The DOI matches its Crossref record; 51 of the 53 references it cites were found in a registry or an index.
Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: Behavioral and electrophysiological proofs for microbiome–gut–brain axis
Abstract
Diabetes mellitus-induced metabolic disturbances underlie the action of many systems including some higher functions of the brain such as learning and memory. Plenty of evidence supports the effects of probiotics on the function of many systems including the nervous system. Here we report the effect of probiotics treatment on the behavioral and electrophysiological aspects of learning and memory disorders. Diabetic rats were made through intraperitoneal injection of streptozocin. The control and diabetic rats were fed with either normal regimen (control rats recieving normal regimen (CO) and diabetics rats receiving normal regimen (DC), respectively) or normal regimen plus probiotic supplementation for 2months (control rats receiving probiotic supplementation (CP) and diabetics rats recieving probiotic supplementation (DP), respectively). The animals were first introduced to spatial learning task in the Morris water maze. Then, in electrophysiological experiments, stimulating the Schaffer collaterals the basic and potentiated excitatory postsynaptic potential (EPSPs) were recorded in the CA1 area of the hippocampus. Finally, the serum levels of glucose, insulin, superoxide dismutase and 8-hydroxy-2'-deoxyguanosine (8-OHdG) were measured. We found that probiotics administration considerably improved the impaired spatial memory in the diabetic animals. The probiotics supplementation in the diabetic rats recovered the declined basic synaptic transmission and further restored the hippocampal long-term potentiation (LTP). While the probiotics administration enhanced the activation of superoxide dismutase and increased the insulin level of serum it decreased both the glucose level of serum and the 8-OHdG factor. From the present results we concluded that probiotics efficiently reverse deteriorated brain functions in the levels of cognitive performances and their proposed synaptic mechanisms in diabetes mellitus. These considerations imply on the necessity of an optimal function of the microbiome-gut-brain axis in the behavioral as well as electrophysiological aspects of brain action.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“For example, probiotic supplementation with a mixture of Lactobacillus and Bifidobacterium strains considerably improved spatial memory deficits in diabetic animals (Davari et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Davari et al., 2013
In the citing paper
“In a seminal in vivo, hippocampal electrophysiology experiment neurophysiological and behavioral impairments in a diabetic rat model of diabetes mellitus were rescued with the probiotic treatment of L. acidophilus, B. lactis and L. fermentum (Davari et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Davari et al., 2013
In the citing paper
“Animal studies suggest that probiotics can modulate endogenous neuroactive molecules [17], prevent and treat neuronal autoimmune diseases [18], and ameliorate impaired spatial memory in diabetic rats [19].”
From Effect of Supplementation with Probiotics in Patients with Schizophrenia: Systematic Review and Meta-Analysis of Randomized Controlled Clinical Trials (2025) · cites this paper as [19]
In the citing paper
“In addition, animal studies imply on the necessity of an optimal function of what is known as the microbiome-gut-brain axis in the behavioral as well as electrophysiological aspects of brain action (Davari et al., 2013).”
From Effect of Probiotic Supplementation on Cognitive Function and Metabolic Status in Alzheimer's Disease: A Randomized, Double-Blind and Controlled Trial (2016) · cites this paper as Davari et al., 2013
In the citing paper
“However, data on the effects of probiotics on improving cognitive disorders are scarce (Bhattacharjee and Lukiw, 2013; Davari et al., 2013).”
From Effect of Probiotic Supplementation on Cognitive Function and Metabolic Status in Alzheimer's Disease: A Randomized, Double-Blind and Controlled Trial (2016) · cites this paper as Davari et al., 2013
In the citing paper
“In our previous work, we have shown that probiotics efficiently reverse the impaired spatial learning and memory as well as synaptic transmission in diabetes mellitus (Davari et al., 2013).”
From Effect of Probiotic Supplementation on Cognitive Function and Metabolic Status in Alzheimer's Disease: A Randomized, Double-Blind and Controlled Trial (2016) · cites this paper as Davari et al., 2013
Citations
Cites
Biochemistry and molecular cell biology of diabetic complications
Brownlee, M. (2001) · Nature · doi:10.1038/414813a · Cited by 9,107
Oxidative stress: oxidants and antioxidants
Sies, H. (1997) · Experimental Physiology · doi:10.1113/expphysiol.1997.sp004024 · Cited by 4,577
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888
Diabetes, oxidative stress, and antioxidants: A review
Maritim, A. C., Sanders, R. A., & Watkins, J. B. (2003) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.10058 · Cited by 3,167
Role of oxidative stress in diabetic complications: a new perspective on an old paradigm.
