Skip to main content

Advertisement

Log in

D-galactose induced dysfunction in mice hippocampus and the possible antioxidant and neuromodulatory effects of selenium

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Aging is an ultimate reality that everyone has to face. D-galactose (D-gal) has been used extensively to develop aging model. Trace elements such as selenium (Se) have been used as a potential antioxidant for neuro-protection. The present work aims to develop therapeutic agents such as Se for the treatment of aging-induced neurological ailments such as anxiety, depression, and memory impairment. For this purpose, mice were treated with D-gal at a dose of 300 mg/ml/kg and various doses of Se (0.175 and 0.35mg/ml/kg) for 28 days. Behavioral tests were monitored after treatment days. After the behavioral assessment, mice were decapitated and their brains were collected. Hippocampi were removed from the brain for biochemical, neurochemical, and histopathological analysis. The present findings of behavioral analysis showed that D-gal-induced anxiety- and depression-like symptoms were inhibited by both doses of Se. D-gal-induced memory alteration was also prevented by repeated doses of Se (0.175 and 0.35mg/ml/kg). Biochemical analysis showed that D-gal-induced increase of oxidative stress and inflammatory markers and decrease of antioxidant enzymes and total protein contents in the hippocampus were prevented by Se administration. An increase in the activity of acetylcholinesterase was also diminished by Se. The neurochemical assessment showed that D-gal-induced increased serotonin metabolism and decreased acetylcholine levels in the hippocampus were restored by repeated treatment of Se. Histopathological estimations also exhibited; normalization of D-gal induced neurodegenerative changes. It is concluded that D-gal-induced dysfunction in mice hippocampus caused anxiety, depression, memory impairment, oxidative stress, neuro-inflammation, and histological alterations that were mitigated by Se via its antioxidant potential, anti-inflammatory property, and modulating capability of serotonergic and cholinergic functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Data Availability

Not applicable

References

  • Ataizi ZS, Ertilav K, Nazıroğlu M (2019) Mitochondrial oxidative stress-induced brain and hippocampus apoptosis decrease through modulation of caspase activity, Ca(2+) influx and inflammatory cytokine molecular pathways in the docetaxel-treated mice by melatonin and selenium treatments. Metab Brain Dis 34:1077–1089

    CAS  Google Scholar 

  • Aydoğan F, Taştan E, Aydın E, Şenes M, Akgedik Ş, Berkem R, Üstün H (2013) Antioxidant role of selenium in rats with experimental acute otitis media. Indian J Otolaryngol Head Neck Surgery 65:541–547

    Google Scholar 

  • Baker DJ, Childs BG, Durik M, Wijers ME, Sieben CJ, Zhong J, Pezeshki A (2016) Naturally occurring p16 Ink4a-positive cells shorten healthy lifespan. Nature 530:7589–7184

    Google Scholar 

  • Bampi SR, Casaril AM, Sabedra Sousa FS, Pesarico AP, Vieira B, Lenardão EJ, Savegnago L (2019). Repeated administration of a selenium-containing indolyl compound attenuates behavioural alterations by streptozotocin through modulation of oxidative stress in mice. Pharmacol Biochem Behav183:46-55.

  • Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. J Nature Reviews Drug Discovery 3:205–214

    CAS  Google Scholar 

  • Benn SC, Woolf CJ (2004) Adult neuron survival strategies—slamming on the brakes. J Nature Reviews Neurosci 5:9–686

    Google Scholar 

  • Besckow EM, Nonemacher NT, Garcia CS, da Silva Espíndola CN, Balbom ÉB, Gritzenco F, Savegnago L, Godoi B, Bortolatto CF, Brüning CA (2020) Antidepressant-like effect of a selenopropargylicbenzamide in mice: involvement of the serotonergic system. J Psychopharmacology (Berl) 237:3149–3159

    CAS  Google Scholar 

  • Biswas S, Anjum A, Banna HU, Rahman M, Siddique AE, Karim Y, Nikkon F, Haque A, Hossain K, Saud ZA (2019) Manganese attenuates the effects of arsenic on neurobehavioral and biochemical changes in mice co-exposed to arsenic and manganese. J Environ Sci Pollut Res Int 26:29257–29266

