Skip to main content
SpringerLink
Log in

The Efficacy of Fecal Transplantation and Bifidobacterium Supplementation in Ameliorating Propionic Acid-Induced Behavioral and Biochemical Autistic Features in Juvenile Male Rats

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

Gut microbiota plays a major role in neurological disorders, including autism. Modulation of the gut microbiota through fecal microbiota transplantation (FMT) or probiotic administration, such as Bifidobacteria, is suggested to alleviate autistic symptoms; however, their effects on the brain are not fully examined. We tested both approaches in a propionic acid (PPA) rodent model of autism as treatment strategies. Autism was induced in Sprague–Dawley rats by administering PPA orally (250 mg/kg) for 3 days. Animals were later treated with either saline, FMT, or Bifidobacteria for 22 days. Control animals were treated with saline throughout the study. Social behavior and selected brain biochemical markers related to stress hormones, inflammation, and oxidative stress were assessed. PPA treatment induced social impairments, which was rescued by the treatments. In the brain, Bifidobacteria treatment increased oxytocin relative to control and PPA groups. Moreover, Bifidobacteria treatment rescued the PPA-induced increase in IFN-γ levels. Both treatments increased GST levels, which was diminished by the PPA treatment. These findings indicate the potential of gut microbiota-targeted therapeutics in ameliorating behavioral deficit and underlying neural biochemistry.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abuaish S, Al-Otaibi NM, Abujamel TS, Alzahrani SA, Alotaibi SM, AlShawakir YA, Aabed K, El-Ansary A (2021) Fecal transplant and Bifidobacterium treatments modulate gut Clostridium bacteria and rescue social impairment and hippocampal BDNF expression in a rodent model of autism. Brain Sci 11:1038

    PubMed  PubMed Central  Google Scholar 

  • Alam R, Abdolmaleky HM, Zhou JR (2017) Microbiome, inflammation, epigenetic alterations, and mental diseases. Am J Med Genet B 174:651–660

    CAS  Google Scholar 

  • Al-Ayadhi L, Zayed N, Bhat RS, Moubayed NMS, Al-Muammar MN, El-Ansary A (2021) The use of biomarkers associated with leaky gut as a diagnostic tool for early intervention in autism spectrum disorder: a systematic review. Gut Pathog 13(1):54

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baio J, Wiggins L, Christensen DL, Maenner MJ, Daniels J, Warren Z, Kurzius-Spencer M, Zahorodny W, Robinson Rosenberg C, White T, Durkin MS, Imm P, Nikolaou L, Yeargin-Allsopp M, Lee LC, Harrington R, Lopez M, Fitzgerald RT, Hewitt A, Pettygrove S, Constantino JN, Vehorn A, Shenouda J, Hall-Lande J, Van Naarden BK, Dowling NF (2018) Prevalence of autism spectrum disorder among children aged 8 years–autism and developmental disabilities monitoring network, 11 sites, United States, 2014. MMWR Morb Mortal Wkly Rep 67(19):564

    Google Scholar 

  • Bastiaanssen TFS, Cryan JF (2021) The microbiota-gut-brain axis in mental health and medication response: parsing directionality and causality. Int J Neuropsychopharmacol 24(3):216–220

    PubMed  PubMed Central  Google Scholar 

  • Beutler E, Duran O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  Google Scholar 

  • Borrelli L, Aceto S, Agnisola C, De Paolo S, Dipineto L, Stilling RM, Dinan TG, Cryan JF, Menna LF, Fioretti A (2016) Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish. Sci Rep 6:30046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M (2016) Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165:1762–1775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carabotti M, Scirocco A, Maselli MA, Severi C (2015) The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol 28(2):203–209

    PubMed  PubMed Central  Google Scholar 

  • Chen K, Fu Y, Wang Y, Liao L, Xu H, Zhang A, Zhang J, Fan L, Ren J, Fang B (2020) Therapeutic effects of the in vitro cultured human gut microbiota as transplants on altering gut microbiota and improving symptoms associated with autism spectrum disorder. Microb Ecol 80:475–486. https://doi.org/10.1007/s00248-020-01494-w

