{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T00:35:55Z","timestamp":1777336555418,"version":"3.51.4"},"reference-count":81,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,12]],"date-time":"2023-10-12T00:00:00Z","timestamp":1697068800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Melatonin (MLT) reportedly has beneficial effects in neurological disorders involving brain excitability (e.g., Epilepsy and Migraine) and behavioral patterns (e.g., Anxiety and Depression). This study was performed to investigate, in the developing rat brain, the effect of early-in-life administration of two different doses of exogenous MLT on behavioral (anxiety and memory) and electrophysiological (CSD analysis) aspects of brain function. Additionally, brain levels of malondialdehyde (MDA) and superoxide dismutase (SOD), both cellular indicators of redox balance status, were evaluated. We hypothesize that MLT differentially affects the behavioral and CSD parameters as a function of the MLT dose.<\/jats:p><\/jats:sec><jats:sec><jats:title>Materials and methods<\/jats:title><jats:p>Male Wistar rats received, from the 7th to the 27th postnatal day (PND), on alternate days, vehicle solution, or 10 mg\/kg\/or 40 mg\/kg MLT (MLT-10 and MLT-40 groups), or no treatment (intact group). To perform behavioral and cognition analysis, from PND30 to PND32, they were tested in the open field apparatus, first for anxiety (PND30) and then for object recognition memory tasks: spatial position recognition (PND31) and shape recognition (PND32). On PND34, they were tested in the elevated plus maze. From PND36 to 42, the excitability-related phenomenon known as cortical spreading depression (CSD) was recorded, and its features were analyzed.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Treatment with MLT did not change the animals\u2019 body weight or blood glucose levels. The MLT-10 treatment, but not the MLT-40 treatment, was associated with behaviors that suggest less anxiety and improved memory. MLT-10 and MLT-40 treatments, respectively, decelerated and accelerated CSD propagation (speed of 2.86 \u00b1 0.14 mm\/min and 3.96 \u00b1 0.16 mm\/min), compared with the control groups (3.3 \u00b1 0.10 mm\/min and 3.25 \u00b1 0.11 mm\/min, for the intact and vehicle groups, respectively;<jats:italic>p<\/jats:italic>&amp;lt; 0.01). Cerebral cortex levels of malondialdehyde and superoxide dismutase were, respectively, lower and higher in the MLT-10 group but not in the MLT40 group.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Our findings suggest that MLT intraperitoneal administration during brain development may differentially act as an antioxidant agent when administered at a low dose but not at a high dose, according to behavioral, electrophysiological, and biochemical parameters.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnins.2023.1269609","type":"journal-article","created":{"date-parts":[[2023,10,12]],"date-time":"2023-10-12T17:56:11Z","timestamp":1697133371000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Effect of neonatal melatonin administration on behavioral and brain electrophysiological and redox imbalance in rats"],"prefix":"10.3389","volume":"17","author":[{"given":"Amanda de Oliveira","family":"Ara\u00fajo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria Lu\u00edsa","family":"Figueira-de-Oliveira","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Arthur Gabriel Alves Furtado de Carvalho","family":"Noya","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vitor Palmares","family":"Oliveira e Silva","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jennyfer Martins de","family":"Carvalho","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Leucio Duarte","family":"Vieira Filho","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rubem Carlos Ara\u00fajo","family":"Guedes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,12]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1080\/1028415X.2019.1575574","article-title":"Topical cortical application of ovarian hormones and modulation of brain electrical activity: analysis of spreading depression in well-nourished and malnourished female rats","volume":"23","author":"Accioly","year":"2020","journal-title":"Nutr. Neurosci."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"118826","DOI":"10.1016\/j.lfs.2020.118826","article-title":"Revisiting the role of neurotransmitters in epilepsy: an updated review","volume":"265","author":"Akyuz","year":"2021","journal-title":"Life Sci."