Cognitive, Emotional, Behavioral and Physiological Evaluation of the Relationship Between Brain and Gut Microbiota

Year 2022, , 446 - 459, 27.12.2022

Selim Günüç , Aylin Şendemir

https://doi.org/10.18863/pgy.1034963

Abstract

The aim of this study is to examine the effect of gut microbiota on brain functions, mood and psychiatric disorders such as depression, anxiety and behavioral addictions, neurotransmitter levels, cognitive processes such as self-control, decision making and delayed gratification. In this context, the relevant literature was reviewed and the findings were evaluated. The relationships of the bidirectional communication between the brain-gut axis with cognitive, emotional, behavioral and physiological processes were explained with a diagram. As a result, although more research is needed on this subject, it has been observed that the brain-gut axis is bidirectionally established through neural, stress, endocrine and immune systems. In this bidirectional communication process, there are interactions in the context of cognitive, emotional, behavioral and other physiological factors. These factors both individually enter into bidirectional relationships with the brain and gut microbiota and are affected by the bidirectional communication between the brain and gut.

Keywords

Gut, Brain, Microbiota, HPA, Behavior, Cognition, Mood

Beyin ve Bağırsak Mikrobiyotası Arasındaki İlişkinin Bilişsel Duygusal Davranışsal ve Fizyolojik Açıdan Değerlendirilmesi

Abstract

Bu araştırmanın amacı, bağırsak mikrobiyotasının; beyin fonksiyonlarında, depresyon, kaygı ve davranışsal bağımlılıklar gibi duygu durum ve psikiyatrik bozukluklarda, nörotransmiter düzeylerinde, özkontrol, karar verme ve haz erteleme gibi bilişsel süreçlerdeki etkisini incelemektir. Bu bağlamda ilgili literatür taranmış ve bulgular değerlendirilmiştir. Literatür incelemeleri sonucu ulaşılan beyin-bağırsak ekseni arasındaki çift yönlü iletişimin bilişsel, duygusal, davranışsal ve fizyolojik süreçlerle ilişkileri bir diyagram ile açıklanmıştır. Sonuç olarak, bu konuda daha çok araştırmaya ihtiyaç olunmasına karşın, beyin-bağırsak ekseninin nöral, stres, endokrin ve bağışıklık sistemleri üzerinden çift yönlü olarak kurulduğu görülmüştür. Bu çift yönlü iletişim sürecinde bilişsel, duygusal, davranışsal ve diğer fizyolojik faktörler bağlamında etkileşimler bulunmaktadır. Bu faktörlerin hem ayrı ayrı beyin ve bağırsak mikrobiyotasıyla çift yönlü ilişkilere girdiği hem de beyin-bağırsak arasındaki çift yönlü iletişimden etkilendiği sonucuna varılmıştır.

