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01-04-2022 | Laser | Original Article

Effect of transcranial near-infrared photobiomodulation on cognitive outcomes in D-galactose/AlCl₃ induced brain aging in BALB/c mice

Authors: Leila Hosseini, Narmin Farazi, Marjan Erfani, Javad Mahmoudi, Morteza Akbari, Seyed Hojjat Hosseini, Saeed Sadigh-Eteghad

Published in: Lasers in Medical Science | Issue 3/2022

Abstract

Brain photobiomodulation (PBM) therapy (PBMT) modulates various biological and cognitive processes in senescence rodent models. This study was designed to investigate the effects of transcranial near-infrared (NIR) laser treatment on D-galactose (D-gal)/aluminum chloride (AlCl₃) induced inflammation, synaptic dysfunction, and cognitive impairment in mice. The aged mouse model was induced by subcutaneously injecting D-gal (60 mg/kg/day) followed by intragastrically administering AlCl₃ (200 mg/kg/day) for 2 months. NIR PBM (810 nm laser, 32, 16, and 8 J/cm²) was administered transcranially every other day (3 days/week) for 2 months. Social, contextual, and spatial memories were assessed by social interaction test, passive avoidance test, and Lashley III maze, respectively. Then, tumor necrosis factor-α (TNF-α), interleukin (IL)-6, and synaptic markers including growth-associated protein 43 (GAP-43), post-synaptic density-95 (PSD-95), and synaptophysin (SYN) levels were measured in the hippocampus using western blot method. Behavioral results revealed that NIR PBM at fluencies of 16 and 8 J/cm² could reduce D-gal/AlCl3 impaired social and spatial memories. Treatment with NIR attenuated neuroinflammation through down-regulation of TNF-α and IL-6. Additionally, NIR significantly inhibited the down-regulation of GAP-43 and SYN. The results indicate that transcranial PBM at the fluencies 16 and 8 J/cm² effectively prevents cognitive impairment in mice model of aging by inhibiting the production of the inflammatory cytokines and enhancing synaptic markers.

Mirshafa A, Mohammadi H, Shokrzadeh M, Mohammadi E, Amiri FT, Shaki F (2020) Tropisetron protects against brain aging via attenuating oxidative stress, apoptosis and inflammation: the role of SIRT1 signaling. Life Sci 248:117452. https://doi.org/10.1016/j.lfs.2020.117452CrossRefPubMed

Raj D, Yin Z, Breur M, Doorduin J, Holtman IR, Olah M, Mantingh-Otter IJ, Van Dam D, De Deyn PP, den Dunnen W (2017) Increased white matter inflammation in aging-and Alzheimer’s disease brain. Front Mol Neurosci 10:206. https://doi.org/10.3389/fnmol.2017.00206CrossRefPubMedPubMedCentral

Shan Q, Lu J, Zheng Y, Li J, Zhou Z, Hu B, Zhang Z, Fan S, Mao Z, Wang Y-j (2009) Purple sweet potato color ameliorates cognition deficits and attenuates oxidative damage and inflammation in aging mouse brain induced by D-galactose. J Biomed Biotechnol 2009.https://doi.org/10.1155/2009/564737

Trollor JN, Smith E, Agars E, Kuan SA, Baune BT, Campbell L, Samaras K, Crawford J, Lux O, Kochan NA (2012) The association between systemic inflammation and cognitive performance in the elderly: the Sydney memory and ageing study. Age (Dordr) 34(5):1295–1308. https://doi.org/10.1007/s11357-011-9301-xCrossRef

Zuliani G, Cavalieri M, Galvani M, Passaro A, Munari M, Bosi C, Zurlo A, Fellin R (2008) Markers of endothelial dysfunction in older subjects with late onset Alzheimer’s disease or vascular dementia. J Neurol Sci 272(1–2):164–170. https://doi.org/10.1016/j.jns.2008.05.020CrossRefPubMed

Tromp D, Dufour A, Lithfous S, Pebayle T, Després O (2015) Episodic memory in normal aging and Alzheimer disease: insights from imaging and behavioral studies. Ageing Res Rev 24:232–262. https://doi.org/10.1016/j.arr.2015.08.006CrossRefPubMed

Joseph J, Shukitt-Hale B, Casadesus G, Fisher D (2005) Oxidative stress and inflammation in brain aging: nutritional considerations. Neurochem Res 30(6–7):927–935. https://doi.org/10.1007/s11064-005-6967-4CrossRefPubMed

