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Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry

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ISSN (Print): 1871-5230
ISSN (Online): 1875-614X

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Research Article

Prepubertal Continuous Dietary Folate Fortification Enhances the Brain Function of Adult Mice by Modulating Antioxidant Status, Inflammation, and Brain Neurotransmitter Levels

Author(s): Olakunle J. Onaolapo, Anthony T. Olofinnade, Folusho O. Ojo, Joshua Falade and Adejoke Y. Onaolapo*

Volume 22, Issue 3, 2023

Published on: 08 October, 2023

Page: [198 - 209] Pages: 12

DOI: 10.2174/0118715230249814230925060325

Price: $65

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Abstract

Background: The benefits of folic acid supplementation have been documented in several studies. However, while evidence exists regarding its benefits for growth and haematologic parameters, its possible effects on the brain have been less examined.

Objectives: The study aimed to examine the benefits of dietary folic acid supplementation (beginning in the prepubertal period) on neurobehaviour, oxidative stress, inflammatory parameters, and neurotransmitter levels in adult mice.

Methods: Forty-eight prepubertal male mice were assigned into four groups of 12 animals each. Mice were grouped into normal control (fed standard diet) and three groups fed folic acid supplemented diet at 2.5, 5, and 10 mg/kg of feed. Animals were fed a standard diet or folic acid-supplemented diet for eight weeks during which food intake and body weight were assessed. On postnatal day 78, animals were exposed to the open-field, Y-maze, radial arm maze, elevated plus maze, bar test, and models of behavioural despair. 24 hours after the last behavioural test, animals were made to fast overnight and then sacrificed by cervical dislocation. Blood was then taken for the assessment of blood glucose, leptin, and insulin levels. Homogenates of brain tissue were prepared and used for the assessment of biochemical parameters.

Results: Results showed a concentration-dependent increase in body weight, and improved antioxidant status, memory scores, and acetylcholine levels. Also, a decrease in food intake, blood glucose, insulin, and leptin levels was observed. A reduction in open-field behaviour, anxiety-related behaviour, and proinflammatory markers, was also observed.

Conclusion: The beneficial effect of prepubertal continuous dietary folate fortification on the brain (as the animal ages) has been shown in this study.