Keywords

Bağırsak, Beyin, Mikrobiyota, HPA, Sinirbilim

References

• Aballay A (2009) Neural regulation of immunity: Role of NPR-1 in pathogen avoidance and regulation of innate immunity. Cell Cycle 8:966–969.
• Amir N, Foa EB, Coles ME 1998 Automatic activation and strategic avoidance of threat-relevant information in social phobia, Journal of abnormal psychology, 107(2), 285.
• Arteaga-Henríquez G, Rosales-Ortiz SK, Arias-Vásquez A, ark. (2020) Treating impulsivity with probiotics in adults (PROBIA): study protocol of a multicenter, double-blind, randomized, placebo-controlled trial. Trials 21, 161.
• Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG Lyte M (2011). Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 25, 397–407.
• Benton, D, Williams C, Brown A 2007 Impact of consuming a milk drink containing a probiotic on mood and cognition, Eur J Clin Nutr, 61, 355–361.
• Bercik P, Verdu EF, Foster JA, Macri J, Potter M, Huang X, Malinowski P, Jackson W, Blennerhassett P, Neufeld KA, Lu J, Khan WI, Corthesy-Theulaz I, Cherbut C, Bergonzelli GE, Collins SM (2010) Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology. 2010 Dec;139(6):2102-2112.e1. doi: 10.1053/j.gastro.2010.06.063. Epub 2010 Jun 27. PMID: 20600016.
• Bercik P, Collins SM (2014) The effects of inflammation, infection and antibiotics on the microbiota-gut-brain axis. Adv. Exp. Med. Biol. 817, 279–89.
• Blasco G, Moreno-Navarrete JM, Rivero M, Pérez-Brocal V, Garre-Olmo J, Puig J, ark. (2017) The gut metagenome changes in parallel to waist circumference, brain iron deposition, and cognitive function. J Clin Endocrinol Metab. 102:2962–73.
• Borre YE, Moloney RD, Clarke G, Dinan TG, Cryan JF (2014) The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv. Exp. Med. Biol. 817, 373–403.
• Brenner DM, Chey WD (2009) Bifidobacterium infantis 35624: a novel probiotic for the treatment of irritable bowel syndrome. Rev Gastroenterol Disord 2009; 9: 7–15.
• Brown K, DeCoffe D, Molcan E, Gibson DL (2012) Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease, Nutrients, 4, 1095–119.
• Buhner S, Schemann M (2012) Mast cell-nerve axis with a focus on the human gut, Biochim Biophys Acta., 1822 (1), 85-92.
• Burokas A, Moloney RD, Dinan TG, Cryan JF (2015) Microbiota regulation of the Mammalian gut–brain axis, Adv Appl Microbiol, 91, 1–62.
• Callaghan B, Fields A, Tottenham N (2017) Regulatory Control and Clinical Implications for Stress, Anxiety, and Depression (Sum). Presented at the New Insights into Affective and Behavioral Regulatory Processes Congress, Rutgers University, New Jersey.
• Carabotti M, Scirocco A, Maselli MA, Severi C (2015) The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. Q. Publ. Hell. Soc. Gastroenterol. 28, 203–209.
• Carpenter S (2012) That Gut Feeling. APA Monitor. 43 (8): 50. Retrieved 16.05.2021.
• Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, Dinan TG, Cryan JF (2013) The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner, Mol Psychiatry, 18, 666-673.
• Comings DE, Rosenthal RJ, Lesieur HR, Rugle LJ, Muhleman D, Chiu C, Dietz G, Gade R (1996) A study of the dopamine D2 receptor gene in pathological gambling, Pharmacogenetics, 6, 223–234.
• Conlon MA, Bird AR (2015) The Impact of Diet and Lifestyle on Gut Microbiota and Human Health, Nutrients, 7, 17-44.
• Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behavior. Nat Rev Neurosci. 13(10):701–12.
• Cryan JF, Page ME, Lucki I (2005) Differential behavioral effects of the antidepressants reboxetine, fluoxetine, and moclobemide in a modified forced swim test following chronic treatment. Psychopharmacology (Berl), 182: 335–44.
• Cryan JF, O’Mahony SM (2011) The Microbiome-Gut-Brain Axis: From Bowel to Behavior. Neurogastroenterology and motility. 23, 187–192.