Baynes, J. W., & Thorpe, S. R. (1999) · Diabetes · doi:10.2337/diabetes.48.1.1 · Cited by 2,441
Evans, J. L., Goldfine, I. D., Maddux, B. A., & Grodsky, G. M. (2003) · Diabetes · doi:10.2337/diabetes.52.1.1 · Cited by 1,482
Tiedge, M., Lortz, S., Drinkgern, J., & Lenzen, S. (1997) · Diabetes · doi:10.2337/diab.46.11.1733 · Cited by 1,211
NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD).
Luscher, C., & Malenka, R. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005710 · Cited by 1,110 · cited 1×
“Long-term potentiation (LTP) and long-term depression (LTD) are activity-dependent changes in synaptic efficacy which have been considered for cellular mechanisms of learning and memory (Luscher and Malenka, 2012).”
BackgroundSingle cocaine exposure in vivo induces long-term potentiation in dopamine neurons
Ungless, M. A., Whistler, J. L., Malenka, R. C., & Bonci, A. (2001) · Nature · doi:10.1038/35079077 · Cited by 1,106
The microbiome-gut-brain axis: from bowel to behavior
Cryan, J. F., & O’Mahony, S. M. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01664.x · Cited by 990
Cited by
Sorted by citations
Items 101–200 of 296
Stanaway, I. B., Wallace, J. C., Shojaie, A., Griffith, W. C., Hong, S., Wilder, C. S., Green, F. H., Tsai, J. M., Knight, M., Workman, T. W., et al. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.02149-16 · Cited by 48
Cerdó, T., Diéguez, E., & Campoy, C. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00188.2019 · Cited by 48
Microbial memories: Sex‐dependent impact of the gut microbiome on hippocampal plasticity
Darch, H. T., Collins, M., O’Riordan, K. J., & Cryan, J. F. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15119 · Cited by 51
Wang, H., He, S., Xin, J., Zhang, T., Sun, N., Li, L., Ni, X., Zeng, D., Ma, H., & Bai, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.662148 · Cited by 47
“Many probiotics have psychobiotic potential of restoring or preventing hippocampal-dependent memory deficits in rodents induced by many different factors such as aging (Jeong et al., 2015) and diabetes (Davari et al., 2013).”
BackgroundHadizadeh, M., Hamidi, G. A., & Salami, M. (2019) · PubMed Central · doi:10.22038/ijbms.2019.33956.8078 · Cited by 48
“The present results are consistent to reports indicating favorable effect of probiotics on the cognitive trends (37, 56).”
ResultSelf-citationGlinert, A., Turjeman, S., Elliott, E., & Koren, O. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12812 · Cited by 48
“Govindarajulu et al. (2020) set out to determine the potential effects on LTP induction by the microbiome-dependent metabolite trimethylamine N-oxide (TMAO).”
BackgroundInfluentialParois, S. P., Calandreau, L., Kraïmi, N., Gabriel, I., & Leterrier, C. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.022 · Cited by 45
Tyagi, P., Tasleem, M., Prakash, S., & Chouhan, G. (2020) · Food Research International · doi:10.1016/j.foodres.2020.109489 · Cited by 42
The gut microbiota‐astrocyte axis: Implications for type 2 diabetic cognitive dysfunction
Li, Z.-H., Jiang, Y., Long, C., Peng, Q., & Yue, R. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14077 · Cited by 41
Infant Gut Microbiota Associated with Fine Motor Skills
Acuña, I., Cerdó, T., Ruiz-Rodriguez, A., Torres-Espínola, F. J., López‐Moreno, A., Aguilera, J., Suárez, A., & Campoy, C. (2021) · Nutrients · doi:10.3390/nu13051673 · Cited by 41
“fermentum improved diabetes-induced impairment of synaptic activity and cognitive function in rats [46].”
BackgroundShabbir, M. A., Mehak, F., Khan, Z. M., Ahmed, W., Haq, S. M. A. U., Khan, M. R., Bhat, Z. F., & Aadil, R. M. (2022) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2021.12.035 · Cited by 47
Gut microbiota composition of Japanese macaques associates with extent of human encroachment
Lee, W., Hayakawa, T., Kiyono, M., Yamabata, N., & Hanya, G. (2019) · American Journal of Primatology · doi:10.1002/ajp.23072 · Cited by 41
Foster, J. A. (2016) · International review of neurobiology · doi:10.1016/bs.irn.2016.07.005 · Cited by 41
“However, it should be noted that while the probiotic treatment did reduce serum glucose levels compared to nonprobiotic diabetic rat group, these levels remained significantly higher than control rats (Davari et al., 2013).”