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[1]
Prado, E.L.; Dewey, K.G. Nutrition and brain development in early life. Nutr. Rev., 2014, 72(4), 267-284.
[http://dx.doi.org/10.1111/nure.12102] [PMID: 24684384]
[2]
Cusick, S.E.; Georgieff, M.K. The role of nutrition in brain development: The golden opportunity of the “first 1000 days”. J. Pediatr., 2016, 175, 16-21.
[http://dx.doi.org/10.1016/j.jpeds.2016.05.013] [PMID: 27266965]
[3]
Onaolapo, A.Y.; Aina, O.A.; Onaolapo, O.J. Melatonin attenuates behavioural deficits and reduces brain oxidative stress in a rodent model of schizophrenia. Biomed. Pharmacother., 2017, 92, 373-383. a
[http://dx.doi.org/10.1016/j.biopha.2017.05.094] [PMID: 28554133]
[4]
Onaolapo, A.Y.; Adebayo, A.N.; Onaolapo, O.J. Exogenous daytime melatonin modulates response of adolescent mice in a repeated un-predictable stress paradigm. Naunyn Schmiedebergs Arch. Pharmacol., 2017, 390(2), 149-161.
[http://dx.doi.org/10.1007/s00210-016-1314-7] [PMID: 27844092]
[5]
Onaolapo, O.J.; Ademakinwa, O.Q.; Olalekan, T.O.; Onaolapo, A.Y. Ketamine-induced behavioural and brain oxidative changes in mice: An assessment of possible beneficial effects of zinc as mono- or adjunct therapy. Psychopharmacology, 2017, 234(18), 2707-2725. c
[http://dx.doi.org/10.1007/s00213-017-4666-x] [PMID: 28612134]
[6]
Onaolapo, O.J.; Onaolapo, A.Y. Nutrition, nutritional deficiencies, and schizophrenia: An association worthy of constant reassessment. World J. Clin. Cases, 2021, 9(28), 8295-8311.
[http://dx.doi.org/10.12998/wjcc.v9.i28.8295] [PMID: 34754840]
[7]
Onaolapo, O.J.; Onaolapo, A.Y. Melatonin, adolescence, and the brain: An insight into the period-specific influences of a multifunctional signaling molecule. Birth Defects Res., 2017, 109(20), 1659-1671.
[http://dx.doi.org/10.1002/bdr2.1171] [PMID: 29251845]
[8]
Falade, J.; Onaolapo, A.Y.; Onaolapo, O.J. Evaluation of the behavioural, antioxidative and histomorphological effects of folic acidsupplemented diet in dexamethasone-induced depression in mice. Cent. Nerv. Syst. Agents Med. Chem., 2021, 21(1), 73-81.
[http://dx.doi.org/10.2174/1871524921666210114125355] [PMID: 33459248]
[9]
Falade, J.; Onaolapo, A.Y.; Onaolapo, O.J. The role of folate-supplementation in depression: A narrative review. Curr. Psychopharmacol., 2021, 10(2), 115-122.
[http://dx.doi.org/10.2174/2211556009666201207233954]
[10]
Onaolapo, A.Y.; Obelawo, A.Y.; Onaolapo, O.J. Brain ageing, cognition and diet: A review of the emerging roles of food-based nootropics in mitigating age-related memory decline. Curr. Aging Sci., 2019, 12(1), 2-14.
[http://dx.doi.org/10.2174/1874609812666190311160754] [PMID: 30864515]
[11]
Onaolapo, A.Y.; Onaolapo, O.J. African plants with antidiabetic potentials: Beyond glycaemic control to central nervous system benefits. Curr. Diabetes Rev., 2020, 16(5), 419-437.
[http://dx.doi.org/10.2174/1573399815666191106104941] [PMID: 31702529]
[12]
Onaolapo, O.J.; Odeniyi, A.O.; Onaolapo, A.Y. Parkinson’s disease: Is there a role for dietary and herbal supplements? CNS Neurol. Disord. Drug Targets, 2021, 20(4), 343-365.
[http://dx.doi.org/10.2174/1871527320666210218082954] [PMID: 33602107]
[13]
Olofinnade, A.T.; Onaolapo, A.Y.; Onaolapo, O.J. Concentration dependent effects of dietary L-ascorbic acid fortification in the brains of healthy mice. Cent. Nerv. Syst. Agents Med. Chem., 2021, 21(2), 104-113.
[http://dx.doi.org/10.2174/1871524921666210315130023] [PMID: 33719957]
[14]