• Dambrova M, Latkovskis G, Kuka J, Strele I, Konrade I, Grinberga S, ark. (2016) Diabetes is associated with higher trimethylamine N-oxide plasma levels. Exp Clin Endocrinol Diabetes. 124:251–6.
• David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome, Nature, 505 (7484), 559-563.
• De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa, Proc Natl Acad Sci USA, 107 (33), 14691-6.
• De Palma G, Collins SM, Bercik P, Verdu EF (2014) The microbiota-gut-brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both? J. Physiol. 592, 2989–97.
• Dean J, Keshavanb M (2017) The neurobiology of depression: An integrated view. Asian Journal of Psychiatry 27, 101-111. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG (2008) The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res, 43: 164–74.
• Dinan TG, Cryan JF (2017) Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol, 595(2):489–503.
• Dinan TG, Borre YE, Cryan JF (2014) Genomics of schizophrenia: time to consider the gut microbiome? Mol. Psychiatry 19, 1252–7.
• Dinan TG, Cryan JF (2013) Melancholic microbes: a link between gut microbiota and depression?, Neurogastroenterology & Motility, 25 (9), 713-719.
• Duerkop BA, Vaishnava S, Hooper LV (2009) Immune responses to the microbiota at the intestinal mucosal surface”, Immunity, 31, 368–376.
• Eutamene H, Bueno L (2007) Role of probiotics in correcting abnormalities of colonic flora induced by stress. Gut 56, 1495–1497.
• Ferrari F, Villa RF (2017) The Neurobiology of Depression: an Integrated Overview from Biological Theories to Clinical Evidence. Mol Neurobiol, 54, 4847-4865.
• Forsythe P, Kunze WA (2013) Voices from within: gut microbes and the CNS, Cell. Mol. Life Sci., 70, 55-69. Fukui H, Oshima T, Tanaka Y, ark. (2018) Effect of probiotic Bifidobacterium bifidum G9-1 on the relationship between gut microbiota profile and stress sensitivity in maternally separated rats. Sci Rep 8, 12384.
• Galley JD, Bailey MT (2014) Impact of stressor exposure on the interplay between commensal microbiota and host inflammation. Gut Microbes. 5(3):390–6.
• Gao X, Cao Q, Cheng Y, Zhao D, Wang Z, Yang H, ark. (2018) Chronic stress promotes colitis by disturbing the gut microbiota and triggering immune system response. Proc Natl Acad Sci USA. 115:E2960–9.
• Gershon MD (1999) The enteric nervous system: A second brain, Hosp Pract., 34 (7).
• Goehler LE, Park SM, Opitz N, Lyte M, Gaykema RP (2008) Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: Possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 22:354–366.
• Grenham, S, Clarke G, Cryan JF, Dinan TG (2011) Brain-gut-microbe communication in health and disease, Front. Physiol., 2, 94. Han DH, Lee YS, Yang KC, Kim EY, Lyoo IK, Renshaw PF (2007) Dopamine genes and reward dependence in adolescents with excessive internet video game play, Journal of addiction medicine, 1 (3), 133-138.
• Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pattersson S (2011) Normal gut microbiota modulates brain development and Behavior, Proc Natl Acad Sci, 108 (7), 3047-3052.
• Huang R, Wang K, Hu J (2016) Effect of probiotics on depression: a systematic review and meta-analysis of randomized controlled trials. Nutrients. 8:483.
• Kelly JR, Borre Y, O’Brien C, Patterson E, El.Aidy S, Deane J, Kennedy PJ, Beers S, Scott K, Moloney G (2016) Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res, 82, 109-118 Järbrink-Sehgal E, Andreasson A (2020) The gut microbiota and mental health in adults, Current Opinion in Neurobiology, Volume 62, 102-114.
• Jernberg C, Löfmark S, Edlund C, Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota, ISME J., 1 (1), 56-66. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, ark. (2015) Altered fecal microbiota composition in patients with major depressive disorder. Brain, Behav, Immun. 48:186–94.