BackgroundInfluentialPsychobiotic Effects of Multi-Strain Probiotics Originated from Thai Fermented Foods in a Rat Model
Luang‐In, V., Katisart, T., Konsue, A., Nudmamud‐Thanoi, S., Narbad, A., Saengha, W., Wangkahart, E., Pumriw, S., Samappito, W., & Ling, N. (2020) · Food Science of Animal Resources · doi:10.5851/kosfa.2020.e72 · Cited by 47
Xiao, J., Li, S., Sui, Y., Wu, Q., Li, X., Xie, B., Zhang, M., & Sun, Z. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112773 · Cited by 39
Gut Microbiota and Parkinson’s Disease: Implications for Faecal Microbiota Transplantation Therapy
Kang, Y., Kang, X., Zhang, H., Liu, Q., Yang, H., & Fan, W. (2021) · ASN NEURO · doi:10.1177/17590914211016217 · Cited by 38
Fülling, C., Lach, G., Bastiaanssen, T. F. S., Fouhy, F., O'Donovan, A. N., Ventura-Silva, A.-P., Stanton, C., Dinan, T. G., & Cryan, J. F. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.02.013 · Cited by 36
Lactic Acid Bacteria in Health and Disease
Xiao, J., Zhang, Y., & Yang, Z. (2014) · Springer eBooks · doi:10.1007/978-94-017-8841-0_5 · Cited by 38
Neurological and Cognitive Significance of Probiotics: A Holy Grail Deciding Individual Personality
Afzal, M., Mazhar, S. F., Sana, S., Naeem, M. A., Rasool, M. H., Saqalein, M., Nisar, M. A., Rasool, M., Bilal, M., Khan, A. A., et al. (2020) · Future Microbiology · doi:10.2217/fmb-2019-0143 · Cited by 34
Zacharias, H. U., Kaleta, C., Cossais, F., Schaeffer, E., Berndt, H., Best, L., Dost, T., Glüsing, S., Groussin, M., Poyet, M., et al. (2022) · Metabolites · doi:10.3390/metabo12121222 · Cited by 38
“Concerning probiotics, various animal and few human studies have shown behavioral and neuropsychiatric effects including effects on cognitive function or fatigue [183,184].”
BackgroundBacillus licheniformis prevents and reduces anxiety-like and depression-like behaviours
Feng, S., Chen, M., Liu, Y., Yi, Y., Liang, A., Zhang, Y., & Hao, Z. (2023) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-023-12580-7 · Cited by 36
ÇİLTAŞ, A. Ç., Toy, C. E., Güneş, H., & Yaprak, M. (2023) · Epilepsy Research · doi:10.1016/j.eplepsyres.2023.107190 · Cited by 36
Tao, D., Zhong, T., Pang, W., & li, X. (2021) · BMC Neuroscience · doi:10.1186/s12868-021-00679-4 · Cited by 33
“The beneficial effects of probiotic consumption on behaviour and brain function are now becoming increasingly appreciated in a variety of inflammatory diseases [66, 67].”
BackgroundZolfaghari, S. I., Khorasgani, M. R., & Noorbakhshnia, M. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113224 · Cited by 32
Sałat, K., Gdula‐Argasińska, J., Malikowska‐Racia, N., Podkowa, A., Lipkowska, A., & Librowski, T. (2016) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-016-1230-x · Cited by 30
“…shown that not only the intracerebral application of STZ leads to memory deficits (Blokland and Jolles 1993; Chen et al. 2013), but the intraperitoneal (ip) administration of this drug can also induce memory impairments (Cai et al. 2011; Davari et al. 2013; Miao et al. 2015; Takizawa et al. 2013).”
BackgroundThinking outside the brain for cognitive improvement: Is peripheral immunomodulation on the way?
Zheng, X., Zhang, X., An, K., Ran, C., Wang, G., & Hao, H. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.06.020 · Cited by 29
“…benefits (e.g., Lactobacillus rhamnosus, Bacteroides fragilis), has shown beneficial effects on cognitive impairment associated with diabetes (Davari et al., 2013), behavioral abnormalities in autism spectrum disorder (Hsiao et al., 2013) and stress-induced depression and anxiety in animal…”
Krishna, G., Divyashri, G., Prapulla, S. G., & ., M. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1687-x · Cited by 29
“These results are consistent with previous reports showing that Bifidobacterium probiotic can augment antioxidant function [61, 62].”
