Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?

Neuroscience

Volumn 342, Issue , 2017, Pages 37-54

  O'Mahony, S M ^a,b   Clarke, G ^a,b   Dinan, T G ^a,b   Cryan, J F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

brain development; brain gut axis; early life; microbiota; stress

Indexed keywords

VALPROIC ACID;

AUTISM; BODY MASS; BRAIN DEVELOPMENT; CELL MIGRATION; CHILDHOOD OBESITY; GASTROINTESTINAL TRACT; HOST SUSCEPTIBILITY; HUMAN; IMMUNE SYSTEM; INTESTINE FLORA; LIFE EVENT; METABOLIC DISORDER; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRENATAL STRESS; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR FUNCTION; ANIMAL; BRAIN; FEMALE; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; BRAIN; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PSYCHOLOGICAL;

EID: 84951325446     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.09.068     Document Type: Review

References (294)

1. Aagaard, K., Ma, J., Antony, K.M., Ganu, R., Petrosino, J., Versalovic, J., The placenta harbors a unique microbiome. Sci Transl Med, 6, 2014, 237ra265.
2. Aagaard, K., Riehle, K., Ma, J., Segata, N., Mistretta, T.A., Coarfa, C., Raza, S., Rosenbaum, S., Van den Veyver, I., Milosavljevic, A., Gevers, D., Huttenhower, C., Petrosino, J., Versalovic, J., A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One, 7, 2012, e36466.
3. Ader, R., Adrenocortical function and the measurement of “emotionality”. Ann N Y Acad Sci 159 (1969), 791–805.
4. Agans, R., Rigsbee, L., Kenche, H., Michail, S., Khamis, H.J., Paliy, O., Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol 77 (2011), 404–412.
5. Albers, E.M., Riksen-Walraven, J.M., Sweep, F.C., de Weerth, C., Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. J Child Psychol Psychiatry 49 (2008), 97–103.
6. Anacker, C., O'Donnell, K.J., Meaney, M.J., Early life adversity and the epigenetic programming of hypothalamic–pituitary–adrenal function. Dialogues Clin Neurosci 16 (2014), 321–333.
7. Andersen, S.L., Trajectories of brain development: point of vulnerability or window of opportunity?. Neurosci Biobehav Rev 27 (2003), 3–18.
8. Andrews, B., Brewin, C.R., Rose, S., Kirk, M., Predicting PTSD symptoms in victims of violent crime: the role of shame, anger, and childhood abuse. J Abnorm Psychol 109 (2000), 69–73.
9. Antony, K.M., Ma, J., Mitchell, K.B., Racusin, D.A., Versalovic, J., Aagaard, K., The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol, 212, 2015, 653 e651–e653 e616.
10. Arabadzisz, D., Diaz-Heijtz, R., Knuesel, I., Weber, E., Pilloud, S., Dettling, A.C., Feldon, J., Law, A.J., Harrison, P.J., Pryce, C.R., Primate early life stress leads to long-term mild hippocampal decreases in corticosteroid receptor expression. Biol Psychiatry 67 (2010), 1106–1109.
11. Azad, M.B., Konya, T., Maughan, H., Guttman, D.S., Field, C.J., Chari, R.S., Sears, M.R., Becker, A.B., Scott, J.A., Kozyrskyj, A.L., Investigators, C.S., Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185 (2013), 385–394.
12. Backhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., Khan, M.T., Zhang, J., Li, J., Xiao, L., Al-Aama, J., Zhang, D., Lee, Y.S., Kotowska, D., Colding, C., Tremaroli, V., Yin, Y., Bergman, S., Xu, X., Madsen, L., Kristiansen, K., Dahlgren, J., Jun, W., Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17 (2015), 690–703.
13. Bailey, M.T., Coe, C.L., Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35 (1999), 146–155.
14. Bale, T.L., Sex differences in prenatal epigenetic programming of stress pathways. Stress 14 (2011), 348–356.
15. Bale, T.L., Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci 16 (2015), 332–344.
16. Bale, T.L., Baram, T.Z., Brown, A.S., Goldstein, J.M., Insel, T.R., McCarthy, M.M., Nemeroff, C.B., Reyes, T.M., Simerly, R.B., Susser, E.S., Nestler, E.J., Early life programming and neurodevelopmental disorders. Biol Psychiatry 68 (2010), 314–319.
17. Barker, E.D., The duration and timing of maternal depression as a moderator of the relationship between dependent interpersonal stress, contextual risk and early child dysregulation. Psychol Med 43 (2013), 1587–1596.
18. Barker, E.D., Kirkham, N., Ng, J., Jensen, S.K., Prenatal maternal depression symptoms and nutrition, and child cognitive function. Br J Psychiatry 203 (2013), 417–421.
19. Barrett, E., Kerr, C., Murphy, K., O'Sullivan, O., Ryan, C.A., Dempsey, E.M., Murphy, B.P., O'Toole, P.W., Cotter, P.D., Fitzgerald, G.F., Ross, R.P., Stanton, C., The individual-specific and diverse nature of the preterm infant microbiota. Arch Dis Child Fetal Neonatal Ed 98 (2013), F334–F340.
20. Barrett, E., Ross, R.P., O'Toole, P.W., Fitzgerald, G.F., Stanton, C., Gamma-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 113 (2012), 411–417.
21. Barzegar, M., Sajjadi, F.S., Talaei, S.A., Hamidi, G., Salami, M., Prenatal exposure to noise stress: anxiety, impaired spatial memory, and deteriorated hippocampal plasticity in postnatal life. Hippocampus 25 (2015), 187–196.
22. Bevans, K., Cerbone, A., Overstreet, S., Relations between recurrent trauma exposure and recent life stress and salivary cortisol among children. Dev Psychopathol 20 (2008), 257–272.
23. Beversdorf, D.Q., Manning, S.E., Hillier, A., Anderson, S.L., Nordgren, R.E., Walters, S.E., Nagaraja, H.N., Cooley, W.C., Gaelic, S.E., Bauman, M.L., Timing of prenatal stressors and autism. J Autism Dev Disord 35 (2005), 471–478.
24. Biasucci, G., Benenati, B., Morelli, L., Bessi, E., Boehm, G., Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr 138 (2008), 1796S–1800S.
25. Bilbo, S.D., Biedenkapp, J.C., Der-Avakian, A., Watkins, L.R., Rudy, J.W., Maier, S.F., Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci 25 (2005), 8000–8009.
26. Bilder, D.A., Bakian, A.V., Viskochil, J., Clark, E.A., Botts, E.L., Smith, K.R., Pimentel, R., McMahon, W.M., Coon, H., Maternal prenatal weight gain and autism spectrum disorders. Pediatrics 132 (2013), e1276–e1283.
27. Blaser, M.J., Webb, G.F., Host demise as a beneficial function of indigenous microbiota in human hosts. mBio, 5(6), 2014.
28. Bonaz, B.L., Bernstein, C.N., Brain–gut interactions in inflammatory bowel disease. Gastroenterology 144 (2013), 36–49.
29. Borre YE, Golubeva AV, Crispie F, Scott KA, Hyland NP, Stanton C, Dinan TG, Cryan JF. Mode of delivery at birth and behavioural outcomes: Rewiring of the brain–gut-microbiome axis? In Society for Neuroscience (SFN) Neuroscience 2014, November 15–19, 2014a, Washington, USA.