• Kim J, Hong H, Lee J, Hyun MH (2017) Effects of time perspective and self-control on procrastination and Internet addiction, Journal of behavioral addictions, 6 (2), 229-236. Kim SH, Baik SH, Park CS, Kim SJ, Choi SW, Kim SE (2011) Reduced striatal dopamine D2 receptors in people with Internet addiction, Neuroreport, 22 (8), 407-411.
• Koepp MJ, Gunn RN, Lawrence AD, Cunningham VJ, Dagher A, Jones T, Brooks DJ, Bench CJ, Grasby PM (1998) Evidence for striatal dopamine release during a video game, Nature. 393, 266–268.
• Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F (2016) From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites, Cell., 165 (6), 1332-1345. Leblhuber F, Egger M, Schuetz B, Fuchs D (2018) Commentary: Effect of Probiotic Supplementation on Cognitive Function and Metabolic Status in Alzheimer's Disease: A Randomized, Double-Blind and Controlled Trial. Front Aging Neurosci. 10:54.
• Li D, Ke Y, Zhan R, Liu C, Zhao M, Zeng A, ark. (2018) Trimethylamine-N-oxide promotes brain aging and cognitive impairment in mice. Aging Cell. 49:e12768.
• Li Q, Tian M, Taxer J, Zheng Y, Wu H, Sun S, Liu X (2016) Problematic internet users' discounting behaviors reflect an inability to delay gratification, not risk taking, Cyberpsychology, Behavior, and Social Networking, 19 (3), 172-178.
• Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., Duan, Y., Jin, F. 2015. “Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress”, Neuroscience, 310, 561-577.
• Logan AC, Katzman M (2005) Major depressive disorder: probiotics may be an adjuvant therapy. Med Hypotheses 2005; 64: 533–8.
• Messaoudi M, Lalonde R, Violle N, ark. (2010) Assessment of psychotropic‐like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr, 26: 1–9.
• 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, Br. J. Nutr., 105 (5), 755-764.
• Ming X, Chen N, Ray C, Brewer G, Kornitzer J, Steer RA (2018) A gut feeling: a hypothesis of the role of the microbiome in attention-deficit/hyperactivity disorders. Child Neurol Open. 5:2329048X18786799.
• Mittal VA, Ellman LM, Cannon TD (2008) Gene-environment interaction and covariation in schizophrenia: The role of obstetric complications. Schizophr Bull 34:1083–1094.
• Mizunoya W, Ohnuki K, Baba K, Miyahara H, Shimizu N, Tabata K, Kino T, Sato Y, Tatsumi R, Ikeuchi Y (2013) Effect of dietary fat type on anxiety-like and depression-like behavior in mice, Springer- plus, (2) 165.
• Moelling K (2016) Nutrition and the microbiome, Ann N Y Acad Sci., 1372 (1), 3-8.
• Myles IA (2014) Fast food fever: reviewing the impacts of the Western diet on immunity, Nutrition journal, 13 (1), 61.
• Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linløkken A, Wilson R, ark. (2014) Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil. 26:1155–62.
• Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linløkken A, Wilson R, Rudi K (2014) Correlation between the human fecal microbiota and depression, Neurogastroenterology & Motility, 26 (8), 1155-1162.
• Neufeld KM, Kang N, Bienenstock J, Foster JA (2010) Reduced anxiety‐like behavior and central neurochemical change in germ‐free mice. Neurogastroenterol and Motility; 23: 255–64.
• Neufeld KM, Kang N, Bienenstock J, Foster JA (2011) Reduced anxiety- like behavior and central neurochemical change in germ-free mice, Neurogastroenterol Motil, 23, 255-264.
• Nishino R, Mikami K, Takahashi H, Tomonaga S, Furuse M, Hiramoto T, Aiba Y, Koga Y, Sudo N (2013) Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods, Neurogastroenterol Motil, 25, 521-528.
• O’Mahony SM, Hyland NP, Dinan TG, Cryan JF (2011) Maternal separation as a model of brain-gut axis dysfunction, Psychopharmacology, 214, 71–88.
• Oh WO (2003) Factors influencing internet addiction tendency among middle school students in Gyeong-buk area”, Taehan Kanho Hakhoe Chi, 33, 1135-1144.
• Özdemir A, Büyüktuncer Demirel Z (2017) Beslenme ve mikrobiyota ilişkisi, J Biotechnol and Strategic Health Res, 1 (Special issue), 25-33.