    CAS  Google Scholar 

  • Bonfili L, Cecarini V, Gogoi O, Berardi S, Scarpona S, Angeletti M, Rossi G, Eleuteri AM (2020) Gut microbiota manipulation through probiotics oral administration restores glucose homeostasis in a mouse model of Alzheimer's disease. Neurobiol Aging 87:35–43

    CAS  Google Scholar 

  • Brüning CA, Prigol M, Roehrs JA, Nogueira CW, Zeni G (2019) Involvement of the serotonergic system in the anxiolytic-like effect caused by m-trifluoromethyl-diphenyl diselenide in mice. J Behav. Brain Res 205:511–517

    Google Scholar 

  • Cabello-Verrugio C, Simon F, Trollet C, Santibañez JF (2016) Oxidative stress in disease and aging: mechanisms and therapies. J Oxidative Medicine and Cellular Longevity 2017:4310469

    Google Scholar 

  • Cai Z, Zhang J, Li H (2019) Selenium, aging and aging-related diseases. Aging Clin Exp Res 31:1035–1047

    Google Scholar 

  • Cao L, Zhang L, Zeng H, Wu RT, Wu TL, Cheng WH (2017) Analyses of selenotranscriptomes and selenium concentrations in response to dietary selenium deficiency and age reveal common and distinct patterns by tissue and sex in telomere-dysfunctional mice. J Nutr 147:1858–1866

    CAS  Google Scholar 

  • Casaril AM, Domingues M, de Andrade Lourenço D, Birmann PT, Padilha N, Vieira B, Begnini K, Seixas FK, Collares T, Lenardão EJ, Savegnago L (2019). Depression- and anxiogenic-like behaviors induced by lipopolysaccharide in mice are reversed by a selenium-containing indolyl compound: behavioral, neurochemical and computational insights involving the serotonergic system. J Psychiatr Res115:1-12.

  • Chow C, Tappel AL (1972) An enzymatic protective mechanism against lipid peroxidation damage to lungs of ozone-exposed rats. J Lipids 7:518–524

    CAS  Google Scholar 

  • Çoban J, Doğan-Ekici I, Aydın AF, Betül-Kalaz E, Doğru-Abbasoğlu S, Uysal M (2015). Blueberry treatment decreased D-galactose-induced oxidative stress and brain damage in rats. Metab Brain Dis 30:3-793-802.

  • Cosín-Tomàs M, Senserrich J, Arumí-Planas M, Alquézar C, Pallàs M, Martín-Requero Á, Daskalova E, Delchev S, Topolov M, Dimitrova S, Uzunova Y, Valcheva-Kuzmanova S, Kratchanova M, Vladimirova-Kitova L, Denev P (2019). Aroniamelano carpa (Michx.) Elliot fruit juice reveals neuroprotective effect and improves cognitive and locomotor functions of aged rats. J Food Chem Toxicol 132:110674.

  • Crawley J, Goodwin FK (1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13(2):167–170

    CAS  Google Scholar 

  • Dominiak A, Wilkaniec A, Jęśko H, Czapski GA, Lenkiewicz AM, Kurek E, Wroczyński P, Adamczyk A (2017) Selol, an organic selenium donor, prevents lipopolysaccharide-induced oxidative stress and inflammatory reaction in the rat brain. Neurochem Int 108:66–77

    CAS  Google Scholar 

  • Daskalova E, Delchev S, Topolov M, Dimitrova S, Uzunova Y, Valcheva-Kuzmanova S, Kratchanova M, Vladimirova-Kitova L, Denev P (2019). Aronia melanocarpa (Michx.) Elliot fruit juice reveals neuroprotective effect and improves cognitive and locomotor functions of aged rats. J Food ChemToxicol132:110674

  • Demirci K, Nazıroğlu M, Övey İS, Balaban H (2017) Selenium attenuates apoptosis, inflammation and oxidative stress in the blood and brain of aged rats with scopolamine-induced dementia. Metab Brain Dis 32:321–329

    CAS  Google Scholar 

  • Dong F, Wang S, Wang Y, Yang X, Jiang J, Wu D, Qu X, Fan H, Yao R. (2017). Quercetin ameliorates learning and memory via the Nrf2-ARE signalling pathway in d galactose-induced neurotoxicity in mice. J Biochem Biophys Res Commun 491:3-636-641.