ResultKarbownik, M. S., Mokros, Ł., Dobielska, M., Kowalczyk, M., & Kowalczyk, E. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.850249 · Cited by 33
Bridging the gap: associations between gut microbiota and psychiatric disorders
Ahmed, G. K., Ramadan, H. K., Elbeh, K., & Haridy, N. A. (2024) · Middle East Current Psychiatry · doi:10.1186/s43045-024-00395-9 · Cited by 33
Probiotic actions on diseases: implications for therapeutic treatments
Chiu, Y., Lin, S.-L., Tsai, J., & Lin, M. (2014) · Food & Function · doi:10.1039/c3fo60600g · Cited by 28
Soda, T., Pasqua, T., Sarro, G. D., & Moccia, F. D. (2024) · Biomedicines · doi:10.3390/biomedicines12102387 · Cited by 28
“…l-3-n -Butylphthalide (NBP) [184], the isoquinoline alkaloid berberine [185], the phenolic compound vanillic acid [186], probiotics treatment [187], inhibition of the receptor for advanced glycation end products (RAGE) with the specific blocker FPS-ZM1 [188], physical exercise [189], and…”
BackgroundKelly, D. L., Lyon, D., Yoon, S. L., & Horgas, A. L. (2015) · Cancer Nursing · doi:10.1097/ncc.0000000000000286 · Cited by 28
“In fact, probiotics supplementation in diabetic rats recovered the declined basic synaptic transmission and further restored the hippocampal long-term potentiation.(40) With respect to humans, emerging literature in humans suggests an association between the microbiome and cognitive outcomes in individuals with chroni…”
BackgroundJoseph, J., & Law, C. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.11.010 · Cited by 26
Molavi, N., Rasouli‐Azad, M., Mirzaei, H., Matini, A. H., Banafshe, H. R., Valiollahzadeh, M., Hassanzadeh, M., Saghazade, A. R., Abbaszadeh‐Mashkani, S., Mamsharifi, P., et al. (2022) · International Journal of Clinical Practice · doi:10.1155/2022/1206914 · Cited by 26
“Probiotics had 6 International Journal of Clinical Practice inhibitory effects on several oxidative stress factors in nervous system disorders in both human [17] and animal models [69–71].”
Microbiota and stress: a loop that impacts memory
Kraïmi, N., Lormant, F., Calandreau, L., Kempf, F., Zemb, O., Lemarchand, J., Constantin, P., Parias, C., Germain, K., Dupont, C., et al. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105594 · Cited by 28
The microbiota-gut- hippocampus axis
Salami, M., & Soheili, M. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1065995 · Cited by 30
“The probiotic administration enhanced LTP in 6 studies (Davari et al., 2013; Distrutti et al., 2014; Asl et al., 2019; Rezaei Asl et al., 2019; Rezaeiasl et al., 2019; Talani et al., 2020).”
BackgroundSelf-citationMittli, D., Tukacs, V., Ravasz, L., Csősz, É., Kozma, T., Kardos, J., Juhász, G. D., & Kékesi, K. A. (2023) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2023.100594 · Cited by 24
Recent findings within the microbiota–gut–brain–endocrine metabolic interactome
Obrenovich, M. E., Mana, T. S. C., Rai, H., Shola, D. T. N., Sass, C., McCloskey, B., & Levison, B. S. (2017) · Pathology and Laboratory Medicine International · doi:10.2147/plmi.s121487 · Cited by 24
“Conversely, probiotic treatment has been shown to improve diabetic complications in synaptic activity and cognitive function.(22) Furthermore, there are compounds chemically related to the catecholamines and 5-hydroxytryptamine (5-HT).”
Probiotics improve insulin resistance status in an experimental model of Alzheimer’s disease
Azm, S. A. N., Djazayeri, A., Safa, M., Azami, K., Djalali, M., Sharifzadeh, M. S., & Vafa, M. (2017) · Medical Journal of the Islamic Republic of Iran · doi:10.14196/mjiri.31.103 · Cited by 24
“…the results of our pilot study, water volume was calculated (30 mL) and 2 g of probiotics (probiotics dosage was selected based on a previous study (Davari et al. 2013) and our pilot study) including lactobacillus acidophilus, fermentum, Bifidobacterium lactis, and longum (1010 colony forming…”
BackgroundL-3-n-butylphthalide attenuates cognitive deficits in db/db diabetic mice
Zhang, S., Ji, S., Bai, X., Yuan, F., Zhang, L., & Li, J. (2018) · Metabolic Brain Disease · doi:10.1007/s11011-018-0356-6 · Cited by 24
Thakur, A. K., Tyagi, S., & Shekhar, N. (2019) · Translational Medicine Communications · doi:10.1186/s41231-019-0043-6 · Cited by 25
A neuroscience perspective of the gut theory of Parkinson's disease
Smith, L. M., & Parr‐Brownlie, L. C. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13869 · Cited by 25
Talani, G., Biggio, F., Mostallino, M. C., Locci, V., Porcedda, C., Boi, L., Saolini, E., Piras, R., Sanna, E., & Biggio, G. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107909 · Cited by 24
Pang, S., Luo, Z., Wang, C. C., Hong, X., Zhou, J., Chen, F., Ge, L., Li, X., Dai, Y., Wu, Y., et al. (2020) · Journal of Integrative Neuroscience · doi:10.31083/j.jin.2020.02.69 · Cited by 23
“Relevant studies have shown that probiotics, such as Lactobacillus, Clostridium butyricum, and SCFAs have antioxidant effects that reduce oxidative stress, alleviate brain damage and improve cognitive dysfunction (Davari et al., 2013; Kim et al., 2018; Liu et al., 2017; Swidsinski et al., 2012).”