Sharma, Y.; Popescu, A.; Horwood, C.; Hakendorf, P.; Thompson, C. Relationship between vitamin C deficiency and cognitive impairment in older hospitalised patients: A cross-sectional study. Antioxidants, 2022, 11(3), 463.
[http://dx.doi.org/10.3390/antiox11030463] [PMID: 35326113]
[15]
Stover, P.J. One-carbon metabolism-genome interactions in folate-associated pathologies. J. Nutr., 2009, 139(12), 2402-2405.
[http://dx.doi.org/10.3945/jn.109.113670] [PMID: 19812215]
[16]
Lyon, P.; Strippoli, V.; Fang, B.; Cimmino, L. B vitamins and one-carbon metabolism: Implications in human health and disease. Nutrients, 2020, 12(9), 2867.
[http://dx.doi.org/10.3390/nu12092867] [PMID: 32961717]
[17]
Hariz, A.; Bhattacharya, P.T. Megaloblastic Anemia.StatPearls; StatPearls Publishing: Treasure Island, FL, 2022.
[18]
Safi, J.; Joyeux, L.; Chalouhi, G.E. Periconceptional folate deficiency and implications in neural tube defects. J. Pregnancy, 2012, 2012, 1-9.
[http://dx.doi.org/10.1155/2012/295083] [PMID: 22900183]
[19]
Wallingford, J.B.; Niswander, L.A.; Shaw, G.M.; Finnell, R.H. The continuing challenge of understanding, preventing, and treating neural tube defects. Science, 2013, 339(6123), 1222002.
[http://dx.doi.org/10.1126/science.1222002] [PMID: 23449594]
[20]
Naninck, E.F.G.; Stijger, P.C.; Brouwer-Brolsma, E.M. The importance of maternal folate status for brain development and function of offspring. Adv. Nutr., 2019, 10(3), 502-519.
[http://dx.doi.org/10.1093/advances/nmy120] [PMID: 31093652]
[21]
Kucha, W.; Seifu, D.; Tirsit, A.; Yigeremu, M.; Abebe, M.; Hailu, D.; Tsehay, D.; Genet, S. Folate, vitamin B12, and homocysteine levels in women with neural tube defect-affected pregnancy in addis ababa, ethiopia. Front. Nutr., 2022, 9, 873900.
[http://dx.doi.org/10.3389/fnut.2022.873900] [PMID: 35464038]
[22]
Bille, C.; Murray, J.C.; Olsen, S.F. Folic acid and birth malformations. BMJ, 2007, 334(7591), 433-434.
[http://dx.doi.org/10.1136/bmj.39133.386296.BE] [PMID: 17332537]
[23]
De-Regil, LM; Fernández-Gaxiola, AC; Dowswell, T; Peña-Rosas, JP Effects and safety of periconceptional folate supplementation for preventing birth defects. Cochrane Database Syst. Rev., 2015, 2015(12), CD007950.
[http://dx.doi.org/10.1002/14651858.CD007950.pub3]
[24]
Kelly, D.; O’Dowd, T.; Reulbach, U. Use of folic acid supplements and risk of cleft lip and palate in infants: A population-based cohort study. Br. J. Gen. Pract., 2012, 62(600), e466-e472.
[http://dx.doi.org/10.3399/bjgp12X652328] [PMID: 22781994]
[25]
Burdge, G.C.; Lillycrop, K.A.; Phillips, E.S.; Slater-Jefferies, J.L.; Jackson, A.A.; Hanson, M.A. Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J. Nutr., 2009, 139(6), 1054-1060.
[http://dx.doi.org/10.3945/jn.109.104653] [PMID: 19339705]
[26]
Silva, C.; Keating, E.; Pinto, E. The impact of folic acid supplementation on gestational and long term health: Critical temporal windows, benefits and risks. Porto Biomed. J., 2017, 2(6), 315-332.
[http://dx.doi.org/10.1016/j.pbj.2017.05.006]
[27]
Tsui, J.C.; Nordstrom, J.W. Folate status of adolescents: Effects of folic acid supplementation. J. Am. Diet. Assoc., 1990, 90(11), 1551-1556.
[http://dx.doi.org/10.1016/S0002-8223(21)01839-3] [PMID: 2229851]
[28]
Taneja, S.; Bhandari, N.; Strand, T.A.; Sommerfelt, H.; Refsum, H.; Ueland, P.M.; Schneede, J.; Bahl, R.; Bhan, M.K. Cobalamin and folate status in infants and young children in a low-to-middle income community in India. Am. J. Clin. Nutr., 2007, 86(5), 1302-1309.
[http://dx.doi.org/10.1093/ajcn/86.5.1302] [PMID: 17991639]