  • Du HM, Wang YJ, Liu X, Wang SL, Wu SM, Yuan Z, Zhu XK. (2019). Defective central immune tolerance induced by high-dose D-galactose resembles aging. J Biochem (Mosc) 84:6-:617-626.

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacol 7:88–95

    CAS  Google Scholar 

  • Fernandes J, Saudubray JM, Van den Berghe G, Walter JH (2006). Inborn metabolic diseases: diagnosis and treatment: Springer Science & Business Media.

  • Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. J Methods Enzymol 105:114–121

    CAS  Google Scholar 

  • Franco R, Vargas MR (2018) Redox biology in neurological function, dysfunction, and aging. J Antioxid Redox Signal 28:18-1583-1586.

  • Frazzini V, Rockabrand E, Mocchegiani E, Sensi S (2006) Oxidative stress and brain aging: is zinc the link? J Biogerontol 7:307–314

    CAS  Google Scholar 

  • Haider S, Liaquat L, Ahmad S, Batool Z, Siddiqui RA, Tabassum S, Shahzad S, Rafiq S, Naz N (2020) Naringenin protects AlCl3/D-galactose induced neurotoxicity in rat model of AD via attenuation of acetylcholinesterase levels and inhibition of oxidative stress. PLoS One 15(1):e0227631

    CAS  Google Scholar 

  • Haider S, Tabassum S, Perveen T (2016) Scopolamine-induced greater alterations in neurochemical profile and increased oxidative stress demonstrated a better model of dementia: a comparative study. Brain Res Bull 127:234–247

    CAS  Google Scholar 

  • Haider S, Naqvi F, Batool Z, Tabassum S, Sadir S, Liaquat L, Naqvi F, Zuberi NA, Shakeel H, Perveen T (2015) Pretreatment with curcumin attenuates anxiety while strengthens memory performance after one short stress experience in male rats. Brain Res Bull 115:1–8

    CAS  Google Scholar 

  • Haider S, Khaliq S, Tabassum S, Haleem DJ (2012) Role of Somatodendritic and postsynaptic 5-HT1A receptors on learning and memory functions in rats. Neurochem Res 37:2161–2166

    CAS  Google Scholar 

  • Haider S, Tabassum S, Ali S, Saleem S, Khan AK, Haleem DJ (2011) Age-related decreases in striatal DA produces cognitive deficits in male rats. J Pharm Nutri Sci 1:20–27

    Google Scholar 

  • Handley SL, Mithani S (1984) Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of ‘fear’-motivated behaviour. Naunyn Schmiedebergs Arch Pharmacol 327:1–5

    CAS  Google Scholar 

  • Ho SC, Liu JH, Wu RY (2003). Establishment of the mimetic aging effect in mice caused by D-galactose. J Biogerontol 4:1- 15-18.

  • Huang Z, Rose AH, Hoffmann PR (2012a) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. J Antioxidants Redox Signaling 16:705–743

    CAS  Google Scholar 

  • Huang Z, Rose AH, Hoffmann PR (2012b) The role of selenium in inflammation and immunity: implication in anxiety behaviors. J CNS Neurosci Ther 26:453–464

    Google Scholar 

  • Garabadu D, Singh D (2020) Ocimum basilicum attenuates ethidium bromide-induced cognitive deficits and pre-frontal cortical neuroinflammation, astrogliosis and mitochondrial dysfunction in rats. Metab Brain Dis 35:483–495

    CAS  Google Scholar 

  • Gatineau E, Cluzet S, Krisa S, Papet I, Migne C, Remond D, Dardevet D, Polakof S, Richard T, Mosoni L (2018) Effects of nutritional state, aging and high chronic intake of sucrose on brain protein synthesis in rats: modulation of it by rutin and other micronutrients. Food Funct 9(5):2922–2930

    CAS  Google Scholar 

  • Grimm M, Regner L, Mett J, Stahlmann C, Schorr P, Nelke C, Zaidan S (2016) Tocotrienol affects oxidative stress, cholesterol homeostasis and the amyloidogenic pathway in neuroblastoma cells: consequences for Alzheimer’s disease. J Mol Sci Intl 17:1809

    Google Scholar 

  • Guo YR, Lee HC, Lo YC, Yu SC, Huang SY. (2018). n-3 polyunsaturated fatty acids prevent d-galactose-induced cognitive deficits in prediabetic rats. J Food Funct 9:4-2228-2239.