BackgroundA future perspective on neurodegenerative diseases: nasopharyngeal and gut microbiota
Khan, F., & Oloketuyi, S. F. (2016) · Journal of Applied Microbiology · doi:10.1111/jam.13327 · Cited by 22
“Similar reports have claimed that gut flora modulation by probiotics influences gut neuromotor functions reviewed in Verdu (2009), and a study showed that bacterial probiotic supplementation improved impaired memory in diabetic rats (Davari et al. 2013).”
ResultKamal, N., Saharan, B. S., Duhan, J. S., Kumar, A., Chaudhary, P., Goyal, C., Kumar, M., Goyat, N., Sindhu, M., & Mudgil, P. (2024) · Medicine in Microecology · doi:10.1016/j.medmic.2024.100118 · Cited by 24
The Brain-gut Axis-where are we now and how can we Modulate these Connections?
Dąbrowski, W., Siwicka-Gieroba, D., Kotfis, K., Zaid, S., Terpiłowska, S., Robba, C., & Siwicki, A. K. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666201119155535 · Cited by 21
“The probiotic supplementation leads to recovery of the basic synaptic transmission in diabetic rats as well as to enhanced activation of superoxide dismutase [66].”
BackgroundDelaying memory decline: different options and emerging solutions
Schneider, F., Horowitz, A., Lesch, K., & Dandekar, T. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0697-x · Cited by 23
Donovan, H. S., Thomas, T. H., Campbell, G. B., Boisen, M. M., Rosenblum, L., Edwards, R. P., Bovbjerg, D. H., & Horn, C. C. (2016) · Supportive Care in Cancer · doi:10.1007/s00520-015-3071-4 · Cited by 23
“Accumulating evidence also implicates additional symptoms such as depression and anxiety [6–8], cognitive/memory problems [9, 10], sleep rhythms [11], and fatigue [12, 13].”
BackgroundZhao, W., Wang, J., Latta, M., Wang, C., Liu, Y., Ma, W., Zhou, Z., Hu, S., Chen, P., & Liu, Y. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.903659 · Cited by 20
Alemohammad, S. M. A., Noori, S. M. R., Samarbafzadeh, E., & Noori, S. M. A. (2022) · Molecular Biology Reports · doi:10.1007/s11033-021-07078-2 · Cited by 18
“Antioxidant and anti-inflammatory characteristics of Bifidobacterium and Lactobacillus have been shown to cause improvement of depression, mood in Pregnant Sprague–Dawley [71], and cognitive function in rats [72] in addition to long-term dietary supplementation with Bifidobacterium and Lactobacillus improving memory i…”
BackgroundReview of the molecular mechanisms in wound healing: new therapeutic targets?
Palmieri, B., Vadalà, M., & Laurino, C. (2017) · Journal of Wound Care · doi:10.12968/jowc.2017.26.12.765 · Cited by 17
Therapeutic Methods for Gut Microbiota Modification in Lipopolysaccharide-Associated Encephalopathy
Li, S., Guo, H., Xu, X., Hua, R., Zhao, Q., Li, J., Lv, J., & Li, J. (2021) · Shock · doi:10.1097/shk.0000000000001758 · Cited by 18
“Davari (7) found that a cocktail of probiotics, L acidophilus, B lactis, and L fermentum, reversed diabetesinduced cognitive and electrophysiological changes.”
BackgroundAlterations of the glutamatergic system in diabetes mellitus
Hristov, M., Nankova, A., & Andreeva-Gateva, P. A. (2023) · Metabolic Brain Disease · doi:10.1007/s11011-023-01299-z · Cited by 20
“In addition, probiotic administration was reported to improve synaptic activity and cognitive function in STZ-induced diabetic rats (Davari et al. 2013).”
Skalny, A. V., Aschner, M., Гриценко, В. А., Martins, A. C., Tizabi, Y., Korobeinikova, T. V., Paoliello, M. M. B., & Tinkov, A. A. (2024) · Advances in neurotoxicology · doi:10.1016/bs.ant.2024.02.002 · Cited by 19
Pan, S. C., Ward, D. V., Yin, Y., Hu, Y., Elfawal, M. A., Clark, R. E., & Aroian, R. V. (2019) · Scientific Reports · doi:10.1038/s41598-019-44301-4 · Cited by 18
Cui, J., Wang, W., Tang, Y., Feng, S., Liu, H., & Hao, Z. (2025) · Interdisciplinary medicine · doi:10.1002/inmd.20240041 · Cited by 21
Song, C., Yin, Y., Qin, Y., Li, T., Zeng, D., Ju, T., Duan, F., Zhang, Y., & Lu, W. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14134 · Cited by 15
Study on the effects of microencapsulatedLactobacillus delbrueckiion the mouse intestinal flora
Sun, Q., Shi, Y., Wang, F., Han, D., Hong, L., Zhao, Y., & Sun, Q. (2015) · Journal of Microencapsulation · doi:10.3109/02652048.2015.1057249 · Cited by 16
“to improving the cognitive ability (Davari et al., 2013).”