[29]
Cuevas-Nasu, L.; Mundo-Rosas, V.; Shamah-Levy, T.; Méndez-Gómez Humaran, I.; Ávila-Arcos, M.A.; Rebollar-Campos, M.R.; Villalpando, S. Prevalence of folate and vitamin B12 deficiency in Mexican children aged 1 to 6 years in a population-based survey. Salud Publica Mex., 2012, 54(2), 116-124.
[http://dx.doi.org/10.1590/S0036-36342012000200007] [PMID: 22535170]
[30]
Zhou, D.; Li, Z.; Sun, Y.; Yan, J.; Huang, G.; Li, W. Early life stage folic acid deficiency delays the neurobehavioral development and cognitive function of rat offspring by hindering de novo telomere synthesis. Int. J. Mol. Sci., 2022, 23(13), 6948.
[http://dx.doi.org/10.3390/ijms23136948] [PMID: 35805953]
[31]
Gosdin, L.; Sharma, A.J.; Tripp, K.; Amoaful, E.F.; Mahama, A.B.; Selenje, L.; Jefferds, M.E.; Martorell, R.; Ramakrishnan, U.; Addo, O.Y. A school-based weekly iron and folic acid supplementation program effectively reduces anemia in a prospective cohort of ghanaian adolescent girls. J. Nutr., 2021, 151(6), 1646-1655.
[http://dx.doi.org/10.1093/jn/nxab024] [PMID: 33758915]
[32]
Honnakamble, R.A.; Singh, M.; Rajoura, O.P. Assessment of weekly iron–Folic acid supplementation with and without health education on anemia in adolescent girls: A comparative study. Int. J. Prev. Med., 2020, 11(1), 203.
[http://dx.doi.org/10.4103/ijpvm.IJPVM_552_18] [PMID: 33815727]
[33]
Henzel, K.S.; Ryan, D.P.; Schröder, S.; Weiergräber, M.; Ehninger, D. High-dose maternal folic acid supplementation before conception impairs reversal learning in offspring mice. Sci. Rep., 2017, 7(1), 3098.
[http://dx.doi.org/10.1038/s41598-017-03158-1] [PMID: 28596566]
[34]
Onaolapo, A.Y.; Onaolapo, O.J.; Nwoha, P.U. Alterations in behaviour, cerebral cortical morphology and cerebral oxidative stress markers following aspartame ingestion. J. Chem. Neuroanat., 2016, 78, 42-56. a
[http://dx.doi.org/10.1016/j.jchemneu.2016.08.006] [PMID: 27565676]
[35]
Onaolapo, A.Y.; Onaolapo, O.J.; Nwoha, P.U. Aspartame and the hippocampus: Revealing a bidirectional, dose/time-dependent behav-ioural and morphological shift in mice. Neurobiol. Learn. Mem., 2017, 139, 76-88.
[http://dx.doi.org/10.1016/j.nlm.2016.12.021] [PMID: 28049023]
[36]
Onaolapo, A.Y.; Sulaiman, H.; Olofinnade, A.T.; Onaolapo, O.J. Antidepressant-like potential of silymarin and silymarin-sertraline combi-nation in mice: Highlighting effects on behaviour, oxidative stress, and neuroinflammation. World J. Pharmacol., 2022, 11(3), 27-47.
[http://dx.doi.org/10.5497/wjp.v11.i3.27]
[37]
Onaolapo, O.J.; Aremu, O.S.; Onaolapo, A.Y. Monosodium glutamate-associated alterations in open field, anxiety-related and conditioned place preference behaviours in mice. Naunyn Schmiedebergs Arch. Pharmacol., 2017, 390(7), 677-689.
[http://dx.doi.org/10.1007/s00210-017-1371-6] [PMID: 28357464]
[38]
Onaolapo, A.Y.; Odetunde, I.; Akintola, A.S.; Ogundeji, M.O.; Ajao, A.; Obelawo, A.Y.; Onaolapo, O.J. Dietary composition modulates impact of food-added monosodium glutamate on behaviour, metabolic status and cerebral cortical morphology in mice. Biomed. Pharmacother., 2019, 109, 417-428.
[http://dx.doi.org/10.1016/j.biopha.2018.10.172] [PMID: 30399577]
[39]
Onaolapo, O.J.; Adekola, M.A.; Azeez, T.O.; Salami, K.; Onaolapo, A.Y. l-Methionine and silymarin: A comparison of prophylactic protective capabilities in acetaminophen-induced injuries of the liver, kidney and cerebral cortex. Biomed. Pharmacother., 2017, 85, 323-333.
[http://dx.doi.org/10.1016/j.biopha.2016.11.033] [PMID: 27889232]