30. Borre, Y.E., Moloney, R.D., Clarke, G., Dinan, T.G., Cryan, J.F., The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv Exp Med Biol 817 (2014), 373–403.
31. Borre, Y.E., O'Keeffe, G.W., Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F., Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med 20 (2014), 509–518.
32. Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Toth, M., Korecka, A., Bakocevic, N., Ng, L.G., Kundu, P., Gulyas, B., Halldin, C., Hultenby, K., Nilsson, H., Hebert, H., Volpe, B.T., Diamond, B., Pettersson, S., The gut microbiota influences blood–brain barrier permeability in mice. Sci Transl Med, 6, 2014, 263ra158.
33. Brown, A.S., Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol 72 (2012), 1272–1276.
34. Brown, A.S., Susser, E.S., Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull 34 (2008), 1054–1063.
35. Buka, S.L., Goldstein, J.M., Seidman, L.J., Tsuang, M.T., Maternal recall of pregnancy history: accuracy and bias in schizophrenia research. Schizophr Bull 26 (2000), 335–350.
36. Burokas, A., Moloney, R.D., Dinan, T.G., Cryan, J.F., Microbiota regulation of the Mammalian gut–brain axis. Adv Appl Microbiol 91 (2015), 1–62.
37. Buss, C., Davis, E.P., Shahbaba, B., Pruessner, J.C., Head, K., Sandman, C.A., Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci U S A 109 (2012), E1312–E1319.
38. Buss, C., Entringer, S., Davis, E.P., Hobel, C.J., Swanson, J.M., Wadhwa, P.D., Sandman, C.A., Impaired executive function mediates the association between maternal pre-pregnancy body mass index and child ADHD symptoms. PLoS One, 7, 2012, e37758.
39. Candon, S., Perez-Arroyo, A., Marquet, C., Valette, F., Foray, A.P., Pelletier, B., Milani, C., Ventura, M., Bach, J.F., Chatenoud, L., Antibiotics in early life alter the gut microbiome and increase disease incidence in a spontaneous mouse model of autoimmune insulin-dependent diabetes. PLoS One, 10, 2015, e0125448.
40. Capra, L., Tezza, G., Mazzei, F., Boner, A.L., The origins of health and disease: the influence of maternal diseases and lifestyle during gestation. Ital J Pediatr, 39, 2013, 7.
41. Carlson, M., Earls, F., Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Ann N Y Acad Sci 807 (1997), 419–428.
42. Carpenter, L.L., Tyrka, A.R., McDougle, C.J., Malison, R.T., Owens, M.J., Nemeroff, C.B., Price, L.H., Cerebrospinal fluid corticotropin-releasing factor and perceived early-life stress in depressed patients and healthy control subjects. Neuropsychopharmacology 29 (2004), 777–784.
43. Champagne, F., Diorio, J., Sharma, S., Meaney, M.J., Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98 (2001), 12736–12741.
44. Champagne, F., Meaney, M.J., Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133 (2001), 287–302.
45. Champagne, F.A., Meaney, M.J., Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121 (2007), 1353–1363.
46. Cheslack-Postava, K., Brown, A.S., Chudal, R., Suominen, A., Huttunen, J., Surcel, H.M., Sourander, A., Maternal exposure to sexually transmitted infections and schizophrenia among offspring. Schizophr Res 166:1–3 (2015), 255–260.
47. Cho, I., Blaser, M.J., The human microbiome: at the interface of health and disease. Nat Rev Genet 13 (2012), 260–270.
48. Chocyk, A., Majcher-Maslanka, I., Przyborowska, A., Mackowiak, M., Wedzony, K., Early-life stress increases the survival of midbrain neurons during postnatal development and enhances reward-related and anxiolytic-like behaviors in a sex-dependent fashion. Int J Dev Neurosci 44 (2015), 33–47.
49. Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R.D., Shanahan, F., Dinan, T.G., Cryan, J.F., The microbiome-gut–brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 18 (2013), 666–673.
50. Clarke, G., O'Mahony, S.M., Dinan, T.G., Cryan, J.F., Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr 103 (2014), 812–819.
51. Clarke, G., O'Toole, P.W., Dinan, T.G., Cryan, J.F., Characterizing the gut microbiome: role in brain-gut function. Coppola, G., (eds.) The OMICS: Applications in Neuroscience, 2014, Oxford University Press, Oxford, UK, 265–287.
52. Clarke, G., Quigley, E.M., Cryan, J.F., Dinan, T.G., Irritable bowel syndrome: towards biomarker identification. Trends Mol Med 15 (2009), 478–489.
53. Clayton, J.A., Collins, F.S., Policy: NIH to balance sex in cell and animal studies. Nature 509 (2014), 282–283.
54. Collins, S.M., A role for the gut microbiota in IBS. Nat Rev Gastroenterol Hepatol 11 (2014), 497–505.
55. Collins, S.M., Surette, M., Bercik, P., The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10 (2012), 735–742.
56. Copeland, W.E., Miller-Johnson, S., Keeler, G., Angold, A., Costello, E.J., Childhood psychiatric disorders and young adult crime: a prospective, population-based study. Am J Psychiatry 164 (2007), 1668–1675.
57. Costello, E.K., Stagaman, K., Dethlefsen, L., Bohannan, B.J., Relman, D.A., The application of ecological theory toward an understanding of the human microbiome. Science 336 (2012), 1255–1262.
58. Cryan, J.F., Dinan, T.G., Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13 (2012), 701–712.
59. Cryan, J.F., Holmes, A., The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4 (2005), 775–790.
60. Cryan, J.F., O'Mahony, S.M., The microbiome-gut–brain axis: from bowel to behavior. Neurogastroenterol Motil 23 (2011), 187–192.
61. Curran, E.A., O'Neill, S.M., Cryan, J.F., Kenny, L.C., Dinan, T.G., Khashan, A.S., Kearney, P.M., Research review: birth by caesarean section and development of autism spectrum disorder and attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. J Child Psychol Psychiatry 56 (2015), 500–508.
62. Darnaudery, M., Maccari, S., Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57 (2008), 571–585.
63. Davidson, R.J., McEwen, B.S., Social influences on neuroplasticity: stress and interventions to promote well-being. Nat Neurosci 15 (2012), 689–695.
64. Davis, E.P., Glynn, L.M., Schetter, C.D., Hobel, C., Chicz-Demet, A., Sandman, C.A., Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry 46 (2007), 737–746.
65. de Theije, C.G., Wopereis, H., Ramadan, M., van Eijndthoven, T., Lambert, J., Knol, J., Garssen, J., Kraneveld, A.D., Oozeer, R., Altered gut microbiota and activity in a murine model of autism spectrum disorders. Brain Behav Immun 37 (2014), 197–206.
66. de Theije, C.G., Wu, J., da Silva, S.L., Kamphuis, P.J., Garssen, J., Korte, S.M., Kraneveld, A.D., Pathways underlying the gut-to-brain connection in autism spectrum disorders as future targets for disease management. Eur J Pharmacol 668:Suppl. 1 (2011), S70–S80.
67. Debnath, M., Venkatasubramanian, G., Berk, M., Fetal programming of schizophrenia: select mechanisms. Neurosci Biobehav Rev 49 (2015), 90–104.