Mu X, Zhang Y, Li J, Xia J, Chen X, Jing P, Song X, Wang L, Wang Y (2017) Angelica sinensis polysaccharide prevents hematopoietic stem cells senescence in D-galactose-induced aging mouse model. Stem Cells Int 2017.https://doi.org/10.1155/2017/3508907

Sadigh-Eteghad S, Majdi A, McCann SK, Mahmoudi J, Vafaee MS, Macleod MR (2017) D-galactose-induced brain ageing model: a systematic review and meta-analysis on cognitive outcomes and oxidative stress indices. PloS one 12(8):e0184122CrossRef

10.

Lu J, Dm Wu, Zheng Yl HuB, Zf Z (2010) Purple sweet potato color alleviates d-galactose-induced brain aging in old mice by promoting survival of neurons via PI3K pathway and inhibiting cytochrome c-mediated apoptosis. Brain Pathol 20(3):598–612. https://doi.org/10.1111/j.1750-3639.2009.00339.xCrossRefPubMed

11.

Nam SM, Choi JH, Yoo DY, Kim W, Jung HY, Kim JW, Kang S-Y, Park J, Kim D-W, Kim WJ (2013) Valeriana officinalis extract and its main component, valerenic acid, ameliorate D-galactose-induced reductions in memory, cell proliferation, and neuroblast differentiation by reducing corticosterone levels and lipid peroxidation. Exp Gerontol 48(11):1369–1377. https://doi.org/10.1016/j.exger.2013.09.002CrossRefPubMed

12.

Rehman SU, Shah SA, Ali T, Chung JI, Kim MO (2017) Anthocyanins reversed D-galactose-induced oxidative stress and neuroinflammation mediated cognitive impairment in adult rats. Mol Neurobiol 54(1):255–271. https://doi.org/10.1007/s12035-015-9604-5CrossRefPubMed

13.

Cui X, Zuo P, Zhang Q, Li X, Hu Y, Long J, Packer L, Liu J (2006) Chronic systemic D-galactose exposure induces memory loss, neurodegeneration, and oxidative damage in mice: Protective effects of R-α-lipoic acid. J Neurosci Res 83(8):1584–1590. https://doi.org/10.1002/jnr.20899CrossRefPubMed

14.

Pogue AI, Jones BM, Bhattacharjee S, Percy ME, Zhao Y, Lukiw WJ (2012) Metal-sulfate induced generation of ROS in human brain cells: detection using an isomeric mixture of 5-and 6-carboxy-2′, 7′-dichlorofluorescein diacetate (carboxy-DCFDA) as a cell permeant tracer. Int J Mol Sci 13(8):9615–9626. https://doi.org/10.3390/ijms13089615CrossRefPubMedPubMedCentral

15.

Yu Z, Li Z, Liu N, Jizhang Y, McCarthy TJ, Tedford CE, Lo EH, Wang X (2015) Near infrared radiation protects against oxygen-glucose deprivation-induced neurotoxicity by down-regulating neuronal nitric oxide synthase (nNOS) activity in vitro. Metab Brain Dis 30(3):829–837. https://doi.org/10.1007/s11011-015-9663-3CrossRefPubMed

16.

Gonzalez-Lima F, Barksdale BR, Rojas JC (2014) Mitochondrial respiration as a target for neuroprotection and cognitive enhancement. Biochem Pharmacol 88(4):584–593. https://doi.org/10.1016/j.bcp.2013.11.010CrossRefPubMed

17.

Zhang Q, Zhou C, Hamblin MR, Wu MX (2014) Low-level laser therapy effectively prevents secondary brain injury induced by immediate early responsive gene X-1 deficiency. J Cereb Blood Flow Metab 34(8):1391–1401. https://doi.org/10.1038/jcbfm.2014.95CrossRefPubMedPubMedCentral

18.

Huang YY, Nagata K, Tedford CE, McCarthy T, Hamblin MR (2013) Low-level laser therapy (LLLT) reduces oxidative stress in primary cortical neurons in vitro. J Biophotonics 6(10):829–838. https://doi.org/10.1002/jbio.201200157CrossRefPubMed

19.

Uozumi Y, Nawashiro H, Sato S, Kawauchi S, Shima K, Kikuchi M (2010) Targeted increase in cerebral blood flow by transcranial near-infrared laser irradiation. Lasers Surg Med 42(6):566–576. https://doi.org/10.1002/lsm.20938CrossRefPubMed

20.

