant effects and decreases oxidative stress in adulthood rats following maternal deprivation. Dev Neurobiol 75:1268–1281. https://doi.org/10.1002/dneu.22283
doi: 10.1002/dneu.22283
pubmed: 25728399
Maciel AL, Abelaira HM, de Moura AB et al (2018) Acute treatment with ketamine and chronic treatment with minocycline exert antidepressant-like effects and antioxidant properties in rats subjected different stressful events. Brain Res Bull 137:204–216. https://doi.org/10.1016/j.brainresbull.2017.12.005
doi: 10.1016/j.brainresbull.2017.12.005
pubmed: 29253605
Marković B, Radonjić NV, Jevtić G et al (2017) Long-term effects of maternal deprivation on redox regulation in rat brain: Involvement of NADPH oxidase. Oxid Med Cell Longev 2017:7390516. https://doi.org/10.1155/2017/7390516
doi: 10.1155/2017/7390516
pubmed: 28408971
pmcid: 5376945
Menezes J, Neves BH, Souza M, Mello-Carpes PB (2017) Green tea protects against memory deficits related to maternal deprivation. Physiol Behav 182:121–127. https://doi.org/10.1016/j.physbeh.2017.10.010
doi: 10.1016/j.physbeh.2017.10.010
pubmed: 29031548
Neves BH, Menezes J, Souza MA, Mello-Carpes PB (2015) Physical exercise prevents short and long-term deficits on aversive and recognition memory and attenuates brain oxidative damage induced by maternal deprivation. Physiol Behav 152:99–105. https://doi.org/10.1016/j.physbeh.2015.09.019
doi: 10.1016/j.physbeh.2015.09.019
pubmed: 26403760
Lucca G, Comim CM, Valvassori SS et al (2009) Increased oxidative stress in submitochondrial particles into the brain of rats submitted to the chronic mild stress paradigm. J Psychiatr Res 43:864–869. https://doi.org/10.1016/j.jpsychires.2008.11.002
doi: 10.1016/j.jpsychires.2008.11.002
pubmed: 19100996
Kaufmann FN, Gazal M, Mondin TC et al (2015) Cognitive psychotherapy treatment decreases peripheral oxidative stress parameters associated with major depression disorder. Biol Psychol 110:175–181. https://doi.org/10.1016/j.biopsycho.2015.08.001
doi: 10.1016/j.biopsycho.2015.08.001
pubmed: 26255227
Mármol F, Rodríguez CA, Sánchez J, Chamizo VD (2015) Anti-oxidative effects produced by environmental enrichment in the hippocampus and cerebral cortex of male and female rats. Brain Res 1613:120–129. https://doi.org/10.1016/j.brainres.2015.04.007
doi: 10.1016/j.brainres.2015.04.007
pubmed: 25881892
Montes S, Yee-Rios Y, Páez-Martínez N (2019) Environmental enrichment restores oxidative balance in animals chronically exposed to toluene: Comparison with melatonin. Brain Res Bull 144:58–67. https://doi.org/10.1016/j.brainresbull.2018.11.007
doi: 10.1016/j.brainresbull.2018.11.007
pubmed: 30453037
Martín-Hernández D, Caso JR, Javier Meana J et al (2018) Intracellular inflammatory and antioxidant pathways in postmortem frontal cortex of subjects with major depression: Effect of antidepressants. J Neuroinflammation 15:1–12. https://doi.org/10.1186/s12974-018-1294-2
doi: 10.1186/s12974-018-1294-2
Almeida Moreira Leal LK, Lima LA, Alexandre de Aquino PE et al (2020) Vitamin D (VD3) antioxidative and anti-inflammatory activities: Peripheral and central effects. Eur J Pharmacol 879:173099. https://doi.org/10.1016/j.ejphar.2020.173099
doi: 10.1016/j.ejphar.2020.173099
pubmed: 32360837