Yu, L., Zhai, Q., Tian, F., Liu, X., Wang, G., Zhao, J., Zhang, H., Narbad, A., & Chen, W. (2017) · Journal of Functional Foods · doi:10.1016/j.jff.2016.12.041 · Cited by 16
Vray, M., Hedible, K. G. B., Adam, P., Tondeur, L., Manirazika, A., Randremanana, R. V., Maïnassara, H. B., Briend, A., Artaud, C., Platen, C. V., et al. (2018) · Trials · doi:10.1186/s13063-018-3027-3 · Cited by 17
The landscape of microbiota research in Iran; a bibliometric and network analysis
Aazami, H., Dehghanbanadaki, H., Ejtahed, H., Fahimfar, N., Razi, F., Soroush, A., Hasani‐Ranjbar, S., Pasalar, P., Badi, S. A., Siadat, S. D., et al. (2020) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-020-00488-2 · Cited by 16
Wu, Y., Yuan, Y., Wu, C., Jiang, T., Wang, B., Xiong, J., Zheng, P., Li, Y., Xu, J., Xu, K., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00602 · Cited by 16
Influence of gut bacteria on type 2 diabetes: Mechanisms and therapeutic strategy
Wen, X., Qi, L., & Zhao, K. (2024) · World Journal of Diabetes · doi:10.4239/wjd.v16.i1.100376 · Cited by 18
Sprenger‐Svačina, A., Svačina, M. K. R., Otlu, H. G., Gao, T., Sheikh, K. A., & Zhang, G. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1602112 · Cited by 16
Effect of Tanshinone IIA on Gut Microbiome in Diabetes-Induced Cognitive Impairment
Zheng, Y., Zhou, X., Wang, C., Zhang, J., Chang, D., Liu, W., Zhu, M.-X., Zhuang, S., Shi, H., Wang, X., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.890444 · Cited by 15
Kim, Y. J., Mun, B.-R., Choi, K. Y., & Choi, W. (2024) · Brain Sciences · doi:10.3390/brainsci14030208 · Cited by 16
“Of these strains, lactic acid bacteria (LAB), such as Lactobacillus and Bifidobacterium , are the most widely utilized probiotics [10].”
BackgroundZhang, W., Yi, C., Song, Z., Yu, B., Jiang, X., Guo, L., Huang, S., Xia, T., Huang, F., Yan, Y., et al. (2025) · Phytomedicine · doi:10.1016/j.phymed.2025.156560 · Cited by 15
Rajab, E., Keogh, M. B., Laiva, A. L., Hannan, F. A., Fateel, M., Abdulwahab, F., Madhoob, F. A., AlHamer, B., Ghazzal, S., Dawaishan, A. A., et al. (2021) · Journal of Functional Foods · doi:10.1016/j.jff.2021.104757 · Cited by 13
Neuroprotective Effects of Probiotic-Supplemented Diet on Cognitive Behavior of 3xTg-AD Mice
Tan, C., Liu, Y., Zhang, H., Di, C., Xu, D., Liang, C., Zhang, N., Han, B., & Lang, W. (2022) · Journal of Healthcare Engineering · doi:10.1155/2022/4602428 · Cited by 14
“In addition, some animal researches have revealed the necessity of the microbiota-gut-brain axis for the optimal function of brain activities in behavior and electrophysiology [14].”
BackgroundRetractedTang, H., Chen, X., Huang, S., Gang, Y., Wang, X., & Shen, G.-M. (2023) · Reviews in the Neurosciences · doi:10.1515/revneuro-2022-0155 · Cited by 14
Chrobak, A. A., Nowakowski, J., & Dudek, D. (2016) · Archives of Psychiatry and Psychotherapy · doi:10.12740/app/62962 · Cited by 15
“One study has shown that Lactobacillus helveticus and Bifidobacterium longum also have beneficial psychological effects that are paired with plasma cortisol reduction [16].”
BackgroundSanborn, V. E., Aljumaah, M. R., Azcárate-Peril, M. A., & Gunstad, J. (2022) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2021-0557 · Cited by 13
Li, W., Wang, Y., Shi, Y., He, F., Zhao, Z., Liu, J., Gao, Z., Zhang, J., & Shen, X. (2024) · FEBS Journal · doi:10.1111/febs.17365 · Cited by 12
“In mice, even moderate alterations in gut microbiota composition induced by probiotic or fecal microbiota transplantation (FMT), elicit significant changes in brain chemistry and function [20,21].”