Purushothuman S, Johnstone DM, Nandasena C, Mitrofanis J, Stone J (2014) Photobiomodulation with near infrared light mitigates Alzheimer’s disease-related pathology in cerebral cortex–evidence from two transgenic mouse models. Alzheimers Res Ther 6(1):2. https://doi.org/10.1186/alzrt232CrossRefPubMedPubMedCentral

21.

Schiffer F, Johnston AL, Ravichandran C, Polcari A, Teicher MH, Webb RH, Hamblin MR (2009) Psychological benefits 2 and 4 weeks after a single treatment with near infrared light to the forehead: a pilot study of 10 patients with major depression and anxiety. Behav Brain Funct 5(1):1–13. https://doi.org/10.1186/1744-9081-5-46CrossRef

22.

Wu Q, Xuan W, Ando T, Xu T, Huang L, Huang YY, Dai T, Dhital S, Sharma SK, Whalen MJ (2012) Low-level laser therapy for closed-head traumatic brain injury in mice: effect of different wavelengths. Lasers Surg Med 44(3):218–226. https://doi.org/10.1002/lsm.22003CrossRefPubMedPubMedCentral

23.

Salehpour F, Ahmadian N, Rasta SH, Farhoudi M, Karimi P, Sadigh-Eteghad S (2017) Transcranial low-level laser therapy improves brain mitochondrial function and cognitive impairment in D-galactose–induced aging mice. Neurobiol Aging 58:140–150. https://doi.org/10.1016/j.neurobiolaging.2017.06.025CrossRefPubMed

24.

Blanco NJ, Saucedo CL, Gonzalez-Lima F (2017) Transcranial infrared laser stimulation improves rule-based, but not information-integration, category learning in humans. Neurobiol Learn Mem 139:69–75. https://doi.org/10.1016/j.nlm.2016.12.016CrossRefPubMed

25.

Hwang J, Castelli DM, Gonzalez-Lima F (2016) Cognitive enhancement by transcranial laser stimulation and acute aerobic exercise. Lasers Med Sci 31(6):1151–1160. https://doi.org/10.1007/s10103-016-1962-3CrossRefPubMed

26.

Blanco NJ, Maddox WT, Gonzalez-Lima F (2017) Improving executive function using transcranial infrared laser stimulation. J Neuropsychol 11(1):14–25. https://doi.org/10.1111/jnp.12074CrossRefPubMed

27.

Chan AS, Lee TL, Yeung MK, Hamblin MR (2019) Photobiomodulation improves the frontal cognitive function of older adults. Int J Geriatr Psychiatry 34(2):369–377. https://doi.org/10.1002/gps.5039CrossRefPubMed

28.

Saltmarche AE, Naeser MA, Ho KF, Hamblin MR, Lim L (2017) Significant improvement in cognition in mild to moderately severe dementia cases treated with transcranial plus intranasal photobiomodulation: case series report. Photomed Laser Surg 35(8):432–441. https://doi.org/10.1089/pho.2016.4227CrossRefPubMedPubMedCentral

29.

Barrett DW, Gonzalez-Lima F (2013) Transcranial infrared laser stimulation produces beneficial cognitive and emotional effects in humans. Neuroscience 230:13–23. https://doi.org/10.1016/j.neuroscience.2012.11.016CrossRefPubMed

30.

Zhang Y, Pi Z, Song F, Liu Z (2016) Ginsenosides attenuate d-galactose-and AlCl3-inducedspatial memory impairment by restoring the dysfunction of the neurotransmitter systems in the rat model of Alzheimer’s disease. J Ethnopharmacol 194:188–195. https://doi.org/10.1016/j.jep.2016.09.007CrossRefPubMed

31.

Cutuli D, Pagani M, Caporali P, Galbusera A, Laricchiuta D, Foti F, Neri C, Spalletta G, Caltagirone C, Petrosini L (2016) Effects of omega-3 fatty acid supplementation on cognitive functions and neural substrates: a voxel-based morphometry study in aged mice. Front Aging Neurosci 8:38. https://doi.org/10.3389/fnagi.2016.00038CrossRefPubMedPubMedCentral

32.