[40]
Olofinnade, A.T.; Onaolapo, A.Y.; Onaolapo, O.J.; Olowe, O.A. Hazelnut modulates neurobehaviour and ameliorates ageing-induced oxidative stress, and caspase-3-mediated apoptosis in mice. Curr. Aging Sci., 2021, 14(2), 154-162.
[http://dx.doi.org/10.2174/1874609813666201228112349] [PMID: 33371863]
[41]
Onaolapo, A.Y.; Adebisi, E.O.; Adeleye, A.E.; Olofinnade, A.T.; Onaolapo, O.J. Dietary melatonin protects against behavioural, metabolic, oxidative, and organ morphological changes in mice that are fed high-fat, high- sugar diet. Endocr. Metab. Immune Disord. Drug Targets, 2020, 20(4), 570-583. a
[http://dx.doi.org/10.2174/1871530319666191009161228] [PMID: 32138638]
[42]
Onaolapo, O.J.; Jegede, O.R.; Adegoke, O.; Ayinde, M.O.; Akeredolu, O.M.; Onaolapo, A.Y. Dietary zinc supplement militates against ketamine-induced behaviours by age-dependent modulation of oxidative stress and acetylcholinesterase activity in mice. Pharmacol. Rep., 2020, 72(1), 55-66.
[http://dx.doi.org/10.1007/s43440-019-00003-2] [PMID: 32016846]
[43]
Olofinnade, A.T.; Onaolapo, A.Y.; Onaolapo, O.J.; Olowe, O.A.; Mollica, A.; Zengin, G.; Stefanucci, A. Corylus avellana L. modulates neurobehaviour and brain chemistry following high-fat diet. Front. Biosci., 2021, 26(3), 537-551.
[http://dx.doi.org/10.2741/4906] [PMID: 33049682]
[44]
Onaolapo, OJ; Odeniyi, AO; Jonathan, SO; Samuel, MO; Amadiegwu, D; Olawale, A; Tiamiyu, AO; Ojo, FO; Yahaya, HA; Ayeni, OJ; Onaolapo, AY An investigation of the anti-parkinsonism potential of Co-enzyme Q10 and Co-enzyme Q10 /Levodopa-carbidopa combi-nation in mice. Curr. Aging Sci., 2021, 14(1), 62-75.
[http://dx.doi.org/10.2174/1874609812666191023153724]
[45]
Fink-Jensen, A.; Schmidt, L.S.; Dencker, D.; Schülein, C.; Wess, J.; Wörtwein, G.; Woldbye, DP. Antipsychotic-induced catalepsy is attenuated in mice lacking the M4 muscarinic acetylcholine receptor. Eur. J. Pharmacol., 2011, 656(1-3), 39-44.
[http://dx.doi.org/10.1016/j.ejphar.2011.01.018]
[46]
Ay, O.; Oi, O.; Fo, Y. am, A.; Io, A.; Oj, O. Oral Monosodium glutamate differentially affects open field behaviours, Behavioural despair and place preference in male and female mice. Curr. Psychopharmacol., 2019, 8(2), 130-145.
[http://dx.doi.org/10.2174/2211556008666181213160527]
[47]
Onaolapo, O.J.; Omotoso, S.A.; Olofinnade, A.T.; Onaolapo, A.Y. Anti-inflammatory, anti-oxidant, and anti-lipaemic effects of daily die-tary coenzyme-Q10 supplement in a mouse model of metabolic syndrome. Antiinflamm. Antiallergy Agents Med. Chem., 2021, 20(4), 380-388. a
[http://dx.doi.org/10.2174/1871523020666210427111328] [PMID: 33906592]
[48]
Chmurzynska, A.; Malinowska, A.M.; Twardowska-Rajewska, J.; Gawecki, J. Elderly women: Homocysteine reduction by short-term folic acid supplementation resulting in increased glucose concentrations and affecting lipid metabolism (C677T MTHFR polymorphism). Nutrition, 2013, 29(6), 841-844.
[http://dx.doi.org/10.1016/j.nut.2012.09.015] [PMID: 23298970]
[49]
Kelly, K.; Kennelly, J.; Ordonez, M.; Nelson, R.; Leonard, K.; Stabler, S.; Gomez-Muñoz, A.; Field, C.; Jacobs, R. Excess folic acid in-creases lipid storage, weight gain, and adipose tissue inflammation in high fat diet-fed rats. Nutrients, 2016, 8(10), 594.
[http://dx.doi.org/10.3390/nu8100594] [PMID: 27669293]
[50]
Yadon, N.; Owen, A.; Cakora, P.; Bustamante, A.; Hall-South, A.; Smith, N.; Felder, M.R.; Vrana, P.B.; Shorter, K.R. A high methyl donor diet affects physiology and behavior in Peromyscus polionotus. Physiol. Behav., 2019, 209, 112615.