Intriguing Role of Gut-Brain Axis on Cognition with an Emphasis on Interaction with Papez Circuit
Xavier, J., Anu, M., Fathima, A. S., Ravichandiran, V., & Kumar, N. (2022) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527321666220614124145 · Cited by 11
Dietary Fibers and Proteins Modulate Behavior via the Activation of Intestinal Gluconeogenesis
Sinet, F., Soty, M., Zemdegs, J. C. S., Guiard, B. P., Estrada-Meza, J., Malleret, G., Silva, M., Mithieux, G., & Gautier‐Stein, A. (2021) · Neuroendocrinology · doi:10.1159/000514289 · Cited by 11
Lin, J., Tsai, B. C., Kao, H., Chiang, C.-Y., Chen, Y., Chen, W. S., Ho, T., Yao, C., Kuo, W., & Huang, C. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09982-w · Cited by 10
Xu, C., Zhao, W.-X., Yu, S., Yun, Y., Ma, T., Fan, N., Song, J., Wang, J., & Zhang, Q. (2025) · World Journal of Psychiatry · doi:10.5498/wjp.v15.i3.102567 · Cited by 10
The metabolic and immunomodulatory functions of Bacteroides fragilis; a next-generation probiotic?
Roustapoor, R., Abdi, E., Khabbaz, A., & Abdi, A. (2025) · Medicine in Microecology · doi:10.1016/j.medmic.2025.100137 · Cited by 11
Altering the Gut Microbiome for Cognitive Benefit?
Huynh, K. A., Schneider, M., & Gareau, M. G. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802304-4.00015-3 · Cited by 10
Two gut microbes are necessary and sufficient for normal cognition in Drosophila melanogasterPreprint
DeNieu, M., Mounts, K., & Manier, M. K. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/593723 · Cited by 10
“Moreover, disease models for inflammatory bowel disease [15, 16], diabetes [17], and schizophrenia [18] have associ22 ated the loss of homeostasis of the gut community (dysbiosis) with learning and memory deficits in experimental animals.”
BackgroundSuperior cervical ganglionectomy alters gut microbiota in rats.
Zhang, W., Li, Y., Sun, T., Li, Z., Manyande, A., Xu, W., Feng, M., & Xiang, H. (2022) · PubMed Central · Cited by 9
زواره, ا. ح. ح., خانی, ر. ح., Pakpour, B., Soheili, M., & Salami, M. (2020) · PubMed Central · doi:10.22038/ijbms.2020.41685.9846 · Cited by 9
“We showed that probiotics restore impaired LTP in an animal model of diabetes (21).”
BackgroundMethodSelf-citationJung, H. Y., Chung, T., & Hwang, I. K. (2016) · Molecular & Cellular Toxicology · doi:10.1007/s13273-016-0047-5 · Cited by 9
Muresanu, D. F., Sharma, A., Sahib, S., Tian, Z. R., Feng, L., Nozari, A., Lafuente, J. V., Buzoianu, A. D., Sjöquist, P.-O. B., Patnaik, R., et al. (2020) · Progress in brain research · doi:10.1016/bs.pbr.2020.09.004 · Cited by 8
Luang‐In, V., Saengha, W., Karirat, T., Deeseenthum, S., Buranrat, B., Nudmamud-Thanoi, S., Ma, N. L., & Narbad, A. (2020) · International Journal of Agriculture and Biology · doi:10.17957/ijab/15.1682 · Cited by 8
Kayode, O. T., Rotimi, D., Okoh, E., Iyobhebhe, M. E., Kayode, A. A. A., & Ojo, O. A. (2021) · Journal of Food Biochemistry · doi:10.1111/jfbc.13907 · Cited by 8
Rezaee, N., Rahmani‐Nia, F., Delfan, M., & Ghahremani, R. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119973 · Cited by 8
Ермоленко, Е. И., Abdurasulova, I. N., Котылева, М. П., Svirido, D. A., Matsulevich, A. V., Karaseva, A. B., Тарасова, Е. А., Sizov, V. V., & Suvorov, A. N. (2018) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-018-0591-7 · Cited by 8
Orsi, C., & Zambrini, A. V. (2017) · doi:10.1002/9781118906460.ch1c · Cited by 8
Experimental Stroke Induces Chronic Gut Dysbiosis and Neuroinflammation in Male MicePreprint
Brichacek, A. L., Nwafor, D. C., Benkovic, S. A., Chakraborty, S., Kenney, S. M., Mace, M. E., Jun, S., Gambill, C. A., Wang, W., Hu, H., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.29.069575 · Cited by 7
“31 probiotic treatment with Lactobacillus plantarum ZDY2013 [84], Clostridium butyricum [85], or probiotic mixtures [86,87] have shown improved outcomes in a number of stroke-related”
BackgroundENVOLVIMENTO DA FLORA INTESTINAL NA MODULAÇÃO DE DOENÇAS PSIQUIÁTRICAS
Lach, G., Morais, L. H., Costa, A. P., & Hoeller, A. A. (2017) · VITTALLE - Revista de Ciências da Saúde · doi:10.14295/vittalle.v29i1.6413 · Cited by 12
“Interessantemente, em um modelo animal onde diabete mellitus é induzida em ratos através da administração de estreptozotocina (159,160), ratos diabéticos apresentam déficits de memória e aprendizado devido a prejuízos na potencialização e depressão de longo prazo (LTP e LTD, do inglês long-term potentiation e long-ter…”
BackgroundErukainure, O. L., Mopuri, R., Chukwuma, C. I., Koorbanally, N. A., & Islam, M. S. (2018) · Journal of Food Biochemistry · doi:10.1111/jfbc.12655 · Cited by 8
Kim, J.-C., Yoon, B., & Jeon, Y. K. (2020) · Healthcare · doi:10.3390/healthcare9010007 · Cited by 9
“Besides this, probiotic ingestion led to changes in the neurotransmitters involved in exercise and cognitive functions [13,14], and enhanced learning and memory in treated mice [15].”