Salehpour F, Farajdokht F, Mahmoudi J, Erfani M, Farhoudi M, Karimi P, Rasta SH, Sadigh-Eteghad S, Hamblin MR, Gjedde A (2019) Photobiomodulation and coenzyme Q10 treatments attenuate cognitive impairment associated with model of transient global brain ischemia in artificially aged mice. Front Cell Neurosci 13:74. https://doi.org/10.3389/fncel.2019.00074CrossRefPubMedPubMedCentral

33.

Micale V, Cristino L, Tamburella A, Petrosino S, Leggio GM, Di Marzo V, Drago F (2010) Enhanced cognitive performance of dopamine D3 receptor “knock-out” mice in the step-through passive-avoidance test: assessing the role of the endocannabinoid/endovanilloid systems. Pharmacol Res 61(6):531–536. https://doi.org/10.1016/j.phrs.2010.02.003CrossRefPubMed

34.

Kramer AF, Cassavaugh N, Horrey WJ, Becic E, Mayhugh JL (2007) Influence of age and proximity warning devices on collision avoidance in simulated driving. Hum Factors 49(5):935–949. https://doi.org/10.1518/001872007X230271CrossRefPubMed

35.

Mueller S, Stables L, Du A, Schuff N, Truran D, Cashdollar N, Weiner M (2007) Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4 T. Neurobiol Aging 28(5):719–726. https://doi.org/10.1016/j.neurobiolaging.2006.03.007CrossRefPubMed

36.

Wei Y, Liu D, Zheng Y, Li H, Hao C, Ouyang W (2017) Protective effects of kinetin against aluminum chloride and D-galactose induced cognitive impairment and oxidative damage in mouse. Brain Res Bull 134:262–272. https://doi.org/10.1016/j.brainresbull.2017.08.014CrossRefPubMed

37.

Li H, Kang T, Qi B, Kong L, Jiao Y, Cao Y, Zhang J, Yang J (2016) Neuroprotective effects of ginseng protein on PI3K/Akt signaling pathway in the hippocampus of D-galactose/AlCl3 inducing rats model of Alzheimer’s disease. J Ethnopharmacol 179:162–169. https://doi.org/10.1016/j.jep.2015.12.020CrossRefPubMed

38.

Chiroma SM, Baharuldin MTH, Taib CNM, Amom Z, Jagadeesan S, Adenan MI, Moklas MAM (2019) Protective effect of Centella asiatica against D-galactose and aluminium chloride induced rats: behavioral and ultrastructural approaches. Biomed Pharmacother 109:853–864. https://doi.org/10.1016/j.biopha.2018.10.111CrossRefPubMed

39.

Gocmez SS, Gacar N, Utkan T, Gacar G, Scarpace PJ, Tumer N (2016) Protective effects of resveratrol on aging-induced cognitive impairment in rats. Neurobiol Learn Mem 131:131–136. https://doi.org/10.1016/j.nlm.2016.03.022CrossRefPubMed

40.

De Taboada L, Yu J, El-Amouri S, Gattoni-Celli S, Richieri S, McCarthy T, Streeter J, Kindy MS (2011) Transcranial laser therapy attenuates amyloid-β peptide neuropathology in amyloid-β protein precursor transgenic mice. J Alzheimers Dis 23(3):521–535. https://doi.org/10.3233/JAD-2010-100894CrossRefPubMed

41.

Chao LL (2019) Effects of home photobiomodulation treatments on cognitive and behavioral function, cerebral perfusion, and resting-state functional connectivity in patients with dementia: a pilot trial. Photobiomodul Photomed Laser Surg 37(3):133–141. https://doi.org/10.1089/photob.2018.4555CrossRefPubMed

42.

Felix-Ortiz AC, Tye KM (2014) Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci 34(2):586–595. https://doi.org/10.1523/JNEUROSCI.4257-13.2014CrossRefPubMedPubMedCentral

43.

Riedel G, Kang S, Choi D, Platt B (2009) Scopolamine-induced deficits in social memory in mice: reversal by donepezil. Behav Brain Res 204(1):217–225. https://doi.org/10.1016/j.bbr.2009.06.012CrossRefPubMed

44.

Shoji H, Miyakawa T (2019) Age-related behavioral changes from young to old age in male mice of a C57 BL/6J strain maintained under a genetic stability program. Neuropsychopharmacol Rep 39(2):100–118. https://doi.org/10.1002/npr2.12052CrossRefPubMedPubMedCentral

45.