    Article  CAS  PubMed  Google Scholar 

  • Coretti L, Paparo L, Riccio MP, Amato F, Cuomo M, Natale A, Borrelli L, Corrado G, Comegna M, Buommino E, Castaldo G, Bravaccio C, Chiariotti L, Berni Canani R, Lembo F (2018) Gut microbiota features in young children with autism spectrum disorders. Front Microbiol 19(9):3146. https://doi.org/10.3389/fmicb.2018.03146

    Article  Google Scholar 

  • De Angelis M, Francavilla R, Piccolo M, De Giacomo A, Gobbetti M (2015) Autism spectrum disorders and intestinal microbiota. Gut Microbes 6:207–213

    PubMed  PubMed Central  Google Scholar 

  • Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG (2010) Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170:1179–1188. https://doi.org/10.1016/j.neuroscience.2010.08.005

    Article  CAS  PubMed  Google Scholar 

  • Dinan JF, Cryan TG (2015) The impact of gut microbiota on brain and behavior: implications for psychiatry. Curr Opin Clin Nutr Metab Care 18(6):552–558

    PubMed  Google Scholar 

  • Duranti S, Ruiz L, Lugli GA, Tames H, Milani C, Mancabelli L, Mancino W, Longhi G, Carnevali L, Sgoifo A, Margolles A, Ventura M, Ruas-Madiedo P, Turroni F (2020) Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA. Sci Rep 10:14112. https://doi.org/10.1038/s41598-020-70986-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Ansary AK, Ben Bacha A, Kotb M (2012) Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J Neuroinflammation 9:74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Estes A, Zwaigenbaum L, Gu H, St John T, Paterson S, Elison JT, Hazlett H, Botteron K, Dager SR, Schultz RT, Kostopoulos P, Evans A, Dawson G, Eliason J, Alvarez S, Piven J, IBIS network (2015) Behavioral, cognitive, and adaptive development in infants with autism spectrum disorder in the first 2 years of life. J Neurodev Disord 7:24. https://doi.org/10.1186/s11689-015-9117-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Fattorusso A, Di Genova L, Dell’Isola GB, Mencaroni E, Esposito S (2019) Autism spectrum disorders and the gut microbiota. Nutrients 11:521

    CAS  PubMed Central  Google Scholar 

  • Filosa S, Di Meo F, Crispi S (2018) Polyphenols-gut microbiota interplay and brain neuromodulation. Neural Regen Res 13:2055–2059. https://doi.org/10.4103/1673-5374.241429

    Article  PubMed  PubMed Central  Google Scholar 

  • Forssberg H (2019) Microbiome programming of brain development: implications for neurodevelopmental disorders. Dev Med Child Neurol 61:744–749

    PubMed  Google Scholar 

  • Friard O, Gamba M (2016) BORIS: A free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7(11):1325–1330. https://doi.org/10.1111/2041-210X.12584

    Article  Google Scholar 

  • Fujita H, Kodama T, du Lac S (2020) Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis. Elife 9:e58613

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo P, Zhang K, Ma X et al (2020) Clostridium species as probiotics: potentials and challenges. J Animal Sci Biotechnol 11:24. https://doi.org/10.1186/s40104-019-0402-1

    Article  Google Scholar 

  • Grenham S, Clarke G, Cryan JF, Dinan TG (2011) Brain-gut-microbe communication in health and disease. Front Physiol 2:94

    PubMed  PubMed Central  Google Scholar 

  • Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, Gionchetti P, Campieri M, Kamm MA, Knight SC, Stagg AJ (2004) Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53:1602–1609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heijtz RD, Wang S, Anuar F, Qian Yu, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108:3047–3052

    PubMed  Google Scholar 

  • Hooks KB, O’malley MA (2017) Dysbiosis and its discontents. Mbio 8:e01492-1517. https://doi.org/10.1128/mbio.01492-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsiao EY (2013) Immune dysregulation in autism spectrum disorder. Int Rev Neurobiol 113:269–302