68. Desai, R.A., Manley, M., Desai, M.M., Potenza, M.N., Gender differences in the association between body mass index and psychopathology. CNS Spectr 14 (2009), 372–383.
69. Desbonnet, L., Clarke, G., Traplin, A., O'Sullivan, O., Crispie, F., Moloney, R.D., Cotter, P.D., Dinan, T.G., Cryan, J.F., Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour. Brain Behav Immun 48 (2015), 165–173.
70. Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J.F., Dinan, T.G., Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170 (2010), 1179–1188.
71. Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Bjorkholm, B., Samuelsson, A., Hibberd, M.L., Forssberg, H., Pettersson, S., Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 108 (2011), 3047–3052.
72. DiGiulio, D.B., Romero, R., Amogan, H.P., Kusanovic, J.P., Bik, E.M., Gotsch, F., Kim, C.J., Erez, O., Edwin, S., Relman, D.A., Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One, 3, 2008, e3056.
73. Dinan, T.G., Cryan, J.F., Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 37 (2012), 1369–1378.
74. Dinan, T.G., Stanton, C., Cryan, J.F., Psychobiotics: a novel class of psychotropic. Biol Psychiatry 74 (2013), 720–726.
75. Dinan, T.G., Stilling, R.M., Stanton, C., Cryan, J.F., Collective unconscious: how gut microbes shape human behavior. J Psychiatr Res 63 (2015), 1–9.
76. Dominguez-Bello, M.G., Costello, E.K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., Knight, R., Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107 (2010), 11971–11975.
77. El Aidy, S., Hooiveld, G., Tremaroli, V., Backhed, F., Kleerebezem, M., The gut microbiota and mucosal homeostasis: colonized at birth or at adulthood, does it matter?. Gut Microbes 4 (2013), 118–124.
78. Ellenbroek, B.A., van den Kroonenberg, P.T., Cools, A.R., The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 30 (1998), 251–260.
79. Erny, D., Hrabe de Angelis, A.L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermohlen, O., Chun, E., Garrett, W.S., McCoy, K.D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I., Prinz, M., Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18:7 (2015), 965–977.
80. Fairbanks, L.A., Early experience and cross-generational continuity of mother-infant contact in vervet monkeys. Dev Psychobiol 22 (1989), 669–681.
81. Fanaro, S., Chierici, R., Guerrini, P., Vigi, V., Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl 91 (2003), 48–55.
82. Fang, S.Y., Wang, S., Huang, N., Yeh, H.H., Chen, C.Y., Prenatal infection and autism spectrum disorders in childhood: a population-based case–control study in Taiwan. Paediatr Perinat Epidemiol 29:4 (2015), 307–316.
83. Farmer, A.D., Randall, H.A., Aziz, Q., It's a gut feeling: how the gut microbiota affects the state of mind. J Physiol 592 (2014), 2981–2988.
84. Felice, V.D., Gibney, S.M., Gosselin, R.D., Dinan, T.G., O'Mahony, S.M., Cryan, J.F., Differential activation of the prefrontal cortex and amygdala following psychological stress and colorectal distension in the maternally separated rat. Neuroscience 267 (2014), 252–262.
85. Fernandez, L., Langa, S., Martin, V., Maldonado, A., Jimenez, E., Martin, R., Rodriguez, J.M., The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 69 (2013), 1–10.
86. Finegold, S.M., Dowd, S.E., Gontcharova, V., Liu, C., Henley, K.E., Wolcott, R.D., Youn, E., Summanen, P.H., Granpeesheh, D., Dixon, D., Liu, M., Molitoris, D.R., Green Iii, J.A., Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 16 (2010), 444–453.
87. Flint, H.J., Scott, K.P., Louis, P., Duncan, S.H., The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9 (2012), 577–589.
88. Francis, D., Diorio, J., Liu, D., Meaney, M.J., Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286 (1999), 1155–1158.
89. Francis, D.D., Champagne, F.A., Liu, D., Meaney, M.J., Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann N Y Acad Sci 896 (1999), 66–84.
90. Francis, D.D., Meaney, M.J., Maternal care and the development of stress responses. Curr Opin Neurobiol 9 (1999), 128–134.
91. Fumagalli, F., Molteni, R., Racagni, G., Riva, M.A., Stress during development: Impact on neuroplasticity and relevance to psychopathology. Prog Neurobiol 81 (2007), 197–217.
92. Funkhouser, L.J., Bordenstein, S.R., Mom knows best: the universality of maternal microbial transmission. PLoS Biol, 11, 2013, e1001631.
93. Ganzel, B.L., Kim, P., Gilmore, H., Tottenham, N., Temple, E., Stress and the healthy adolescent brain: evidence for the neural embedding of life events. Dev Psychopathol 25 (2013), 879–889.
94. Glasson, E.J., Bower, C., Petterson, B., de Klerk, N., Chaney, G., Hallmayer, J.F., Perinatal factors and the development of autism: a population study. Arch Gen Psychiatry 61 (2004), 618–627.
95. Glynn, L.M., Wadhwa, P.D., Dunkel-Schetter, C., Chicz-Demet, A., Sandman, C.A., When stress happens matters: effects of earthquake timing on stress responsivity in pregnancy. Am J Obstet Gynecol 184 (2001), 637–642.
96. Goehler, L.E., Park, S.M., Opitz, N., Lyte, M., Gaykema, R.P., Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 22 (2008), 354–366.
97. Goldani, H.A., Bettiol, H., Barbieri, M.A., Silva, A.A., Agranonik, M., Morais, M.B., Goldani, M.Z., Cesarean delivery is associated with an increased risk of obesity in adulthood in a Brazilian birth cohort study. Am J Clin Nutr 93 (2011), 1344–1347.
98. Goldenberg, R.L., Hauth, J.C., Andrews, W.W., Intrauterine infection and preterm delivery. N Engl J Med 342 (2000), 1500–1507.
99. Goldstein, J.M., Seidman, L.J., Buka, S.L., Horton, N.J., Donatelli, J.L., Rieder, R.O., Tsuang, M.T., Impact of genetic vulnerability and hypoxia on overall intelligence by age 7 in offspring at high risk for schizophrenia compared with affective psychoses. Schizophr Bull 26 (2000), 323–334.
100. Golubeva, A.V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K.W., Zhdanov, A.V., Crispie, F., Moloney, R.D., Borre, Y.E., Cotter, P.D., Hyland, N.P., O'Halloran, K.D., Dinan, T.G., O'Keeffe, G.W., Cryan, J.F., Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood 60 (2015), 58–74.
101. Gondalia, S.V., Palombo, E.A., Knowles, S.R., Cox, S.B., Meyer, D., Austin, D.W., Molecular characterisation of gastrointestinal microbiota of children with autism (with and without gastrointestinal dysfunction) and their neurotypical siblings. Autism Res 5:6 (2012), 419–427.
102. Gonzalez, A., Jenkins, J.M., Steiner, M., Fleming, A.S., The relation between early life adversity, cortisol awakening response and diurnal salivary cortisol levels in postpartum women. Psychoneuroendocrinology 34 (2009), 76–86.
103. Grenham, S., Clarke, G., Cryan, J.F., Dinan, T.G., Brain–gut-microbe communication in health and disease. Front Physiol, 2, 2011, 94.