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1024","DOI":"10.1080\/01480545.2022.2119994","article-title":"Pinealectomy and melatonin administration in rats: their effects on pulmonary edema induced by \u03b1-naphthylthiourea","volume":"46","author":"Al Gburi","year":"2023","journal-title":"Drug Chem. Toxicol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"104827","DOI":"10.1016\/j.neubiorev.2022.104827","article-title":"Effects of personality on assessments of anxiety and cognition","volume":"141","author":"Am\u00e9ndola","year":"2022","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1007\/s40261-015-0368-5","article-title":"The safety of melatonin in humans","volume":"36","author":"Andersen","year":"2016","journal-title":"Clin. Drug Investig."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1177\/0748730405277492","article-title":"Melatonin: characteristics, concerns, and prospects","volume":"20","author":"Arendt","year":"2005","journal-title":"J. Biol. Rhythms"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1253","DOI":"10.1007\/s10571-020-01000-3","article-title":"Remote and persistent alterations in glutamate receptor subunit composition induced by spreading depolarizations in rat brain","volume":"42","author":"Barhorst","year":"2022","journal-title":"Cell. Mol. Neurobiol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"712","DOI":"10.1016\/j.neuroscience.2007.09.030","article-title":"Melatonin prevents learning disorders in brain-lesioned newborn mice","volume":"150","author":"Bouslama","year":"2007","journal-title":"Neuroscience"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"943","DOI":"10.3390\/biom13060943","article-title":"Melatonin: facts, Extrapolations and Clinical Trials","volume":"13","author":"Boutin","year":"2023","journal-title":"Biomolecules"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1285","DOI":"10.1111\/j.1471-4159.2010.06696.x","article-title":"Neonatal exposure to estradiol in rats influences neuroactive steroid concentrations, GABAA receptor expression, and behavioral sensitivity to anxiolytic drugs","volume":"113","author":"Calza","year":"2010","journal-title":"J. Neurochem."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"34","DOI":"10.3389\/fnsyn.2019.00034","article-title":"An assessment of Melatonin\u2019s therapeutic value in the hypoxic-ischemic encephalopathy of the newborn","volume":"11","author":"Cardinali","year":"2019","journal-title":"Front Synap Neurosci."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/bs.vh.2020.12.004","article-title":"Melatonin and healthy aging","volume":"115","author":"Cardinali","year":"2020","journal-title":"Vitam. Horm."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.earlhumdev.2016.09.001","article-title":"Melatonin and the newborn brain","volume":"102","author":"Colella","year":"2016","journal-title":"Early Hum. Dev."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"4595","DOI":"10.1016\/j.clnu.2021.06.007","article-title":"Effects of melatonin supplementation on diabetes: a systematic review and meta-analysis of randomized clinical trials","volume":"40","author":"Delpino","year":"2021","journal-title":"Clin. Nutr."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1177\/00912700022009422","article-title":"The absolute bioavailability of oral melatonin","volume":"40","author":"DeMuro","year":"2000","journal-title":"J. Clin. Pharmacol."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1016\/j.nlm.2005.07.002","article-title":"Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice","volume":"84","author":"Dere","year":"2005","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"615","DOI":"10.3390\/nu13020615","article-title":"Vitamin C-sources, physiological role, kinetics, deficiency, use, toxicity, and determination","volume":"13","author":"Dosed\u011bl","year":"2021","journal-title":"Nutrients"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1211","DOI":"10.1096\/fasebj.12.12.1211","article-title":"Selective MT2 melatonin receptor antagonists block melatonin-mediated phase advances of circadian rhythms","volume":"12","author":"Dubocovich","year":"1998","journal-title":"FASEB J."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/s0304-3940(99)00376-6","article-title":"Biphasic effects of melatonin on the propagation of excitation waves in the chicken retina","volume":"268","author":"Ebert","year":"1999","journal-title":"Neurosci. Lett."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1080\/1028415X.1998.11747230","article-title":"Dietary antioxidant deficiency facilitates cortical spreading depression induced by photo-activated riboflavin","volume":"1","author":"El-Bach\u00e1","year":"1998","journal-title":"Nutr. Neurosci."