    CAS  PubMed  Google Scholar 

  • Jagota SK, Dani HM (1982) A new colorimetric technique for the estimation of vitamin C using Folin phenol reagent. Anal Biochem 127(1):178–182

    CAS  PubMed  Google Scholar 

  • Kreiser NL, White SW (2014) ASD in females: are we overstating the gender difference in diagnosis? Clin Child Fam Psychol Rev 17:67–84

    PubMed  Google Scholar 

  • Kwon HK, Kim GC, Kim Y, Hwang W, Jash A, Sahoo A, Kim JE, Nam JH, Im SH (2013) Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol 146(3):217–227

    CAS  PubMed  Google Scholar 

  • Livanos AE, Snider EJ, Whittier S et al (2018) Rapid gastrointestinal loss of Clostridial Clusters IV and XIVa in the ICU associates with an expansion of gut pathogens. PLoS One 13(8):e0200322

    PubMed  PubMed Central  Google Scholar 

  • Li N, Wang Q, Wang Y, Sun A, Lin Y, JinY LX (2018) Oral probiotics ameliorate the behavioral deficits induced by chronic mild stress in mice via the gut microbiota-inflammation axis. Front Behav Neurosci 12:266. https://doi.org/10.3389/fnbeh.2018.00266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Li X, Shang Q, Gao Z, Hao F, Guo H, Guo C (2017) nFecal microbiota transplantation (FMT) could reverse the severity of experimental necrotizing enterocolitis (NEC) via oxidative stress modulation. Free Radic Biol Medn 108:32–43

    CAS  Google Scholar 

  • Liu S, Li E, Sun Z, Fu D, Duan G, Jiang M, Yu Y, Mei L, Yang P, Tang Y et al (2019) Altered gut microbiota and short chain fatty acids in Chinese children with autism spectrum disorder. Sci Rep 9:287

    PubMed  PubMed Central  Google Scholar 

  • Lo SC, Scearce-Levie K, Sheng M (2016) Characterization of social behaviors in caspase-3 deficient mice. Sci Rep 6:18335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma B, Liang J, Dai M, Wang J, Luo J, Zhang Z, Jing J (2019) Altered gut microbiota in Chinese children with autism spectrum disorder. Front Cell Infect Microbiol 9:40

    CAS  PubMed  PubMed Central  Google Scholar 

  • MacFabe DF (2015) Enteric short-chain fatty acids: microbial messengers of metabolism, mitochondria, and mind: implications in autism spectrum disorders. Microb Ecol Health Dis 26:28177

    PubMed  Google Scholar 

  • MacFabe DF, Cain DP, Rodriguez-Capote K, Franklin AE, Hoffman JE, Boon F, Taylor AR, Kavaliers M, Ossenkopp KP (2007) Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav Brain Res 176:149–169

    CAS  PubMed  Google Scholar 

  • Mardani F, Mahmoudi M, Esmaeili SA, Khorasani S, Tabasi N, Rastin M (2018) In vivo study: Th1-Th17 reduction in pristane-induced systemic lupus erythematosus mice after treatment with tolerogenic Lactobacillus probiotics. J Cell Physiol 234:642–649

    PubMed  Google Scholar 

  • Margari L, Palumbi R, Peschechera A, Craig F, De Giambattista C, Ventura P, Margari F (2019) Sex-gender comparisons in comorbidities of children and adolescents with high functioning autism spectrum disorder. Front Psychiatr 10:159

    Google Scholar 

  • Martin CR, Osadchiy V, Kalani A, Mayer EA (2018) The brain-gut-microbiome axis. Cell Mol Gastroenterol Hepatol 6(2):133–148

    PubMed  PubMed Central  Google Scholar 

  • Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Rougeot C, Pichelin M, Cazaubiel M, Cazaubiel JM (2011) Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Brit J Nutr 105:755–764. https://doi.org/10.1017/S0007114510004319