104. Guerri, C., Neuroanatomical and neurophysiological mechanisms involved in central nervous system dysfunctions induced by prenatal alcohol exposure. Alcohol Clin Exp Res 22 (1998), 304–312.
105. Gunnar, M.R., Integrating neuroscience and psychological approaches in the study of early experiences. Ann N Y Acad Sci 1008 (2003), 238–247.
106. Gunnar, M.R., Donzella, B., Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27 (2002), 199–220.
107. Harmsen, H.J., Wildeboer-Veloo, A.C., Raangs, G.C., Wagendorp, A.A., Klijn, N., Bindels, J.G., Welling, G.W., Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30 (2000), 61–67.
108. Harris, A., Endresen Reme, S., Tangen, T., Hansen, A.M., Helene Garde, A., Eriksen, H.R., Diurnal cortisol rhythm: associated with anxiety and depression, or just an indication of lack of energy?. Psychiatry Res 228:2 (2015), 209–215.
109. Heim, C., Binder, E.B., Current research trends in early life stress and depression: review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Exp Neurol 233 (2012), 102–111.
110. Heim, C., Newport, D.J., Miller, A.H., Nemeroff, C.B., Long-term neuroendocrine effects of childhood maltreatment. JAMA, 284, 2000, 2321.
111. Heim, C., Newport, D.J., Mletzko, T., Miller, A.H., Nemeroff, C.B., The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33 (2008), 693–710.
112. Heitkemper, M.M., Cain, K.C., Deechakawan, W., Poppe, A., Jun, S.E., Burr, R.L., Jarrett, M.E., Anticipation of public speaking and sleep and the hypothalamic–pituitary–adrenal axis in women with irritable bowel syndrome. Neurogastroenterol Motil 24 (2012), 626–631 e270–e621.
113. Herschkowitz, N., Kagan, J., Zilles, K., Neurobiological bases of behavioral development in the first year. Neuropediatrics 28 (1997), 296–306.
114. Hilimire, M.R., DeVylder, J.E., Forestell, C.A., Fermented foods, neuroticism, and social anxiety: an interaction model. Psychiatry Res 228 (2015), 203–208.
115. Holmes, A.J., Lee, P.H., Hollinshead, M.O., Bakst, L., Roffman, J.L., Smoller, J.W., Buckner, R.L., Individual differences in amygdala-medial prefrontal anatomy link negative affect, impaired social functioning, and polygenic depression risk. J Neurosci 32 (2012), 18087–18100.
116. Hornung, O.P., Heim, C.M., Gene-environment interactions and intermediate phenotypes: early trauma and depression. Front Endocrinol (Lausanne), 5, 2014, 14.
117. Horowitz, M.A., Zunszain, P.A., Neuroimmune and neuroendocrine abnormalities in depression: two sides of the same coin. Ann N Y Acad Sci 1351 (2015), 68–79.
118. Howerton, C.L., Bale, T.L., Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav 62 (2012), 237–242.
119. Hsiao, E.Y., McBride, S.W., Hsien, S., Sharon, G., Hyde, E.R., McCue, T., Codelli, J.A., Chow, J., Reisman, S.E., Petrosino, J.F., Patterson, P.H., Mazmanian, S.K., Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155 (2013), 1451–1463.
120. Huh, S.Y., Rifas-Shiman, S.L., Zera, C.A., Edwards, J.W., Oken, E., Weiss, S.T., Gillman, M.W., Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Arch Dis Child 97 (2012), 610–616.
121. Hunter, P., The changing hypothesis of the gut. The intestinal microbiome is increasingly seen as vital to human health. EMBO Rep 13 (2012), 498–500.
122. Huot, R.L., Gonzalez, M.E., Ladd, C.O., Thrivikraman, K.V., Plotsky, P.M., Foster litters prevent hypothalamic–pituitary–adrenal axis sensitization mediated by neonatal maternal separation. Psychoneuroendocrinology 29 (2004), 279–289.
123. Hussey, S., Wall, R., Gruffman, E., O'Sullivan, L., Ryan, C.A., Murphy, B., Fitzgerald, G., Stanton, C., Ross, R.P., Parenteral antibiotics reduce bifidobacteria colonization and diversity in neonates. Int J Microbiol, 2011, 2011, 10.1155/2011/130574.
124. Huttunen, M.O., Niskanen, P., Prenatal loss of father and psychiatric disorders. Arch Gen Psychiatry 35 (1978), 429–431.
125. Hyland, N.P., O'Mahony, S.M., O'Malley, D., O'Mahony, C.M., Dinan, T.G., Cryan, J.F., Early-life stress selectively affects gastrointestinal but not behavioral responses in a genetic model of brain-gut axis dysfunction. Neurogastroenterol Motil 27 (2015), 105–113.
126. Jakobsson, H.E., Abrahamsson, T.R., Jenmalm, M.C., Harris, K., Quince, C., Jernberg, C., Bjorksten, B., Engstrand, L., Andersson, A.F., Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by Caesarean section. Gut 63:4 (2014), 559–566.
127. Jasarevic, E., Howerton, C.L., Howard, C.D., Bale, T.L., Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology, 2015 en20151177.
128. Jasarevic, E., Rodgers, A.B., Bale, T.L., A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment. Neurobiol Stress 1 (2015), 81–88.
129. Jeffery, I.B., Quigley, E.M., Ohman, L., Simren, M., O'Toole, P.W., The microbiota link to irritable bowel syndrome: an emerging story. Gut Microbes 3 (2012), 572–576.
130. Jimenez, E., Delgado, S., Maldonado, A., Arroyo, R., Albujar, M., Garcia, N., Jariod, M., Fernandez, L., Gomez, A., Rodriguez, J.M., Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol, 8, 2008, 143.
131. Jimenez, E., Marin, M.L., Martin, R., Odriozola, J.M., Olivares, M., Xaus, J., Fernandez, L., Rodriguez, J.M., Is meconium from healthy newborns actually sterile?. Res Microbiol 159 (2008), 187–193.
132. Jimenez, E., Villar-Tajadura, M.A., Marin, M., Fontecha, J., Requena, T., Arroyo, R., Fernandez, L., Rodriguez, J.M., Complete genome sequence of Bifidobacterium breve CECT 7263, a strain isolated from human milk. J Bacteriol 194 (2012), 3762–3763.
133. Jo, H., Schieve, L.A., Sharma, A.J., Hinkle, S.N., Li, R., Lind, J.N., Maternal prepregnancy body mass index and child psychosocial development at 6 years of age. Pediatrics 135 (2015), e1198–e1209.
134. Johnson, C.L., Versalovic, J., The human microbiome and its potential importance to pediatrics. Pediatrics 129 (2012), 950–960.
135. Kaplow, J.B., Widom, C.S., Age of onset of child maltreatment predicts long-term mental health outcomes. J Abnorm Psychol 116 (2007), 176–187.
136. Kapoor, A., Kostaki, A., Janus, C., Matthews, S.G., The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor. Behav Brain Res 197 (2009), 144–149.
137. Kapoor, A., Matthews, S.G., Short periods of prenatal stress affect growth, behaviour and hypothalamo–pituitary–adrenal axis activity in male guinea pig offspring. J Physiol 566 (2005), 967–977.