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1002\/jnr.10605","article-title":"Melatonin regulates neuronal plasticity in the hippocampus","volume":"72","author":"El-Sherif","year":"2003","journal-title":"J. Neurosci. Res."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/0166-4328(88)90157-x","article-title":"A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data","volume":"31","author":"Ennaceur","year":"1988","journal-title":"Behav. Brain Res."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/jas\/skaa372","article-title":"Supplementing merino ewes with melatonin during the last half of pregnancy improves tolerance of prolonged parturition and survival of second-born twin lambs","volume":"98","author":"Flinn","year":"2020","journal-title":"J. Anim. Sci."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1002\/hup.2416","article-title":"Administration of exogenous melatonin increases spreading activation in lexical memory networks","volume":"29","author":"Foster","year":"2014","journal-title":"Hum. Psychopharmacol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"2437","DOI":"10.1007\/s00726-015-2036-8","article-title":"Neonatal taurine and alanine modulate anxiety-like behavior and decelerate cortical spreading depression in rats previously suckled under different litter sizes","volume":"47","author":"Francisco","year":"2015","journal-title":"Amino Acids"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1823","DOI":"10.1002\/ijc.25204","article-title":"Involvement of ca(2+) and ROS in alpha-tocopheryl succinate-induced mitochondrial permeabilization","volume":"127","author":"Gogvadze","year":"2010","journal-title":"Int. J. Cancer"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1080\/1028415X.2019.1632570","article-title":"Neonatal pyridoxine administration long lastingly accelerates cortical spreading depression in male rats, without affecting anxiety-like behavior","volume":"24","author":"Gondim-Silva","year":"2021","journal-title":"Nutr. Neurosci."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1340","DOI":"10.3390\/brainsci12101340","article-title":"Blast exposure dysregulates nighttime melatonin synthesis and signaling in the pineal gland: a potential mechanism of blast-induced sleep disruptions","volume":"12","author":"Govindarajulu","year":"2022","journal-title":"Brain Sci."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"2233S","DOI":"10.1093\/jn\/125.suppl_8.2233S","article-title":"A review of studies of the effect of severe malnutrition on mental development","volume":"125","author":"Grantham-Mcgregor","year":"1995","journal-title":"J. Nutr."},{"key":"ref30","doi-asserted-by":"crossref","first-page":"2343","DOI":"10.1007\/978-0-387-92271-3_148","article-title":"Cortical spreading depression: a model for studying brain consequences of malnutrition","volume-title":"Handbook of Behavior, Food and Nutrition","author":"Guedes","year":"2011"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"136","DOI":"10.3389\/fnagi.2019.00136","article-title":"Brain aging and electrophysiological signaling: revisiting the spreading depression model","volume":"11","author":"Guedes","year":"2019","journal-title":"Front. Aging Neurosci."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1179\/1476830511Y.0000000024","article-title":"The use of cortical spreading depression for studying the brain actions of antioxidants","volume":"15","author":"Guedes","year":"2012","journal-title":"Nutr. Neurosci."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.brainres.2017.07.011","article-title":"Evidence of an inverse correlation between serotonergic activity and spreading depression propagation in the rat cortex","volume":"1672","author":"Guedes","year":"2017","journal-title":"Brain Res."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.neurol.2019.07.025","article-title":"Melatonin: a review of its potential functions and effects on neurological diseases","volume":"176","author":"Gunata","year":"2020","journal-title":"Rev. Neurol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"e12703","DOI":"10.1111\/jpi.12703","article-title":"The melatonin metabolite N1-acetyl-5-methoxykynuramine facilitates long-term object memory in young and aging mice","volume":"70","author":"Iwashita","year":"2021","journal-title":"J. Pineal Res."