Smith BM, Yao X, Chen KS, Kirby ED (2018) A larger social network enhances novel object location memory and reduces hippocampal microgliosis in aged mice. Front Aging Neurosci 10:142. https://doi.org/10.3389/fnagi.2018.00142CrossRefPubMedPubMedCentral

46.

Dimopoulos N, Piperi C, Salonicioti A, Mitropoulos P, Kallai E, Liappas I, Lea RW, Kalofoutis A (2006) Indices of low-grade chronic inflammation correlate with early cognitive deterioration in an elderly Greek population. Neurosci Lett 398(1–2):118–123. https://doi.org/10.1016/j.neulet.2005.12.064CrossRefPubMed

47.

Belarbi K, Jopson T, Tweedie D, Arellano C, Luo W, Greig NH, Rosi S (2012) TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflammation 9(1):23. https://doi.org/10.1186/1742-2094-9-23CrossRefPubMedPubMedCentral

48.

Yamaura M, Yao M, Yaroslavsky I, Cohen R, Smotrich M, Kochevar IE (2009) Low level light effects on inflammatory cytokine production by rheumatoid arthritis synoviocytes. Lasers Surg Med 41(4):282–290. https://doi.org/10.1002/lsm.20766CrossRefPubMed

49.

Khuman J, Zhang J, Park J, Carroll JD, Donahue C, Whalen MJ (2012) Low-level laser light therapy improves cognitive deficits and inhibits microglial activation after controlled cortical impact in mice. J Neurotrauma 29(2):408–417. https://doi.org/10.1089/neu.2010.1745CrossRefPubMedPubMedCentral

50.

Salehpour F, Farajdokht F, Erfani M, Sadigh-Eteghad S, Shotorbani SS, Hamblin MR, Karimi P, Rasta SH, Mahmoudi J (2018) Transcranial near-infrared photobiomodulation attenuates memory impairment and hippocampal oxidative stress in sleep-deprived mice. Brain Res 1682:36–43. https://doi.org/10.1016/j.brainres.2017.12.040CrossRefPubMedPubMedCentral

51.

Salehpour F, Farajdokht F, Cassano P, Sadigh-Eteghad S, Erfani M, Hamblin MR, Salimi MM, Karimi P, Rasta SH, Mahmoudi J (2019) Near-infrared photobiomodulation combined with coenzyme Q10 for depression in a mouse model of restraint stress: reduction in oxidative stress, neuroinflammation, and apoptosis. Brain Res Bull 144:213–222. https://doi.org/10.1016/j.brainresbull.2018.10.010CrossRefPubMed

52.

Lee HI, Park JH, Park MY, Kim NG, Park K-J, Choi BT, Shin Y-I, Shin HK (2016) Pre-conditioning with transcranial low-level light therapy reduces neuroinflammation and protects blood-brain barrier after focal cerebral ischemia in mice. Restor Neurol Neurosci 34(2):201–214. https://doi.org/10.3233/RNN-150559CrossRefPubMed

53.

Eshaghi E, Sadigh-Eteghad S, Mohaddes G, Rasta SH (2019) Transcranial photobiomodulation prevents anxiety and depression via changing serotonin and nitric oxide levels in brain of depression model mice: a study of three different doses of 810 nm laser. Lasers Surg Med 51(7):634–642CrossRef

54.

Robinson JL, Molina-Porcel L, Corrada MM, Raible K, Lee EB, Lee VM-Y, Kawas CH, Trojanowski JQ (2014) Perforant path synaptic loss correlates with cognitive impairment and Alzheimer’s disease in the oldest-old. Brain 137(9):2578–2587. https://doi.org/10.1093/brain/awu190CrossRefPubMedPubMedCentral

55.

Yao W-D, Gainetdinov RR, Arbuckle MI, Sotnikova TD, Cyr M, Beaulieu J-M, Torres GE, Grant SG, Caron MG (2004) Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 41(4):625–638. https://doi.org/10.1016/s0896-6273(04)00048-0CrossRefPubMed

56.

Carlisle HJ, Fink AE, Grant SG, O’Dell TJ (2008) Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. J Physiol 586(24):5885–5900. https://doi.org/10.1113/jphysiol.2008.163469CrossRefPubMedPubMedCentral

57.

Schmitt U, Tanimoto N, Seeliger M, Schaeffel F, Leube R (2009) Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162(2):234–243. https://doi.org/10.1016/j.neuroscience.2009.04.046CrossRefPubMed

58.