138. Kennedy, P.J., Cryan, J.F., Dinan, T.G., Clarke, G., Irritable bowel syndrome: a microbiome-gut–brain axis disorder?. World J Gastroenterol 20 (2014), 14105–14125.
139. Kennedy, P.J., Cryan, J.F., Quigley, E.M., Dinan, T.G., Clarke, G., A sustained hypothalamic–pituitary–adrenal axis response to acute psychosocial stress in irritable bowel syndrome. Psychol Med 44 (2014), 3123–3134.
140. Khandaker, G.M., Zimbron, J., Lewis, G., Jones, P.B., Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies. Psychol Med 43 (2013), 239–257.
141. Khashan, A.S., Abel, K.M., McNamee, R., Pedersen, M.G., Webb, R.T., Baker, P.N., Kenny, L.C., Mortensen, P.B., Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65 (2008), 146–152.
142. Khashan, A.S., Kenny, L.C., The effects of maternal body mass index on pregnancy outcome. Eur J Epidemiol 24 (2009), 697–705.
143. Kim, D.R., Bale, T.L., Epperson, C.N., Prenatal programming of mental illness: current understanding of relationship and mechanisms. Curr Psychiatry Rep, 17, 2015, 5.
144. King, S., Laplante, D.P., The effects of prenatal maternal stress on children's cognitive development: project ice storm. Stress 8 (2005), 35–45.
145. King, S., Mancini-Marie, A., Brunet, A., Walker, E., Meaney, M.J., Laplante, D.P., Prenatal maternal stress from a natural disaster predicts dermatoglyphic asymmetry in humans. Dev Psychopathol 21 (2009), 343–353.
146. Kinney, D.K., Miller, A.M., Crowley, D.J., Huang, E., Gerber, E., Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J Autism Dev Disord 38 (2008), 481–488.
147. Kinney, D.K., Munir, K.M., Crowley, D.J., Miller, A.M., Prenatal stress and risk for autism. Neurosci Biobehav Rev 32 (2008), 1519–1532.
148. Kocak, H., Ballew, B.J., Bisht, K., Eggebeen, R., Hicks, B.D., Suman, S., O'Neil, A., Giri, N., Maillard, I., Alter, B.P., Keegan, C.E., Nandakumar, J., Savage, S.A., Hoyeraal-Hreidarsson syndrome caused by a germline mutation in the TEL patch of the telomere protein TPP1. Genes Dev 28 (2014), 2090–2102.
149. Koenig, J.I., Elmer, G.I., Shepard, P.D., Lee, P.R., Mayo, C., Joy, B., Hercher, E., Brady, D.L., Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav Brain Res 156 (2005), 251–261.
150. Koren, O., Goodrich, J.K., Cullender, T.C., Spor, A., Laitinen, K., Backhed, H.K., Gonzalez, A., Werner, J.J., Angenent, L.T., Knight, R., Backhed, F., Isolauri, E., Salminen, S., Ley, R.E., Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150 (2012), 470–480.
151. Korosi, A., Baram, T.Z., The pathways from mother's love to baby's future. Front Behav Neurosci, 3, 2009, 27.
152. Ladd, C.O., Huot, R.L., Thrivikraman, K.V., Nemeroff, C.B., Plotsky, P.M., Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo–pituitary–adrenal axis following neonatal maternal separation. Biol Psychiatry 55 (2004), 367–375.
153. Lee, R.J., Gollan, J., Kasckow, J., Geracioti, T., Coccaro, E.F., CSF corticotropin-releasing factor in personality disorder: relationship with self-reported parental care. Neuropsychopharmacology 31 (2006), 2289–2295.
154. Lehmann, J., Pryce, C.R., Bettschen, D., Feldon, J., The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 64 (1999), 705–715.
155. Lemaire, V., Koehl, M., Le Moal, M., Abrous, D.N., Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 97 (2000), 11032–11037.
156. Levine, S., The ontogeny of the hypothalamic–pituitary–adrenal axis. The influence of maternal factors. Ann N Y Acad Sci 746 (1994), 275–288 Discussion 289–293.
157. Levine, S., Alpert, M., Lewis, G.W., Infantile experience and the maturation of the pituitary adrenal axis. Science, 126, 1957, 1347.
158. Levine, S.Z., Levav, I., Yoffe, R., Pugachova, I., The effects of pre-natal-, early-life- and indirectly-initiated exposures to maximum adversities on the course of schizophrenia. Schizophr Res 158 (2014), 236–240.
159. Li, J., Vestergaard, M., Obel, C., Christensen, J., Precht, D.H., Lu, M., Olsen, J., A nationwide study on the risk of autism after prenatal stress exposure to maternal bereavement. Pediatrics 123 (2009), 1102–1107.
160. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P.M., Meaney, M.J., Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science 277 (1997), 1659–1662.
161. Loman, M.M., Gunnar, M.R., Early experience and the development of stress reactivity and regulation in children. Neurosci Biobehav Rev 34 (2010), 867–876.
162. Lucassen, P.J., Naninck, E.F., van Goudoever, J.B., Fitzsimons, C., Joels, M., Korosi, A., Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci 36 (2013), 621–631.
163. Lucassen, P.J., Pruessner, J., Sousa, N., Almeida, O.F., Van Dam, A.M., Rajkowska, G., Swaab, D.F., Czeh, B., Neuropathology of stress. Acta Neuropathol 127 (2014), 109–135.
164. Lundy, B., Field, T., Pickens, J., Newborns of mothers with depressive symptoms are less expressive. Infant Behav Dev 19 (1996), 419–424.
165. Lupien, S.J., King, S., Meaney, M.J., McEwen, B.S., Child's stress hormone levels correlate with mother's socioeconomic status and depressive state. Biol Psychiatry 48 (2000), 976–980.
166. Lupien, S.J., McEwen, B.S., Gunnar, M.R., Heim, C., Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10 (2009), 434–445.
167. Lupien, S.J., McEwen, B.S., Gunnar, M.R., Heim, C., Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10 (2009), 434–445.
168. Lupien, S.J., Parent, S., Evans, A.C., Tremblay, R.E., Zelazo, P.D., Corbo, V., Pruessner, J.C., Seguin, J.R., Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proc Natl Acad Sci U S A 108 (2011), 14324–14329.
169. Lupp, C., Skipper, M., Weiss, U., Gut microbes and health. Nature, 489, 2012, 219.
170. Maccari, S., Piazza, P.V., Kabbaj, M., Barbazanges, A., Simon, H., Le Moal, M., Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15 (1995), 110–116.
171. MacQueen, G.M., Ramakrishnan, K., Ratnasingan, R., Chen, B., Young, L.T., Desipramine treatment reduces the long-term behavioural and neurochemical sequelae of early-life maternal separation. Int J Neuropsychopharmacol 6 (2003), 391–396.
172. Maestripieri, D., Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc Natl Acad Sci U S A 102 (2005), 9726–9729.
173. Majumdar, A.P., Nielsen, H., Influence of glucocorticoids on prenatal development of the gut and pancreas in rats. Scand J Gastroenterol 20 (1985), 65–71.
174. Markham, J.A., Koenig, J.I., Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology 214 (2011), 89–106.
175. Marques, T.M., Wall, R., Ross, R.P., Fitzgerald, G.F., Ryan, C.A., Stanton, C., Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opin Biotechnol 21 (2010), 149–156.