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1097\/nen.0b013e31820d8f92","article-title":"Hypoxia-induced cellular and vascular changes in the nucleus tractus solitarius and ventrolateral medulla","volume":"70","author":"Kaur","year":"2011","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"20200713","DOI":"10.1098\/rspb.2020.0713","article-title":"Androgen-dependent sexual dimorphism in pituitary tryptophan hydroxylase expression: relevance to sex differences in pituitary hormones","volume":"287","author":"Kawabata-Sakata","year":"2020","journal-title":"Proc. R. Soc."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0013-4694(80)90038-3","article-title":"Blockade of cortical spreading depression in electrically and chemically stimulated areas of cerebral cortex in rats","volume":"48","author":"Koroleva","year":"1980","journal-title":"Electroencephalogr. Clin. Neurophysiol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1111\/jpi.12224","article-title":"Anatomical and cellular localization of melatonin MT1 and MT2 receptors in the adult rat brain","volume":"58","author":"Lacoste","year":"2015","journal-title":"J. Pineal Res."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1445","DOI":"10.1007\/s12011-020-02247-z","article-title":"Melatonin ameliorates cadmium-induced affective and cognitive impairments and hippocampal oxidative stress in rat","volume":"199","author":"Lamtai","year":"2021","journal-title":"Biol. Trace Elem. Res."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"1553","DOI":"10.1177\/0271678X16657092","article-title":"\u2018Spreading depression of Le\u00e3o\u2019 and its emerging relevance to acute brain injury in humans","volume":"37","author":"Lauritzen","year":"2017","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1152\/jn.1944.7.6.359","article-title":"Spreading depression of activity in the cerebral cortex","volume":"7","author":"Le\u00e3o","year":"1944","journal-title":"J. Neurophysiol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1152\/jn.1947.10.6.409","article-title":"Further observations on the spreading depression of activity in the cerebral cortex","volume":"10","author":"Le\u00e3o","year":"1947","journal-title":"J. Neurophysiol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/j.lfs.2009.05.017","article-title":"L-glutamine supplementation during the lactation period facilitates cortical spreading depression in well-nourished and early-malnourished rats","volume":"85","author":"Lima","year":"2009","journal-title":"Life Sci."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1096\/fj.03-0739com","article-title":"Taurine prevents the neurotoxicity of beta-amyloid and glutamate receptor agonists: activation of GABA receptors and possible implications for Alzheimer\u2019s disease and other neurological disorders","volume":"18","author":"Louzada","year":"2004","journal-title":"FASEB J."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"1827","DOI":"10.1007\/s00726-011-0903-5","article-title":"Interactions of melatonin with mammalian mitochondria. Reducer of energy capacity and amplifier of permeability transition","volume":"42","author":"Martinis","year":"2012","journal-title":"Amino Acids"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.neuropharm.2014.06.027","article-title":"Prooxidant versus antioxidant brain action of ascorbic acid in well-nourished and malnourished rats as a function of dose: a cortical spreading depression and malondialdehyde analysis","volume":"86","author":"Mendes-Da-Silva","year":"2014","journal-title":"Neuropharmacology"},{"key":"ref9001","doi-asserted-by":"crossref","first-page":"3170","DOI":"10.1016\/S0021-9258(19)45228-9","article-title":"The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase","volume":"247","author":"Misra","year":"1972","journal-title":"J. Biol. Chem."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1111\/j.1751-1097.1989.tb04153.x","article-title":"Elicitation of spreading depression by rose Bengal photodynamic action","volume":"50","author":"Netto","year":"1989","journal-title":"Photochem. Photobiol."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"1369","DOI":"10.1016\/S0006-2952(01)00615-3","article-title":"Comparative pharmacological studies of melatonin receptors: MT1, MT2 and MT3\/QR2. Tissue distribution of MT3\/QR2","volume":"61","author":"Nosjean","year":"2001","journal-title":"Biochem. Pharmacol."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1016\/0003-2697(79)90738-3","article-title":"Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction","volume":"95","author":"Ohkawa","year":"1979","journal-title":"Anal. Biochem."