[http://dx.doi.org/10.1016/j.physbeh.2019.112615] [PMID: 31299371]
[51]
Mlodzik-Czyzewska, M.A.; Malinowska, A.M.; Chmurzynska, A. Low folate intake and serum levels are associated with higher body mass index and abdominal fat accumulation: A case control study. Nutr. J., 2020, 19(1), 53.
[http://dx.doi.org/10.1186/s12937-020-00572-6] [PMID: 32498709]
[52]
Asbaghi, O.; Ashtary-Larky, D.; Bagheri, R.; Moosavian, S.P.; Olyaei, H.P.; Nazarian, B.; Rezaei Kelishadi, M.; Wong, A.; Candow, D.G.; Dutheil, F.; Suzuki, K.; Alavi Naeini, A. Folic acid supplementation improves glycemic control for diabetes prevention and management: A systematic review and dose-response meta-analysis of randomized controlled trials. Nutrients, 2021, 13(7), 2355.
[http://dx.doi.org/10.3390/nu13072355] [PMID: 34371867]
[53]
Li, X.; Zhang, Y.; Jing, W.; Tang, W.; Xing, J.; Zhang, Y. Effects of folic acid supplementation to basal diets of broilers on growth perfor-mance, slaughter performance, IGF2 gene expression and methylation. Czech J. Anim. Sci., 2021, 66(12), 504-512.
[http://dx.doi.org/10.17221/76/2021-CJAS]
[54]
Chan, C.W.; Chan, P.H.; Lin, B.F. Folate deficiency increased lipid accumulation and leptin production of adipocytes. Front. Nutr., 2022, 9, 852451.
[http://dx.doi.org/10.3389/fnut.2022.852451] [PMID: 35548560]
[55]
Liang, S.; Liu, X.; Zhao, J.; Liu, R.; Huang, X.; Liu, Y.; Yang, X.; Yang, X. Effects of high-dose folic acid on protein metabolism in breast muscle and performance of broilers. Poultry Science, 2022, 2022, 101935.
[http://dx.doi.org/10.1016/j.psj.2022.101935]
[56]
Cosín-Tomás, M.; Luan, Y.; Leclerc, D.; Malysheva, O.V.; Lauzon, N.; Bahous, R.H.; Christensen, K.E.; Caudill, M.A.; Rozen, R. Moderate folic acid supplementation in pregnant mice results in behavioral alterations in offspring with sex-specific changes in methyl metabolism. Nutrients, 2020, 12(6), 1716.
[http://dx.doi.org/10.3390/nu12061716] [PMID: 32521649]
[57]
Jadavji, N.M.; Wieske, F.; Dirnagl, U.; Winter, C. Methylenetetrahydrofolate reductase deficiency alters levels of glutamate and γ-aminobutyric acid in brain tissue. Mol. Genet. Metab. Rep., 2015, 3, 1-4.
[http://dx.doi.org/10.1016/j.ymgmr.2015.02.001] [PMID: 26937386]
[58]
Sharples, S.A.; Humphreys, J.M.; Jensen, A.M.; Dhoopar, S.; Delaloye, N.; Clemens, S.; Whelan, P.J. Dopaminergic modulation of loco-motor network activity in the neonatal mouse spinal cord. J. Neurophysiol., 2015, 113(7), 2500-2510.
[http://dx.doi.org/10.1152/jn.00849.2014] [PMID: 25652925]
[59]
Onaolapo, A.Y.; Onaolapo, O.J.; Ibekwe, C.B.; Sulaiman, A.H.; Rauf, R. Low-dose L-methionine-associated changes in behavioural indi-ces in young rats. Int. J. Neurosci. Behav. Sci., 2016, 4(1), 11-19.
[http://dx.doi.org/10.13189/ijnbs.2016.040102]
[60]
Onaolapo, O.J.; Onaolapo, A.Y.; Akanmu, M.A.; Gbola, O. Evidence of alterations in brain structure and antioxidant status following ‘low-dose’ monosodium glutamate ingestion. Pathophysiology, 2016, 23(3), 147-156.
[http://dx.doi.org/10.1016/j.pathophys.2016.05.001] [PMID: 27312658]
[61]
Onaolapo, O.J.; Onaolapo, A.Y.; Akanmu, M.A.; Olayiwola, G. Foraging enrichment modulates open field response to monosodiumglutamate in mice. Ann. Neurosci., 2015, 22(3), 162-170.
[http://dx.doi.org/10.5214/ans.0972.7531.220306] [PMID: 26130924]
[62]