176. Mars, B., Collishaw, S., Hammerton, G., Rice, F., Harold, G.T., Smith, D., Bevan Jones, R., Sellers, R., Potter, R., Craddock, N., Thapar, A.K., Heron, J., Thapar, A., Longitudinal symptom course in adults with recurrent depression: impact on impairment and risk of psychopathology in offspring. J Affect Disord 182 (2015), 32–38.
177. Mayer, E., Tillisch, K., Bradesi, S., Review article: modulation of the brain–gut axis as a therapeutic approach in gastrointestinal disease. Aliment Pharmacol Ther 24 (2006), 919–933.
178. Mayer, E.A., Knight, R., Mazmanian, S.K., Cryan, J.F., Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci 34 (2014), 15490–15496.
179. Mazina, V., Gerdts, J., Trinh, S., Ankenman, K., Ward, T., Dennis, M.Y., Girirajan, S., Eichler, E.E., Bernier, R., Epigenetics of autism-related impairment: copy number variation and maternal infection. J Dev Behav Pediatr 36 (2015), 61–67.
180. McCrory, E., De Brito, S.A., Viding, E., Research review: the neurobiology and genetics of maltreatment and adversity. J Child Psychol Psychiatry 51 (2010), 1079–1095.
181. McLaughlin, K.A., Green, J.G., Gruber, M.J., Sampson, N.A., Zaslavsky, A.M., Kessler, R.C., Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: associations with persistence of DSM-IV disorders. Arch Gen Psychiatry 67 (2010), 124–132.
182. McPeake, J.M., Shaw, M., O'Neill, A., Forrest, E., Puxty, A., Quasim, T., Kinsella, J., Do alcohol use disorders impact on long term outcomes from intensive care?. Crit Care, 19, 2015, 185.
183. Meaney, M.J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J.R., Plotsky, P.M., Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18 (1996), 49–72.
184. Meinlschmidt, G., Heim, C., Decreased cortisol awakening response after early loss experience. Psychoneuroendocrinology 30 (2005), 568–576.
185. Mesquita, D.N., Barbieri, M.A., Goldani, H.A., Cardoso, V.C., Goldani, M.Z., Kac, G., Silva, A.A., Bettiol, H., Cesarean section is associated with increased peripheral and central adiposity in young adulthood: cohort study. PLoS One, 8, 2013, e66827.
186. Meyer, J.S., Early adrenalectomy stimulates subsequent growth and development of the rat brain. Exp Neurol 82 (1983), 432–446.
187. Meyer, U., Feldon, J., Dammann, O., Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation?. Pediatr Res 69 (2011), 26R–33R.
188. Mian, A.I., Depression in pregnancy and the postpartum period: balancing adverse effects of untreated illness with treatment risks. J Psychiatr Pract 11 (2005), 389–396.
189. Microbiology AAo (2014) The Human Microbiome. http://academy.asm.org/.
190. Mischke, M., Plosch, T., More than just a gut instinct-the potential interplay between a baby's nutrition, its gut microbiome, and the epigenome. Am J Physiol Regul Integr Comp Physiol 304 (2013), R1065–R1069.
191. Moloney, R.D., Desbonnet, L., Clarke, G., Dinan, T.G., Cryan, J.F., The microbiome: stress, health and disease. Mamm Genome 25:1–2 (2014), 49–74.
192. Moloney, R.D., O'Leary, O.F., Felice, D., Bettler, B., Dinan, T.G., Cryan, J.F., Early-life stress induces visceral hypersensitivity in mice. Neurosci Lett 512 (2012), 99–102.
193. Morgan, X.C., Segata, N., Huttenhower, C., Biodiversity and functional genomics in the human microbiome. Trends Genet 29:1 (2013), 51–58.
194. Morley-Fletcher, S., Darnaudery, M., Koehl, M., Casolini, P., Van Reeth, O., Maccari, S., Prenatal stress in rats predicts immobility behavior in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res 989 (2003), 246–251.
195. Mshvildadze, M., Neu, J., The infant intestinal microbiome: friend or foe?. Early Hum Dev 86:Suppl. 1 (2010), 67–71.
196. Mueller, B.R., Bale, T.L., Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity. Physiol Behav 88 (2006), 605–614.
197. Mueller, B.R., Bale, T.L., Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav 91 (2007), 55–65.
198. Mueller, B.R., Bale, T.L., Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28 (2008), 9055–9065.
199. Mueller, N.T., Bakacs, E., Combellick, J., Grigoryan, Z., Dominguez-Bello, M.G., The infant microbiome development: mom matters. Trends Mol Med 21 (2015), 109–117.
200. Mueller, N.T., Whyatt, R., Hoepner, L., Oberfield, S., Dominguez-Bello, M.G., Widen, E.M., Hassoun, A., Perera, F., Rundle, A., Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes (Lond) 39 (2015), 665–670.
201. Mulle, J.G., Sharp, W.G., Cubells, J.F., The gut microbiome: a new frontier in autism research. Curr Psychiatry Rep, 15, 2013, 337.
202. Myhrman, A., Rantakallio, P., Isohanni, M., Jones, P., Partanen, U., Unwantedness of a pregnancy and schizophrenia in the child. Br J Psychiatry 169 (1996), 637–640.
203. Naughton, M., Dinan, T.G., Scott, L.V., Corticotropin-releasing hormone and the hypothalamic–pituitary–adrenal axis in psychiatric disease. Handb Clin Neurol 124 (2014), 69–91.
204. Nguyen, T.L., Vieira-Silva, S., Liston, A., Raes, J., How informative is the mouse for human gut microbiota research?. Dis Model Mech 8 (2015), 1–16.
205. O'Connor, R.M., Cryan, J.F., Adolescent brain vulnerability and psychopathology through the generations: role of diet and dopamine. Biol Psychiatry 75 (2014), 4–6.
206. O'Donnell, K.J., Glover, V., Barker, E.D., O'Connor, T.G., The persisting effect of maternal mood in pregnancy on childhood psychopathology. Dev Psychopathol 26 (2014), 393–403.
207. O'Hare, F.M., Watson, R.W., O'Neill, A., Blanco, A., Donoghue, V., Molloy, E.J., Persistent systemic monocyte and neutrophil activation in neonatal encephalopathy. J Matern Fetal Neonatal Med, 2015, 1–8.
208. O'Leary, O.F., Cryan, J.F., Towards translational rodent models of depression. Cell Tissue Res 354 (2013), 141–153.
209. O'Mahony, S.M., Clarke, G., Borre, Y.E., Dinan, T.G., Cryan, J.F., Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 277 (2015), 32–48.
210. O'Mahony, S.M., Felice, V.D., Nally, K., Savignac, H.M., Claesson, M.J., Scully, P., Woznicki, J., Hyland, N.P., Shanahan, F., Quigley, E.M., Marchesi, J.R., O'Toole, P.W., Dinan, T.G., Cryan, J.F., Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats. Neuroscience 277 (2014), 885–901.
211. O'Mahony, S.M., Marchesi, J.R., Scully, P., Codling, C., Ceolho, A.M., Quigley, E.M., Cryan, J.F., Dinan, T.G., Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65 (2009), 263–267.
212. O'Mahony, S.M., Myint, A.M., van den Hove, D., Desbonnet, L., Steinbusch, H., Leonard, B.E., Gestational stress leads to depressive-like behavioural and immunological changes in the rat. Neuroimmunomodulation 13 (2006), 82–88.