    Article  CAS  PubMed  Google Scholar 

  • Meyyappan CA, Forth E, Wallace CJK, Milev R (2020) Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review. BMC Psychiatry 20:299. https://doi.org/10.1186/s12888-020-02654-5

    Article  Google Scholar 

  • Molina-Torres G, Rodriguez-Arrastia M, Roman P, Sanchez-Labraca N, Cardona D (2019) Stress and the gut microbiota-brain axis. Behav Pharmacol 30:187–200. https://doi.org/10.1097/fbp.0000000000000478

    Article  PubMed  Google Scholar 

  • Nankova BB, Agarwal R, Macfabe DF, La Gamma EF (2014) Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells–possible relevance to autism spectrum disorders. PLoS One 9:e103740

    PubMed  PubMed Central  Google Scholar 

  • Petra AI, Panagiotidou S, Hatziagelaki E, Stewart JM, Conti P, Theoharides TC (2015) Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther 37(5):984–995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ristori MV, Quagliariello A, Reddel S, Ianiro G, Vicari S, Gasbarrini A, Putignani L (2019) Autism, gastrointestinal symptoms and modulation of gut microbiota by nutritional interventions. Nutrients 11:2812

    CAS  PubMed Central  Google Scholar 

  • Roman P, Rueda-Ruzafa L, Cardona D, Cortes-Rodríguez A (2018) Gut-brain axis in the executive function of austism spectrum disorder. Behav Pharmacol 29(7):654-663. https://doi.org/10.1097/FBP.0000000000000428. PMID:30179883.

  • Savignac HM, Kiely B, Dinan TG, Cryan JF (2014) Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 26:1615–1627

    CAS  PubMed  Google Scholar 

  • Schwarzer M, Srutkova D, Schabussova I, Hudcovic T, Akgün J, Wiedermann U, Kozakova H (2013) Neonatal colonization of germ-free mice with Bifidobacterium longum prevents allergic sensitization to major birch pollen allergen Bet v 1. Vaccine 31(46):5405–5412

    CAS  PubMed  Google Scholar 

  • Sealey LA, Hughes BW, Sriskanda AN, Guest JR, Gibson AD, Johnson-Williams L, Pace DG, Bagasra O (2016) Environmental factors in the development of autism spectrum disorders. Environ Int 88:288–298

    CAS  PubMed  Google Scholar 

  • Sgritta M, Dooling SW, Buffington SA, Momin EN, Francis MB, Britton RA (2019) Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 101:246–259

    CAS  PubMed  Google Scholar 

  • Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, Blugeon S, Bridonneau C, Furet J-P, Corthier G et al (2008) (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105:16731–16736

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558:263–275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian P, Wang G, Zhao J, Zhang H, Chen W (2019) Bifidobacterium with the role of 5-hydroxytryptophan synthesis regulation alleviates the symptom of depression and related microbiota dysbiosis. J Nutr Biochem 66:43–51. https://doi.org/10.1016/j.jnutbio.2019.01.007

    Article  CAS  PubMed  Google Scholar 

  • Wang JJ, Wang J, Pang XY, Zhao LP, Tian L, Wang XP (2016) Sex differences in colonization of gut microbiota from a man with short-term vegetarian and inulin-supplemented diet in germ-free mice. Sci Rep 6:36137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ward L, O’Grady H, Wu K, Cannon K, Workentine M, Louie T (2019) Combined oral fecal capsules plus fecal enema as treatment of late-onset autism spectrum disorder in children: report of a small case series. Open Forum Infect Dis 3:2219

    Google Scholar 

  • Xu HM, Huang HL, Zhou YL, Zhao HL, Xu J, Shou DW, Liu YD, Zhou YJ, Nie YQ (2021) Fecal microbiota transplantation: a new therapeutic attempt from the gut to the brain. Gastroenterol Res Pract 2021:6699268. https://doi.org/10.1155/2021/6699268