Muñoz-Villegas, P.; Rodríguez, V.M.; Giordano, M.; Juárez, J. Risk-taking, locomotor activity and dopamine levels in the nucleus accum-bens and medial prefrontal cortex in male rats treated prenatally with alcohol. Pharmacol. Biochem. Behav., 2017, 153, 88-96.
[http://dx.doi.org/10.1016/j.pbb.2016.12.011] [PMID: 28011337]
[63]
Ryczko, D.; Dubuc, R. Dopamine and the Brainstem Locomotor Networks: From Lamprey to Human. Front. Neurosci., 2017, 11, 295.
[http://dx.doi.org/10.3389/fnins.2017.00295] [PMID: 28603482]
[64]
Ryczko, D.; Grätsch, S.; Alpert, M.H.; Cone, J.J.; Kasemir, J.; Ruthe, A.; Beauséjour, P.A.; Auclair, F.; Roitman, M.F.; Alford, S.; Dubuc, R. Descending dopaminergic inputs to reticulospinal neurons promote locomotor movements. J. Neurosci., 2020, 40(44), 8478-8490.
[http://dx.doi.org/10.1523/JNEUROSCI.2426-19.2020] [PMID: 32998974]
[65]
Mustard, J.A.; Jones, L.; Wright, G.A. GABA signaling affects motor function in the honey bee. J. Insect Physiol., 2020, 120, 103989.
[http://dx.doi.org/10.1016/j.jinsphys.2019.103989] [PMID: 31805284]
[66]
Zhou, Y.; Cong, Y.; Liu, H. Folic acid ameliorates depression-like behaviour in a rat model of chronic unpredictable mild stress. BMC Neurosci., 2020, 21(1), 1.
[http://dx.doi.org/10.1186/s12868-020-0551-3] [PMID: 31941442]
[67]
Al-Khatib, I.M.H.; Dökmeci, I.; Fujiwara, M. Differential role of nucleus accumbens and caudate-putamen in mediating the effect of nomifensine and methamphetamine on ambulation and rearing of rats in the open-field test. Jpn. J. Pharmacol., 1995, 67(1), 69-77.
[http://dx.doi.org/10.1254/jjp.67.69] [PMID: 7745847]
[68]
McGarel, C.; Pentieva, K.; Strain, J.J.; McNulty, H. Emerging roles for folate and related B-vitamins in brain health across the lifecycle. Proc. Nutr. Soc., 2015, 74(1), 46-55.
[http://dx.doi.org/10.1017/S0029665114001554] [PMID: 25371067]
[69]
Shooshtari, M.K.; Moazedi, A.A.; Parham, G.A. Memory and motor coordination improvement by folic Acid supplementation in healthy adult male rats. Iran. J. Basic Med. Sci., 2012, 15(6), 1173-1179.
[PMID: 23653847]
[70]
Reynolds, E.H. Folic acid, ageing, depression, and dementia. BMJ, 2002, 324(7352), 1512-1515.
[http://dx.doi.org/10.1136/bmj.324.7352.1512] [PMID: 12077044]
[71]
Singh, R.; Kanwar, S.S.; Sood, P.K.; Nehru, B. Beneficial effects of folic acid on enhancement of memory and antioxidant status in aged rat brain. Cell. Mol. Neurobiol., 2011, 31(1), 83-91.
[http://dx.doi.org/10.1007/s10571-010-9557-1] [PMID: 21170581]
[72]
Barichello, T.; Generoso, J.S.; Simões, L.R.; Steckert, A.V.; Moreira, A.P.; Dominguini, D.; Ferrari, P.; Gubert, C.; Kapczinski, F.; Jornada, L.K.; Danielski, L.G.; Petronilho, F.; Budni, J.; Quevedo, J. Folic acid prevented cognitive impairment in experimental pneumococcal meningitis. J. Neural Transm. (Vienna), 2015, 122(5), 643-651.
[http://dx.doi.org/10.1007/s00702-014-1302-3] [PMID: 25233798]
[73]
Eskandary, A.; Moazedi, A.A.; Mamani, N. The synergist effects of folic acid and vitamin B12 on spatial memory in adult male rat model of alzheimer’s disease. Majallah-i Ilmi-i Danishgah-i Ulum-i Pizishki-i Rafsanjan, 2018, 16(10), 925-938.
[74]
Gofir, A.; Wibowo, S.; Hakimi, M.; Putera, D.D.; Satriotomo, I.; Mustofa, M. Folic acid treatment for patients with vascular cognitive im-pairment: A systematic review and meta-analysis. Int. J. Neuropsychopharmacol., 2021, 25(2), pyab076. Epub ahead of print
[http://dx.doi.org/10.1093/ijnp/pyab076] [PMID: 34791275]
[75]