213. O'Malley, D., Dinan, T.G., Cryan, J.F., Neonatal maternal separation in the rat impacts on the stress responsivity of central corticotropin-releasing factor receptors in adulthood. Psychopharmacology 214 (2011), 221–229.
214. O'Neil, A., Itsiopoulos, C., Skouteris, H., Opie, R.S., McPhie, S., Hill, B., Jacka, F.N., Preventing mental health problems in offspring by targeting dietary intake of pregnant women. BMC Med, 12, 2014, 208.
215. O'Neil, A., Quirk, S.E., Housden, S., Brennan, S.L., Williams, L.J., Pasco, J.A., Berk, M., Jacka, F.N., Relationship between diet and mental health in children and adolescents: a systematic review. Am J Public Health 104 (2014), e31–e42.
216. O'Connor, R.M., Pusceddu, M.M., Dinan, T.G., Cryan, J.F., Impact of early-life stress, on group III mGlu receptor levels in the rat hippocampus: effects of ketamine, electroconvulsive shock therapy and fluoxetine treatment. Neuropharmacology 66 (2013), 236–241.
217. Ogbonnaya, E.S., Clarke, G., Shanahan, F., Dinan, T.G., Cryan, J.F., O'Leary, O.F., Adult hippocampal neurogenesis is regulated by the microbiome. Biol Psychiatry 78:4 (2015), e7–e9.
218. Paksarian, D., Eaton, W.W., Mortensen, P.B., Merikangas, K.R., Pedersen, C.B., A population-based study of the risk of schizophrenia and bipolar disorder associated with parent-child separation during development. Psychol Med, 2015, 1–13.
219. Parfrey, L.W., Knight, R., Spatial and temporal variability of the human microbiota. Clin Microbiol Infect 18:Suppl. 4 (2012), 8–11.
220. Pawlby, S., Hay, D.F., Sharp, D., Waters, C.S., O'Keane, V., Antenatal depression predicts depression in adolescent offspring: prospective longitudinal community-based study. J Affect Disord 113 (2009), 236–243.
221. Pearson, R.M., Evans, J., Kounali, D., Lewis, G., Heron, J., Ramchandani, P.G., O'Connor, T.G., Stein, A., Maternal depression during pregnancy and the postnatal period: risks and possible mechanisms for offspring depression at age 18 years. JAMA Psychiatry 70 (2013), 1312–1319.
222. Pechtel, P., Pizzagalli, D.A., Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 214 (2011), 55–70.
223. Penders, J., Thijs, C., Vink, C., Stelma, F.F., Snijders, B., Kummeling, I., van den Brandt, P.A., Stobberingh, E.E., Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118 (2006), 511–521.
224. Petanjek, Z., Judas, M., Simic, G., Rasin, M.R., Uylings, H.B., Rakic, P., Kostovic, I., Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A 108 (2011), 13281–13286.
225. Pitter, G., Ludvigsson, J.F., Romor, P., Zanier, L., Zanotti, R., Simonato, L., Canova, C., Antibiotic exposure in the first year of life and later treated asthma, a population based birth cohort study of 143,000 children. Eur J Epidemiol, 2015 [Epub ahead of print].
226. Plotsky, P.M., Meaney, M.J., Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18 (1993), 195–200.
227. Pusceddu, M.M., Kelly, P., Ariffin, N., Cryan, J.F., Clarke, G., Dinan, T.G., N-3 PUFAs have beneficial effects on anxiety and cognition in female rats: effects of early life stress. Psychoneuroendocrinology 58 (2015), 79–90.
228. Pynoos, R.S., Steinberg, A.M., Piacentini, J.C., A developmental psychopathology model of childhood traumatic stress and intersection with anxiety disorders. Biol Psychiatry 46 (1999), 1542–1554.
229. Qiu, A., Anh, T.T., Li, Y., Chen, H., Rifkin-Graboi, A., Broekman, B.F., Kwek, K., Saw, S.M., Chong, Y.S., Gluckman, P.D., Fortier, M.V., Meaney, M.J., Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants. Transl Psychiatry, 5, 2015, e508.
230. Randall, C.P., Gupta, A., Jackson, N., Busse, D., O'Neill, A.J., Silver resistance in Gram-negative bacteria: a dissection of endogenous and exogenous mechanisms. J Antimicrob Chemother 70 (2015), 1037–1046.
231. Ravelli, G.P., Stein, Z.A., Susser, M.W., Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295 (1976), 349–353.
232. Relman, D.A., The human microbiome: ecosystem resilience and health. Nutr Rev 70:Suppl. 1 (2012), S2–S9.
233. Reynolds, L.C., Inder, T.E., Neil, J.J., Pineda, R.G., Rogers, C.E., Maternal obesity and increased risk for autism and developmental delay among very preterm infants. J Perinatol 34 (2014), 688–692.
234. Rice, D., Barone, S. Jr., Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108:Suppl. 3 (2000), 511–533.
235. Rice, F., Jones, I., Thapar, A., The impact of gestational stress and prenatal growth on emotional problems in offspring: a review. Acta Psychiatr Scand 115 (2007), 171–183.
236. Ridaura, V., Belkaid, Y., Gut microbiota: the link to your second brain. Cell 161 (2015), 193–194.
237. Rizzo, T.A., Silverman, B.L., Metzger, B.E., Cho, N.H., Behavioral adjustment in children of diabetic mothers. Acta Paediatr 86 (1997), 969–974.
238. Rodriguez, A., Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. J Child Psychol Psychiatry 51 (2010), 134–143.
239. Rodriguez, J.M., Murphy, K., Stanton, C., Ross, R.P., Kober, O.I., Juge, N., Avershina, E., Rudi, K., Narbad, A., Jenmalm, M.C., Marchesi, J.R., Collado, M.C., The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis, 26, 2015, 26050.
240. Rofey, D.L., Kolko, R.P., Iosif, A.M., Silk, J.S., Bost, J.E., Feng, W., Szigethy, E.M., Noll, R.B., Ryan, N.D., Dahl, R.E., A longitudinal study of childhood depression and anxiety in relation to weight gain. Child Psychiatry Hum Dev 40 (2009), 517–526.
241. Romeo, R.D., The teenage brain: the stress response and the adolescent brain. Curr Dir Psychol Sci 22 (2013), 140–145.
242. Romero, R., Hassan, S.S., Gajer, P., Tarca, A.L., Fadrosh, D.W., Bieda, J., Chaemsaithong, P., Miranda, J., Chaiworapongsa, T., Ravel, J., The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome, 2, 2014, 18.
243. Roth, T.L., Lubin, F.D., Funk, A.J., Sweatt, J.D., Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 65 (2009), 760–769.
244. Round, J.L., Mazmanian, S.K., The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9 (2009), 313–323.
245. Saari, A., Virta, L.J., Sankilampi, U., Dunkel, L., Saxen, H., Antibiotic exposure in infancy and risk of being overweight in the first 24 months of life. Pediatrics 135 (2015), 617–626.
246. Saavedra, J.M., Use of probiotics in pediatrics: rationale, mechanisms of action, and practical aspects. Nutr Clin Pract 22 (2007), 351–365.