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan S, Yang B, Paul R, Stanton C, Zhang H, Zhao J, Chen W (2020) Bifidobacterium longum subsp. longum YS108R fermented milk alleviates DSS induced colitis via anti-inflammation, mucosal barrier maintenance and gut microbiota modulation. J Funct Foods 73:104153

    CAS  Google Scholar 

  • Yang Y, Tian J, Yang B (2018) Targeting gut microbiome: a novel and potential therapy for autism. Life Sci 194:111–119. https://doi.org/10.1016/j.lfs.2017.12.027

    Article  CAS  PubMed  Google Scholar 

  • Young SL, Simon MA, Baird MA, Tannock GW, Bibiloni R, Spencely K, Lane JM, Fitzharris P, Crane J, Town I, Addo-Yobo E, Murray CS, Woodcock A (2004) Bifidobacterial species differentially affect expression of cell surface markers and cytokines of dendritic cells harvested from cord blood. Clin Diagn Lab Immunol 11:686–690

    PubMed  PubMed Central  Google Scholar 

  • Zurita MF, Cárdenas PA, Sandoval ME, Peña MC, Fornasini M, Flores N, Monaco MH, Berding K, Donovan SM, Kuntz T, Gilbert JA, Baldeón ME (2020) Analysis of gut microbiome, nutrition and immune status in autism spectrum disorder: a case-control study in Ecuador. Gut Microb 11:453–464

    Google Scholar 

Download references

Funding

This research project was funded by the Deanship of Scientific Research, Princess Nourah Bint Abdulrahman University, Grant number RGP-1441–0027.

Author information

Authors and Affiliations

  1. Department of Basic Sciences, College of Medicine, Princess Nourah Bint Abdulrahman University, Riyadh, Saudi Arabia

    Sameera Abuaish

  2. Department of Biology, College of Science, Princess Nourah Bint Abdulrahman University, Riyadh, Saudi Arabia

    Norah M. Al-Otaibi, Kawther Aabed, Saleha Ahmad Alzahrani & Sohailah Masoud Alotaibi

  3. Vaccines and Immunotherapy Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Turki S. Abujamel

  4. Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Turki S. Abujamel

  5. Department of Biochemistry, College of Science, King Saud University, Riyadh, Saudi Arabia

    Ramesa Shafi Bhat

  6. Department of Food Science and Nutrition, King Saud University, Riyadh, Saudi Arabia

    Shaista Arzoo

  7. Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

    Nadine MS Moubayed

  8. Central Research Laboratory, King Saud University Female Campus, P O Box 22452, Prince Turki Road, Riyadh, 22452, Saudi Arabia

    Norah Algahtani & Afaf El-Ansary

Authors
  1. Sameera Abuaish
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norah M. Al-Otaibi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kawther Aabed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Turki S. Abujamel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Saleha Ahmad Alzahrani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sohailah Masoud Alotaibi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ramesa Shafi Bhat
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shaista Arzoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Norah Algahtani
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nadine MS Moubayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Afaf El-Ansary
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SA: data acquisition, statistical analysis, co-drafting the manuscript. NM: experimental work. KA: fund acquisition and revision of the manuscript. TA: revised the manuscript. SA: experimental work. SM: experimental work. RSB: data acquisition. SA: data acquisition. NA: data acquisition. NM: experimental work. AE: conceptualization, and drafting the manuscript.

Corresponding author

Correspondence to Afaf El-Ansary.

Ethics declarations

Ethical Approval and Consent to Participate

Ethical approval from the Institutional Review Board were obtained, and no need for consent as the study used rodent model.

Consent for Publication

All authors read the manuscript and agree to publish.

Competing Interests

The authors declare no competing interests.

Additional information

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

Abuaish, S., Al-Otaibi, N.M., Aabed, K. et al. The Efficacy of Fecal Transplantation and Bifidobacterium Supplementation in Ameliorating Propionic Acid-Induced Behavioral and Biochemical Autistic Features in Juvenile Male Rats. J Mol Neurosci 72, 372–381 (2022). https://doi.org/10.1007/s12031-021-01959-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-021-01959-8

Keywords

Search

Navigation