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"619","DOI":"10.3109\/10715769709097865","article-title":"Antioxidant and prooxidant effects of ascorbic acid, dehydroascorbic acid and flavonoids on LDL submitted to different degrees of oxidation","volume":"27","author":"Otero","year":"1997","journal-title":"Free Radic. Res."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1007\/s12640-012-9337-4","article-title":"Melatonin antioxidative defense: therapeutical implications for aging and neurodegenerative processes","volume":"23","author":"Pandi-Perumal","year":"2013","journal-title":"Neurotox. Res."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/0165-0270(85)90031-7","article-title":"Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat","volume":"14","author":"Pellow","year":"1985","journal-title":"J. Neurosci. Methods"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1038\/33308","article-title":"Vitamin C exhibits prooxidant properties","volume":"392","author":"Podmore","year":"1998","journal-title":"Nature"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1111\/j.1600-079x.1993.tb00498.x","article-title":"Melatonin, hydroxyl radical-mediated oxidative damage, and aging: a hypothesis","volume":"14","author":"Poeggeler","year":"1993","journal-title":"J. Pineal Res."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.ejpn.2022.03.010","article-title":"Sleep in children with refractory epilepsy and epileptic encephalopathies: a systematic review of literature","volume":"38","author":"Proost","year":"2022","journal-title":"Eur. J. Paediatr. Neurol."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"1844","DOI":"10.1016\/j.bcp.2010.07.041","article-title":"Melatonin: a pleiotropic molecule regulating inflammation","volume":"80","author":"Radogna","year":"2010","journal-title":"Biochem. Pharmacol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"3863","DOI":"10.1007\/s00018-017-2609-7","article-title":"Melatonin as a mitochondria-targeted antioxidant: one of evolution\u2019s best ideas","volume":"74","author":"Reiter","year":"2017","journal-title":"Cell. Mol. Life Sci."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1007\/s00018-023-04736-5","article-title":"Brain washing and neural health: role of age, sleep, and the cerebrospinal fluid melatonin rhythm","volume":"80","author":"Reiter","year":"2023","journal-title":"Cell. Mol. Life Sci."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"509","DOI":"10.3390\/molecules23020509","article-title":"Mitochondria: central organelles for melatonin\u2019s antioxidant and anti-aging actions","volume":"23","author":"Reiter","year":"2018","journal-title":"Molecules"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1046\/j.1600-079x.2003.00092.x","article-title":"Regulation of antioxidant enzymes: a significant role for melatonin","volume":"36","author":"Rodriguez","year":"2004","journal-title":"J. Pineal Res."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"3851","DOI":"10.2174\/0929867324666170718105557","article-title":"Clinical uses of melatonin in neurological diseases and mental and behavioural disorders","volume":"24","author":"Sanchez-Barcelo","year":"2017","journal-title":"Curr. Med. Chem."},{"key":"ref63","first-page":"866","article-title":"The laboratory rat: relating its age with Human's","volume":"4","author":"Sengupta","year":"2013","journal-title":"Int. J. Prev. Med."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1016\/j.physbeh.2017.02.012","article-title":"Maternal administration of melatonin prevents spatial learning and memory deficits induced by developmental ethanol and lead co-exposure","volume":"173","author":"Soleimani","year":"2017","journal-title":"Physiol. Behav."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1080\/1028415X.2019.1602987","article-title":"Sepsis impairs the propagation of cortical spreading depression in rats and this effect is prevented by antioxidant extract","volume":"24","author":"Sousa","year":"2021","journal-title":"Nutr. Neurosci."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1016\/j.neubiorev.2021.04.034","article-title":"Neurocognitive effects of melatonin treatment in healthy adults and individuals with Alzheimer\u2019s disease and insomnia: a systematic review and meta-analysis of randomized controlled trials","volume":"127","author":"Sumsuzzman","year":"2021","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"598788","DOI":"10.3389\/fendo.2021.598788","article-title":"Effects of melatonin on Neurobehavior and cognition in a cerebral palsy model of plppr5\u2212\/\u2212 mice","volume":"12","author":"Sun","year":"2021","journal-title":"Front. Endocrinol."