  • Jadeja RN, Jones MA, Abdelrahman AA, Powell FL, Thounaojam MC, Gutsaeva D, Bartoli M, Martin PM (2020) Inhibiting microRNA-144 potentiates Nrf2-dependent antioxidant signalling in RPE and protects against oxidative stress-induced outer retinal degeneration. J Redox Biol 28:101336

    CAS  Google Scholar 

  • Kaviani E, Rahmani M, Kaeidi A, Shamsizadeh A, Allahtavakoli M, Mozafari N, Fatemi I. (2017). Protective effect of atorvastatin on d-galactose-induced aging model in mice. J Behav Brain Res 15:334-55-60.

  • Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigó R, Gladyshev VN (2003) Characterization of mammalian selenoproteomes. Science 300:1439–1443

    CAS  Google Scholar 

  • Kumar A, Prakash A, Dogra S (2011) Centella asiatica attenuates D-galactose-induced cognitive impairment, oxidative and mitochondrial dysfunction in mice. J Alzheimer’s disease 2011:347569

    Google Scholar 

  • Li Y, Jiang B, Zhang T, Mu W, Liu J (2008) Antioxidant and free radical-scavenging activities of chickpea protein hydrolysate (CPH). Food Chem 106(2):444–450

    CAS  Google Scholar 

  • Liaquat L, Sadir S, Batool Z, Tabassum S, Shahzad S, Afzal A, Haider S (2019) Acute aluminum chloride toxicity revisited: study on DNA damage and histopathological, biochemical and neurochemical alterations in rat brain. Life Sci 217:202–211

    CAS  Google Scholar 

  • Liaquat L, Ahmad S, Sadir S, Batool Z, Khaliq S, Tabassum S, Emad S, Madiha S, Shahzad S, Haider S (2017). Development of AD like symptoms following co-administration of AlCl3 and D-gal in rats: a neurochemical, biochemical and behavioural study. Pak J Pharm Sci 30(2(Suppl.)):647-653

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  Google Scholar 

  • Miyata T, Takizawa S, Van Ypersele de Strihou C (2010) Hypoxia. 1. Intracellular sensors for oxygen and oxidative stress: novel therapeutic targets. Am J Physiol Cell Physiol 300:226–231

    Google Scholar 

  • Mecocci P, Boccardi V, Cecchetti R, Bastiani P, Scamosci M, Ruggiero C, Baroni M (2018) a long journey into aging, brain aging, and Alzheimer’s disease following the oxidative stress tracks. J Alzheimer’s Dis 62:1319–1335

    Google Scholar 

  • Méplan C (2011) Trace elements and ageing, a genomic perspective using selenium as an example. J Trace Elem Medicine Bio 25:S11–S16

    Google Scholar 

  • Mladenov M, Gjorgoski I, Stafilov T, Duridanova D (2006) Effect of vitamin C on lipid hydroperoxides and carbonyl groups content of rat plasma depending on age and acute heat exposure. J Thermal Biol 31:588–593

    CAS  Google Scholar 

  • Mohammadi E, Mehri S, Badie Bostan H, Hosseinzadeh H (2018) Protective effect of crocin against d-galactose-induced aging in mice. Avicenna J Phytomed 8(1):14–23

    Google Scholar 

  • Morris RGM (1981) Spatial localization does not require the presence of local cues. Learn Motiv 12:239–260

    Google Scholar 

  • Nam SM, Seo M, Seo JS, Rhim H, Nahm SS, Cho IH, Chang BJ, Kim HJ, Choi SH, Nah SY (2019) Ascorbic acid mitigates D-galactose-induced brain aging by increasing hippocampal neurogenesis and improving memory function. J Nutrients 11:171–176

    Google Scholar 

  • Naskar S, Islam A, Mazumder UK, Saha P, Haldar PK, Gupta M (2010) In vitro and in vivo antioxidant potential of hydromethanolic extract of Phoenix dactylifera fruits. J Sci Res 2:144–157

    CAS  Google Scholar 

  • Nogueira CW, Rocha JB (2011) Toxicology and pharmacology of selenium: emphasis on synthetic organoselenium compounds. Arch Toxicol 85:1313–1359

    CAS  Google Scholar 

  • Oliveira CES, Gai BM, Godoi B, Zeni G, Nogueira CW (2012). The antidepressant-like action of a simple selenium-containing molecule, methyl phenyl selenide, in mice. Eur J Pharm 690:13- 119-123.