Garcez, M.L.; Cassoma, R.C.S.; Mina, F.; Bellettini-Santos, T.; da Luz, A.P.; Schiavo, G.L.; Medeiros, E.B.; Campos, A.C.B.F.; da Silva, S.; Rempel, L.C.T.; Steckert, A.V.; Barichello, T.; Budni, J. Folic acid prevents habituation memory impairment and oxidative stress in an ag-ing model induced by D-galactose. Metab. Brain Dis., 2021, 36(2), 213-224.
[http://dx.doi.org/10.1007/s11011-020-00647-7] [PMID: 33219893]
[76]
Gao, L.; Liu, X.; Yu, L.; Wu, J.; Xu, M.; Liu, Y. Folic acid exerts antidepressant effects by upregulating brain-derived neurotrophic factor and glutamate receptor 1 expression in brain. Neuroreport, 2017, 28(16), 1078-1084.
[http://dx.doi.org/10.1097/WNR.0000000000000887] [PMID: 28906345]
[77]
Deniz, B.F.; Confortim, H.D.; Deckmann, I.; Miguel, P.M.; Bronauth, L.; de Oliveira, B.C.; Barbosa, S.; Cechinel, L.R.; Siqueira, I.R.; Pereira, L.O. Folic acid supplementation during pregnancy prevents cognitive impairments and BDNF imbalance in the hippocampus of the offspring after neonatal hypoxia-ischemia. J. Nutr. Biochem., 2018, 60, 35-46.
[http://dx.doi.org/10.1016/j.jnutbio.2018.06.008] [PMID: 30064014]
[78]
Zhang, Q.; Huang, Q.; Yao, L.; Liu, W.; Ruan, J.; Nong, Y.; Chen, Y.; Fan, L.; Wei, J.; Wang, S.; Sun, L.; Li, H.; Zhang, Y.; Zhang, X.; Liu, F. Gestational folic acid administration alleviated maternal postpartum emotional and cognitive dysfunction in mice. Front. Pharmacol., 2021, 12, 701009.
[http://dx.doi.org/10.3389/fphar.2021.701009] [PMID: 34177603]
[79]
Bennett, C.; Green, J.; Ciancio, M.; Goral, J.; Pitstick, L.; Pytynia, M.; Meyer, A.; Kwatra, N.; Jadavji, N.M. Dietary folic acid deficiency impacts hippocampal morphology and cortical acetylcholine metabolism in adult male and female mice. Nutr. Neurosci., 2021, 1-9. Epub ahead of print
[http://dx.doi.org/10.1080/1028415X.2021.1932242] [PMID: 34042561]
[80]
Joshi, R.; Adhikari, S.; Patro, B.S.; Chattopadhyay, S.; Mukherjee, T. Free radical scavenging behavior of folic acid: Evidence for possible antioxidant activity. Free Radic. Biol. Med., 2001, 30(12), 1390-1399.
[http://dx.doi.org/10.1016/S0891-5849(01)00543-3] [PMID: 11390184]
[81]
Samblas, M.; Martínez, J.A.; Milagro, F. Folic acid improves the inflammatory response in LPS-activated THP-1 macrophages. Mediators Inflamm., 2018, 2018, 1-8.
[http://dx.doi.org/10.1155/2018/1312626] [PMID: 30116142]
[82]
El-khodary, N.M.; Dabees, H.; Werida, R.H. Folic acid effect on homocysteine, sortilin levels and glycemic control in type 2 diabetes mellitus patients. Nutr. Diabetes, 2022, 12(1), 33.
[http://dx.doi.org/10.1038/s41387-022-00210-6] [PMID: 35732620]
[83]
Cianciulli, A.; Calvello, R.; Porro, C.; Trotta, T.; Salvatore, R.; Panaro, M.A. PI3k/Akt signalling pathway plays a crucial role in the anti-inflammatory effects of curcumin in LPS-activated microglia. Int. Immunopharmacol., 2016, 36, 282-290.
[http://dx.doi.org/10.1016/j.intimp.2016.05.007] [PMID: 27208432]
[84]
Zhao, T.; Wu, D.; Du, J.; Liu, G.; Ji, G.; Wang, Z.; Peng, F.; Man, L.; Zhou, W.; Hao, A. Folic acid attenuates glial activation in neonatal mice and improves adult mood disorders through epigenetic regulation. Front. Pharmacol., 2022, 13, 818423.
[http://dx.doi.org/10.3389/fphar.2022.818423] [PMID: 35197855]
[85]
Amirahmadi, S.; Hosseini, M.; Ahmadabady, S.; Akbarian, M.; Abrari, K.; Vafaee, F.; Rajabian, A. Folic acid attenuated learning and memory impairment via inhibition of oxidative damage and acetylcholinesterase activity in hypothyroid rats. Metab. Brain Dis., 2021, 36(8), 2393-2403.
[http://dx.doi.org/10.1007/s11011-021-00815-3] [PMID: 34562187]

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