• Pallanti S, Haznedar MM, Hollander E, LiCalzi EM, Bernardi S, Newmark R, Buchsbaum MS (2010) Basal ganglia activity in pathological gambling: A fluorodeoxyglucose-positron emission tomography study, Neuropsychobiology, 62, 132-138.
• Panda S, El khader I, Casellas F, López Vivancos J, García Cors M, Santiago A, Cuenca S, Guarner F, Manichanh C (2014) Short-term effect of antibiotics on human gut microbiota, PLoS One, 9 (4), 54-76.
• Paulus MP (2007) Decision-making dysfunctions in psychiatry-altered homeostatic processing?, Science, 318 (5850), 602-606.
• Paulus MP, Angela JY (2012) Emotion and decision-making: affect-driven belief systems in anxiety and depression, Trends in cognitive sciences, 16 (9), 476-483.
• Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE (2006) Factors influencing the composition of the intestinal microbiota in early infancy, Pediatrics, 118, 511-521.
• 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. 2015;37(5):984–95.
• Pirbaglou M, Katz J, de Souza RJ, Stearns JC, Motamed M, Ritvo P (2016) Probiotic supplementation can positively affect anxiety and depressive symptoms: a systematic review of randomized controlled trials. Nutr Res. 36:889–98.
• Popoli M, Yan Z, McEwen BS, Sanacora G (2012) The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat. Rev. Neurosci. 13, 22–37.
• Putignani L, Del Chierico F, Petrucca A, Vernocchi P, Dallapiccola B (2014) The human gut microbiota: A dynamic interplay with the host from birth to senescence settled during childhood, Pediatr Res., 76 (1), 2-10.
• Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing, Nature, 464, 59-65.
• Rieder R. Wisniewski PJ, Alderman BL, Campbell SC (2017) Microbes and mental health: A review, Brain Behav Immun., 66, 9-17.
• Roager HM, Vogt JK, Kristensen M, Hansen LB, Ibrügger S, Mærkedahl RB, ark. (2019) Whole grain-rich diet reduces body weight and systemic low-grade inflammation without inducing major changes of the gut microbiome: a randomised cross-over trial, Gut, Jan, 68 (1), 83-93.
• Rogers GB, Keating DJ, Young RL, Wong ML, Licinio J, Wesselingh S (2016) From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol Psychiatry. 21:738–48.
• Roman P. Estevez AF, Miras A, Sanchez-abraca N, Canadas F, Vivas AB, Cardona D (2018) A pilot randomized controlled trial to explore cognitive and emotional effects of probiotics in fibromyalgia. Sci Rep, 8 ,Article 10965
• Romijn AR, Rucklidge JJ, Kuijer RG, Frampton C (2017) A double-blind, randomized, placebo-controlled trial of Lactobacillus helveticus and Bifidobacterium longum for the symptoms of depression. Aust NZ J Psychiatry. 51:810–21.
• Salazar N, Arboleya S, Valdes L, Stanton C, Ross P, Ruiz L, Gueimonde M, de Los Reyes Gavilan CG (2014) The human intestinal microbiome at extreme ages of life. Dietary intervention as a way to counteract alterations, Front Genet., 5, 406.
• Saville BK, Gisbert A, Kopp J, Telesco C (2010) Internet addiction and delay discounting in college students. The Psychological Record, 60, 273-286.
• Schroeder FA, Lin CL, Crusio WE, Akbarian S (2007) Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse, Biol Psychiatry, 62, 55-64.
• Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task, Journal of neuroscience, 13(3), 900-913.
• Seok JW, Lee KH, Sohn S, Sohn JH (2015) Neural substrates of risky decision making in individuals with Internet addiction, Australian & New Zealand Journal of Psychiatry, 49 (10), 923-932.
• Sherwin E, Rea K, Dinan TG, Cryan JF (2016) A gut (microbiome) feeling about the brain. Curr. Opin. Gastroenterol. 32, 96–102. Singh RK, Chang HW, Yan D, Lee KM, Ucmak D, Wong K, Abrouk M, Farahnik B, Nakamura M, Zhu TH, Bhutani T, Liao W (2017) Influence of diet on the gut microbiome and implications for human health”, J Transl Med., 8, 15 (1), 73.