  • Papandreou MA, Tsachaki M, Efthimiopoulos S, Cordopatis P, Lamari FN, Margarity M (2011) Memory enhancing effects of saffron in aged mice are correlated with antioxidant protection. Behav Brain Res 219:197–204

    CAS  Google Scholar 

  • Pari L, Latha M (2001) Protective role of Scorparia dulcis plant extract on brain antioxidant status and lipid peroxidation in STZ diabetic male Wistar rats. BMC Complement Alternat Med 6:16

    Google Scholar 

  • Pérez VI, Buffenstein R, Masamsetti V, Leonard S, Salmon AB, Mele J, Friguet B (2009). Protein stability and resistance to oxidative stress are determinants of longevity in the longest living rodent, the naked mole-rat. Proceedings of the National Academy of Sciences, 106:93059-3064.

  • Porsolt RD (1981). Behavioral despair. In “Antidepressants: neurochemical, behavioral and clinical perspectives,” eds. Enna SJ, Malick JB, Richelson E, Raven Press, New York, pp. 121–139

  • Qu Z, Zhang J, Yang H, Huo L, Gao J, Chen H, Gao W (2016) Protective effect of tetrahydropalmatine against d-galactose induced memory impairment in rat. J Physiol Behav 154:114–125

    CAS  Google Scholar 

  • Samad N, Bilal K, Yasmin F, Khaliq S, Zaman A, Ayaz MM (2020). Effect of lithium chloride on d-galactose induced organs injury: possible antioxidative role. Pak J Pharm Sci 33(4(Supplementary)):1795-1803

  • Samad N, Yasmin F, Manzoor N (2019a). Biomarkers in drug free subjects with depression: correlation with tryptophan. Psychiatry Investig 16:12-948-953

  • Samad N, Imran I, Zulfiqar I, Bilal K. (2019b) Ameliorative effect of lithium chloride against d galactose induced behavioral and memory impairment, oxidative stress and alteration in serotonin function in rats. Pharmacol Rep 71:5-909-916

  • Samad N, Jabeen S, Imran I, Zulfiqar I, Bilal K (2019c) Protective effect of gallic acid against arsenic-induced anxiety-/depression- like behaviors and memory impairment in male rats. Metab Brain Dis 34:1091–1102

    CAS  Google Scholar 

  • Samad N, Saleem A (2018) Administration of Allium cepa L. bulb attenuates stress-produced anxiety and depression and improves memory in male mice. Metab Brain Dis 33:271–281

    CAS  Google Scholar 

  • Samad N, Saleem A, Yasmin F, Shehzad MA (2018) Quercetin protects against stress-induced anxiety- and depression-like behaviour and improves memory in male mice. J Physiol Res 67:795–808

    CAS  Google Scholar 

  • Samad N, Parveen T, Haider S, Haleem DJ (2005) Attenuation of restraint induced behavioral deficits by buspirone and propranolol in rats. J Coll Physicians Surg Pak 15:795–798

    Google Scholar 

  • Samad N, Haleem DJ (2009) Behavioral and neurochemical profile of m-CPP following exposure to single restraint stress in rat. Acta Neurol Belg 109:24–31

    Google Scholar 

  • Sant'Ana AB, Vilela-Costa HH, Vicente MA, Hernandes PM, de Andrade TGCS, Zangrossi H Jr (2019) Role of 5-HT2C receptors of the dorsal hippocampus in the modulation of anxiety- and panic-related defensive responses in rats. J Neuropharmaco l148:311–319

    Google Scholar 

  • Saso L, Firuzi O (2014) Pharmacological applications of antioxidants: lights and shadows. J Current Drug Targets 15:1177–1199

    CAS  Google Scholar 

  • Sumathi T, Shobana C, Thangarajeswari M, Usha R (2015) Protective effect of L-theanine against aluminium induced neurotoxicity in cerebral cortex, hippocampus and cerebellum of rat brain–histopathological, and biochemical approach. Drug Chem Toxicol 38:22–31