BackgroundLi, L., Du, F., Liu, X., Song, M., Grosso, G., Battino, M., Boesch, C., Li, H., & Liu, X. (2025) · Foods · doi:10.3390/foods14101773 · Cited by 8
“Animal studies suggest that probiotics can modulate endogenous neuroactive molecules [17], prevent and treat neuronal autoimmune diseases [18], and ameliorate impaired spatial memory in diabetic rats [19].”
Alteration of oral microbiome composition in children living with pesticide-exposed farm workers
Stanaway, I. B., Wallace, J. C., Hong, S., Wilder, C. S., Green, F. H., Tsai, J. M., Knight, M., Workman, T. W., Vigoren, E. M., Smith, M. N., et al. (2022) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2022.114090 · Cited by 6
A Probiotic Mixture Decreases Neuropathy and Oxidative Stress Markers in Diabetic Rats
Shabani, M., Hasanpour, E., Aghighi, F., Mohammadifar, M., Bahmani, F., & Talaei, S. A. (2024) · OBM Neurobiology · doi:10.21926/obm.neurobiol.2403247 · Cited by 7
“A single intraperitoneal dose of Streptozotocin (65 mg/kg) was injected for diabetes induction [30].”
Self-citationLathiya, N., Aziz, Q., Fawwad, A., Siddiqui, I. A., & Basit, A. (2023) · Pakistan Journal of Medical Sciences · doi:10.12669/pjms.39.3.6485 · Cited by 6
Selvam, R., Koothappan, M., & Subramanian, S. P. (2019) · Asian Journal of Pharmacy and Pharmacology · doi:10.31024/ajpp.2019.5.2.18 · Cited by 6
Probiyotik ve Prebiyotiklerin Bağırsak-Beyin Aksına Etkisi
Özer, M., Özyurt, G., & Harsa, Ş. (2019) · Akademik Gıda · doi:10.24323/akademik-gida.613637 · Cited by 7
Metadata
- Authors
- Davari, S., Talaei, S. A., Alaei, H., & salami, M.
- Affiliations
- Isfahan University of Medical Sciences (IR)
- Kashan University of Medical Sciences (IR)
- Corresponding author
- salami, M.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2013-06
- Volume
- 240
- Pages
- 287-296
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2082281485
- Cited by
- 290
- References
- 53
- Citations by year
- 2026: 6 · 2025: 17 · 2024: 19 · 2023: 31 · 2022: 24 · 2021: 25 · 2020: 32 · 2019: 31 · 2018: 18 · 2017: 19 · 2016: 31 · 2015: 17 · 2014: 11 · 2013: 9
- FWCI
- 33.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deputy of Research, Isfahan University of Medical Sciences (390491)
- Deputy of Research, Kashan University of Medical Sciences (9020)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- probiotics, diabetes mellitus, microbiome-gut-brain axis, spatial memory, learning disabilities, hippocampus, synaptic transmission, long-term potentiation, excitatory postsynaptic potentials, Schaffer collaterals, oxidative stress, superoxide dismutase, 8-hydroxy-2'-deoxyguanosine, insulin, streptozotocin-induced diabetes, cognitive function
- MeSH terms
- 8-Hydroxy-2'-Deoxyguanosine, Analysis of Variance, Animals, Biophysics, Blood Glucose, Brain, Cognition Disorders, Deoxyguanosine, Diabetes Mellitus, Experimental, Disease Models, Animal, Drug Administration Schedule, Electric Stimulation, Hippocampus, Insulin, Male, Streptozocin, Superoxide Dismutase, Rats, Wistar, Long-Term Potentiation, Maze Learning, Probiotics, Rats, Metagenome, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review