• Sinha R (2009) Modeling stress and drug craving in the laboratory: Implications for addiction treatment development, Addiction biology, 14 (1), 84-98.
• Skosnik PD, Cortes-Briones JA (2016) Targeting the ecology within: The role of the gut–brain axis and human microbiota in drug addiction, Medical hypotheses, 93, 77-80.
• Solís G, de Los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M (2010) Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut, Anaerobe., 16 (3), 307-310.
• Stasi C, Sadalla S, Milani S (2019) The Relationship Between the Serotonin Metabolism, Gut-Microbiota and the Gut-Brain Axis. Curr Drug Metab, 20(8): 646-655.
• Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS. (2015). A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain, Behav, Immun. 48:258–64.
• Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS (2015) A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood, Brain, Behav. Immun., 48, 258-264.
• Sudo N, Chida Y, Aiba Y, ark. (2004) Postnatal microbial colonization programs the hypothalamic‐pituitary‐adrenal system for stress response in mice. J Physiol; 558(Pt 1): 263–75.
• Sullivan R, ark. (2006) The International Society for Developmental Psychobiology annual meeting symposium: Impact of early life experiences on brain and behavioral development. Dev Psychobiol 48:583–602.
• Sun DL, Chen ZJ, Ma N, Zhang XC, Fu XM, Zhang DR. (2009) Decision-making and prepotent response inhibition functions in excessive internet users, CNS spectrums, 14 (2), 75-81.
• Tangney JP, Baumeister RF, Boone AL (2004) High self-control predicts good adjustment, better grades, and inter-personal success, Journal of Personality, 72 (2), 271-324.
• Thomas V, Clark J, Dore J (2015) Fecal microbiota analysis: An overview of sample collection methods and sequencing strategies, Future Microbiol, 10, 1485-1504.
• Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, Guyonnet D, Legrain-Raspaud S, Trotin B, Naliboff B, Mayer EA (2013) Consumption of a fermented milk product with probiotic modulates brain activity, Gastroenterology, 144, 1394-1401.
• Vogt NM, Romano KA, Darst BF, Engelman CD, Johnson SC, Carlsson CM, ark. (2018) The gut microbiota-derived metabolite trimethylamine N-oxide is elevated in Alzheimer’s disease. Alzheimers Res Ther. 10:124
• Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J, Alexoff D, Ding YS, Wong C, Ma Y, Pradhan K (2008) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible ontributing factors, Neuroimage, 42, 1537-1543.
• Vythilingam M, Blair KS, McCaffrey D, Scaramozza M, Jones M, Nakic M, Mondillo K, Hadd K, Bonne O, Mitchell DGV, Pine DS, Charney DS, Blair O (2007) Biased emotional attention in post-traumatic stress disorder: a help as well as a hindrance?, Psychological medicine, 37 (10), 1445-1455.
• Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota, ISME J., 5 (2), 220-30.
• Wampach L, Heintz-Buschart A, Fritz JV, ark. (2018) Birthmode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential, Nat Commun., 9 (1), 5091. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W, Netusil N, Fowler JS (2001) Brain dopamine and obesity, Lancet, 357, 354-357.
• Ward A, Mann T (2000) Don't mind if I do: Disinhibited eating under cognitive load, Journal of personality and social psychology, 78 (4), 753.
• Wu GD, Chen J, Hoffmann C, ark. (2011) Linking long-term dietary patterns with gut microbial enterotypes, Science, 7, 334 (6052), 105-8.
• Xu Z, Knight R (2015) Dietary effects on human gut microbiome diversity, Br J Nutr., 113 Suppl, 1-5.
• Zalar B, Haslberger A, Peterlin B (2018) The role of microbiota in depression: A brief review, Psychiatr Danub., 30(2), 136-141.
• Zaura E, Brandt BW, Teixeira de Mattos MJ, Buijs MJ, Caspers MP, Rashid MU, ark. (2015) Same Exposure but Two Radically Different Responses to Antibiotics: Resilience of the Salivary Microbiome versus Long-Term Microbial Shifts in Feces, M.Bio, 10, 6 (6), 1693-15.