    CAS  Google Scholar 

  • Suñol C, Kaliman P, Sanfeliu C (2019) Role of resveratrol and selenium on oxidative stress and expression of antioxidant and anti-aging genes in immortalized lymphocytes from Alzheimer’s disease patients. J Nutrients 11:8–1764

    Google Scholar 

  • Tang KK, Li HQ, Qu KC, Fan RF (2019) Selenium alleviates cadmium-induced inflammation and meat quality degradation via antioxidant and anti-inflammation in chicken breast muscles. J Environ Sci Pollut Res Int 26:23453–23459

    CAS  Google Scholar 

  • Timal S, Hoischen A, Lehle L, Adamowicz M, Huijben K, Sykut-Cegielska J, Körner C (2012) Gene identification in the congenital disorders of glycosylation type I by whole-exome sequencing. J Human Mol Genetics 21(19):4151–4161

    CAS  Google Scholar 

  • Thenmozhi AJ, Raja TR, Janakiraman U, Manivasagam T (2015) Neuroprotective effect of hesperidin on aluminium chloride induced Alzheimer’s disease in Wistar rats. Neurochem Res 40:767–776

    CAS  Google Scholar 

  • Ullah F, Ali T, Ullah N, Kim MO (2015) Caffeine prevents d-galactose-induced cognitive deficits, oxidative stress, neuroinflammation and neurodegeneration in the adult rat brain. J Neurochem Int 90:114–124

    CAS  Google Scholar 

  • Vinceti M, Filippini T, Wise LA (2018) Environmental selenium and human health: an update. J Curr Environ Health Rep 5:464–485

    Google Scholar 

  • Wagner KH, Cameron-Smith D, Wessner B, Franzke B (2016) Biomarkers of aging: from function to molecular biology. Nutrients 8:6–338

    Google Scholar 

  • Wang N, Tan HY, Li S, Xu Y, Guo W, Feng Y (2017) Supplementation of micronutrient selenium in metabolic diseases: its role as an antioxidant. J Oxid Med Cell Longev 2017:7478523

    Google Scholar 

  • Wang ZL, Chen LB, Qiu Z, Chen XB, Liu Y, Li J, Wang L, Wang YP (2018) Ginsenoside Rg1 ameliorates testicular senescence changes in D-gal-induced aging mice via antiinflammatory and antioxidative mechanisms. Mol Med Rep 17:6269–6276

    CAS  Google Scholar 

  • Wu Z, Chen T, Pan D, Zeng X, Guo Y, Zhao G (2021) Resveratrol and organic selenium-rich fermented milk reduces D-galactose-induced cognitive dysfunction in mice. Food Funct 12(3):1318–1326

  • Yan J, Pang Y, Zhuang J, Lin H, Zhang Q, Han L, Ke P, Zhuang J, Huang X (2019) Selenepezil, a selenium-containing compound, exerts neuroprotective effect via modulation of the Keap1-Nrf2-are pathway and attenuates Aβ-induced cognitive impairment in vivo. J ACS Chem Neurosci 10:2903–2914

    CAS  Google Scholar 

  • Zhu LJ, Xu C, Ren J, Chang L, Zhu XH, Sun N, Meng GL, Liu MY, Zhang J, Li YY, Tang YL, Zhou QG (2020) Dentate nNOS accounts for stress-induced 5HT(1A) receptor deficiency: implication in anxiety behaviors. J CNS Neurosci Ther 26:453–464

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Bahauddin Zakariya University, Multan, Pakistan, for their support.

Author information

Authors and Affiliations

Authors

Contributions

NS conceived and design research. FH conducted experiments. II provided laboratory for the conduction of experiments. NS wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Noreen Samad.

Ethics declarations

Ethics approval

Institutional ethical approval (Ref No# Biochem/D/162/2020; Dated: January 2, 2020) was received for the animal experiment from the Department of Biochemistry, Bahauddin Zakariya University, Multan, Pakistan.

Consent to participate

Not applicable

Consent for publication

Not applicable

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Samad, ., Hafeez, F. & Imran, I. D-galactose induced dysfunction in mice hippocampus and the possible antioxidant and neuromodulatory effects of selenium. Environ Sci Pollut Res 29, 5718–5735 (2022). https://doi.org/10.1007/s11356-021-16048-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-16048-x

Keywords

Navigation