Lambert TJ, Fernandez SM, Frick KM (2005) Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice. Neurobiol Learn Mem 83(3):206–216. https://doi.org/10.1016/j.nlm.2004.12.001CrossRefPubMed

59.

Shen X, Sun Y, Wang M, Shu H, Zhu L-J, Yan P-Y, Zhang J-F, Jin X (2018) Chronic N-acetylcysteine treatment alleviates acute lipopolysaccharide-induced working memory deficit through upregulating caveolin-1 and synaptophysin in mice. Psychopharmacology 235(1):179–191. https://doi.org/10.1007/s00213-017-4762-yCrossRefPubMed

60.

Holahan MR (2017) A shift from a pivotal to supporting role for the growth-associated protein (GAP-43) in the coordination of axonal structural and functional plasticity. Front Cell Neurosci 11:266. https://doi.org/10.3389/fncel.2017.00266CrossRefPubMedPubMedCentral

61.

Nemes AD, Ayasoufi K, Ying Z, Zhou Q-G, Suh H, Najm IM (2017) Growth associated protein 43 (GAP-43) as a novel target for the diagnosis, treatment and prevention of Epileptogenesis. Sci Rep 7(1):1–13. https://doi.org/10.1038/s41598-017-17377-zCrossRef

62.

Zhang Y, Wu J, Feng X, Wang R, Chen A, Shao L (2017) Current understanding of the toxicological risk posed to the fetus following maternal exposure to nanoparticles. Expert Opin Drug Metab Toxicol 13(12):1251–1263. https://doi.org/10.1080/17425255.2018.1397131CrossRefPubMed

63.

Li Z, Wang Y, Xie Y, Yang Z, Zhang T (2011) Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia. Neurochem Res 36(10):1840–1849. https://doi.org/10.1007/s11064-011-0502-6CrossRefPubMed

64.

Xu L, Long J, Su Z, Xu B, Lin M, Chen Y, Long D (2019) Restored presynaptic synaptophysin and cholinergic inputs contribute to the protective effects of physical running on spatial memory in aged mice. Neurobiol Dis 132:104586. https://doi.org/10.1016/j.nbd.2019.104586CrossRefPubMed

65.

Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y (2004) Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci 24(35):7648–7653. https://doi.org/10.1523/JNEUROSCI.1725-04.2004CrossRefPubMedPubMedCentral

66.

Rogers JT, Liu C-C, Zhao N, Wang J, Putzke T, Yang L, Shinohara M, Fryer JD, Kanekiyo T, Bu G (2017) Subacute ibuprofen treatment rescues the synaptic and cognitive deficits in advanced-aged mice. Neurobiol Aging 53:112–121. https://doi.org/10.1016/j.neurobiolaging.2017.02.001CrossRefPubMedPubMedCentral

67.

Shen C, Sun F-l, Zhang R-y, Zhang L, Li Y-l, Zhang L, Li L (2015) Tetrahydroxystilbene glucoside ameliorates memory and movement functions, protects synapses and inhibits α-synuclein aggregation in hippocampus and striatum in aged mice. Restor Neurol Neurosci 33(4):531–541. https://doi.org/10.3233/RNN-150514CrossRefPubMed

68.

Hamblin MR (2016) Shining light on the head: photobiomodulation for brain disorders. BBA Clin 6:113–124. https://doi.org/10.1016/j.bbacli.2016.09.002CrossRefPubMedPubMedCentral

69.

Salehpour F, Mahmoudi J, Kamari F, Sadigh-Eteghad S, Rasta SH, Hamblin MR (2018) Brain photobiomodulation therapy: a narrative review. Mol Neurobiol 55(8):6601–6636. https://doi.org/10.1007/s12035-017-0852-4CrossRefPubMedPubMedCentral

Title: Effect of transcranial near-infrared photobiomodulation on cognitive outcomes in D-galactose/AlCl3 induced brain aging in BALB/c mice
Authors: Leila Hosseini
Narmin Farazi
Marjan Erfani
Javad Mahmoudi
Morteza Akbari
Seyed Hojjat Hosseini
Saeed Sadigh-Eteghad
Publication date: 01-04-2022
Publisher: Springer London
Keyword: Laser
Published in: Lasers in Medical Science / Issue 3/2022
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-021-03433-8

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Effect of transcranial near-infrared photobiomodulation on cognitive outcomes in D-galactose/AlCl₃ induced brain aging in BALB/c mice

Abstract

At a glance: The ONWARDS insulin icodec trials

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Abstract

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