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1111\/j.1600-079X.2007.00513.x","article-title":"Melatonin as a naturally occurring co-substrate of quinone reductase-2, the putative MT3 melatonin membrane receptor: hypothesis and significance","volume":"43","author":"Tan","year":"2007","journal-title":"J. Pineal Res."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1023\/a:1022575716111","article-title":"Application of potassium chloride to the surface of the rat visual cortex differentially affects the expression of presumptive neuroprotective molecules","volume":"31","author":"Torr\u00e3o","year":"2002","journal-title":"J. Neurocytol."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1016\/j.neuroscience.2013.02.019","article-title":"Litter size, age-related memory impairments, and microglial changes in rat dentate gyrus: stereological analysis and three dimensional morphometry","volume":"238","author":"Viana","year":"2013","journal-title":"Neuroscience"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1590\/1516-4446-2021-2156","article-title":"Melatonin use during pregnancy and lactation: a scoping review of human studies","volume":"44","author":"Vine","year":"2022","journal-title":"Braz J Psychiatry."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1016\/j.freeradbiomed.2018.12.014","article-title":"Melatonin receptor activation provides cerebral protection after traumatic brain injury by mitigating oxidative stress and inflammation via the Nrf2 signaling pathway","volume":"131","author":"Wang","year":"","journal-title":"Free Radic. Biol. Med."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"903","DOI":"10.3390\/cells8080903","article-title":"Antioxidant and Prooxidant activities of melatonin in the presence of copper and polyphenols in vitro and in vivo","volume":"8","author":"Wang","year":"","journal-title":"Cells"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/s0014-5793(01)02680-1","article-title":"Prooxidant activity of melatonin promotes fas-induced cell death in human leukemic Jurkat cells","volume":"502","author":"Wolfler","year":"2001","journal-title":"FEBS Lett."},{"key":"ref9002","doi-asserted-by":"publisher","first-page":"1406","DOI":"10.3390\/nu15061406","article-title":"Molecular Mechanisms of the Melatonin Receptor Pathway Linking Circadian Rhythm to Type 2 Diabetes Mellitus","volume":"15","author":"Xia","year":"2023","journal-title":"Nutrients"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1111\/j.1600-079x.1997.tb00302.x","article-title":"Pharmacokinetics and oral bioavailability of exogenous melatonin in preclinical animal models and clinical implications","volume":"22","author":"Yeleswaram","year":"1997","journal-title":"J. Pineal Res."},{"key":"ref76","doi-asserted-by":"crossref","first-page":"181","DOI":"10.14712\/fb2016062050181","article-title":"The potential role of melatonin on memory function: lessons from rodent studies","volume":"62","author":"Zakaria","year":"2016","journal-title":"Folia Biol."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1111\/jpi.12162","article-title":"Melatonin: a well-documented antioxidant with conditional prooxidant actions","volume":"57","author":"Zhang","year":"2014","journal-title":"J. Pineal Res."},{"key":"ref78","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1111\/j.1600-079X.2011.00894.x","article-title":"Impaired mitochondrial complex III and melatonin responsive reactive oxygen species generation in kidney mitochondria of db\/db mice","volume":"51","author":"Zhang","year":"2011","journal-title":"J. Pineal Res."},{"key":"ref79","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1111\/j.1600-079X.2010.00815.x","article-title":"The role of mitochondrial complex III in melatonin-induced ROS production in cultured mesangial cells","volume":"50","author":"Zhang","year":"2011","journal-title":"J. Pineal Res."}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1269609\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,30]],"date-time":"2024-10-30T19:04:45Z","timestamp":1730315085000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1269609\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,12]]},"references-count":81,"alternative-id":["10.3389\/fnins.2023.1269609"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2023.1269609","relation":{},"ISSN":["1662-453X"],"issn-type":[{"value":"1662-453X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,12]]},"article-number":"1269609"}}