247. Salazar, N., Arboleya, S., Valdes, L., Stanton, C., Ross, P., Ruiz, L., Gueimonde, M., de Los Reyes-Gavilan, C.G., The human intestinal microbiome at extreme ages of life. Dietary intervention as a way to counteract alterations. Front Genet, 5, 2014, 406.
248. Sampson, T.R., Mazmanian, S.K., Control of brain development, function, and behavior by the microbiome. Cell Host Microbe 17 (2015), 565–576.
249. Satokari, R., Gronroos, T., Laitinen, K., Salminen, S., Isolauri, E., Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 48 (2009), 8–12.
250. Schéle, E., Grahnemo, L., Anesten, F., Hallen, A., Backhed, F., Jansson, J.O., Regulation of body fat mass by the gut microbiota: possible mediation by the brain. Peptides, 2015, 10.1016/j.peptides.2015.03.027.
251. Schellekens, H., Finger, B.C., Dinan, T.G., Cryan, J.F., Ghrelin signalling and obesity: at the interface of stress, mood and food reward. Pharmacol Ther 135 (2012), 316–326.
252. Schmidt, K., Cowen, P.J., Harmer, C.J., Tzortzis, G., Errington, S., Burnet, P.W., Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology 232 (2015), 1793–1801.
253. Schneider, M.L., Moore, C.F., Kraemer, G.W., Roberts, A.D., DeJesus, O.T., The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 27 (2002), 285–298.
254. Scott, L.V., Dinan, T.G., Vasopressin and the regulation of hypothalamic–pituitary–adrenal axis function: implications for the pathophysiology of depression. Life Sci 62 (1998), 1985–1998.
255. Selevan, S.G., Kimmel, C.A., Mendola, P., Identifying critical windows of exposure for children's health. Environ Health Perspect 108:Suppl. 3 (2000), 451–455.
256. Shaw, S.Y., Blanchard, J.F., Bernstein, C.N., Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol 105 (2010), 2687–2692.
257. Siegel, L.S., Correction for prematurity and its consequences for the assessment of the very low birth weight infant. Child Dev 54 (1983), 1176–1188.
258. Silva, P.A., McGee, R., Williams, S., A longitudinal study of the intelligence and behavior of preterm and small for gestational age children. J Dev Behav Pediatr 5 (1984), 1–5.
259. Sirimi, N., Goulis, D.G., Obesity in pregnancy. Hormones 9 (2010), 299–306.
260. Slattery, D.A., Cryan, J.F., The ups and downs of modelling mood disorders in rodents. ILAR J 55 (2014), 297–309.
261. Smythe, J.W., Rowe, W.B., Meaney, M.J., Neonatal handling alters serotonin (5-HT) turnover and 5-HT2 receptor binding in selected brain regions: relationship to the handling effect on glucocorticoid receptor expression. Brain Res Dev Brain Res 80 (1994), 183–189.
262. Sohr-Preston, S.L., Scaramella, L.V., Implications of timing of maternal depressive symptoms for early cognitive and language development. Clin Child Fam Psychol Rev 9 (2006), 65–83.
263. Sowa, J., Bobula, B., Glombik, K., Slusarczyk, J., Basta-Kaim, A., Hess, G., Prenatal stress enhances excitatory synaptic transmission and impairs long-term potentiation in the frontal cortex of adult offspring rats. PLoS One, 10, 2015, e0119407.
264. Spiller, R., Garsed, K., Postinfectious irritable bowel syndrome. Gastroenterology 136 (2009), 1979–1988.
265. Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J.A., Colzato, L.S., A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav Immun 48 (2015), 258–264.
266. Stetler, C., Miller, G.E., Depression and hypothalamic–pituitary–adrenal activation: a quantitative summary of four decades of research. Psychosom Med 73 (2011), 114–126.
267. Stilling, R.M., Bordenstein, S.R., Dinan, T.G., Cryan, J.F., Friends with social benefits: host-microbe interactions as a driver of brain evolution and development?. Front Cell Infect Microbiol, 4, 2014, 147.
268. Stilling, R.M., Dinan, T.G., Cryan, J.F., The brain's Geppetto-microbes as puppeteers of neural function and behaviour?. J Neurovirol, 2015 [Epub ahead of print].
269. Struber, N., Struber, D., Roth, G., Impact of early adversity on glucocorticoid regulation and later mental disorders. Neurosci Biobehav Rev 38 (2014), 17–37.
270. Sullivan, E.L., Riper, K.M., Lockard, R., Valleau, J.C., Maternal high-fat diet programming of the neuroendocrine system and behavior. Horm Behav, 2015, 10.1016/j.yhbeh.2015.04.008.
271. Suren, P., Gunnes, N., Roth, C., Bresnahan, M., Hornig, M., Hirtz, D., Lie, K.K., Lipkin, W.I., Magnus, P., Reichborn-Kjennerud, T., Schjolberg, S., Susser, E., Oyen, A.S., Smith, G.D., Stoltenberg, C., Parental obesity and risk of autism spectrum disorder. Pediatrics 133 (2014), e1128–e1138.
272. Susser, E., St Clair, D., He, L., Latent effects of prenatal malnutrition on adult health: the example of schizophrenia. Ann N Y Acad Sci 1136 (2008), 185–192.
273. Tannock, G.W., Savage, D.C., Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun 9 (1974), 591–598.
274. Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain-Raspaud, S., Trotin, B., Naliboff, B., Mayer, E.A., Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144 (2013), 1394–1401 1401, e1391–e1394.
275. Tougas, G., The autonomic nervous system in functional bowel disorders. Gut 47:Suppl. 4 (2000), iv78–iv80 Discussion iv87.
276. Vaishampayan, P.A., Kuehl, J.V., Froula, J.L., Morgan, J.L., Ochman, H., Francino, M.P., Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2 (2010), 53–66.
277. Van Lieshout, R.J., Taylor, V.H., Boyle, M.H., Pre-pregnancy and pregnancy obesity and neurodevelopmental outcomes in offspring: a systematic review. Obes Rev 12 (2011), e548–e559.
278. van Os, J., Selten, J.P., Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br J Psychiatry 172 (1998), 324–326.
279. Vangay, P., Ward, T., Gerber, J.S., Knights, D., Antibiotics, pediatric dysbiosis, and disease. Cell Host Microbe 17 (2015), 553–564.
280. Wang, M., Radlowski, E.C., Monaco, M.H., Fahey, G.C. Jr., Gaskins, H.R., Donovan, S.M., Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. J Nutr 143 (2013), 795–803.
281. Weaver, S.A., Aherne, F.X., Meaney, M.J., Schaefer, A.L., Dixon, W.T., Neonatal handling permanently alters hypothalamic–pituitary–adrenal axis function, behaviour, and body weight in boars. J Endocrinol 164 (2000), 349–359.
282. Weinstock, M., The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32 (2008), 1073–1086.
283. Wichers, M., Geschwind, N., Jacobs, N., Kenis, G., Peeters, F., Derom, C., Thiery, E., Delespaul, P., van Os, J., Transition from stress sensitivity to a depressive state: longitudinal twin study. Br J Psychiatry 195 (2009), 498–503.
284. Widom, C.S., White, H.R., Czaja, S.J., Marmorstein, N.R., Long-term effects of child abuse and neglect on alcohol use and excessive drinking in middle adulthood. J Stud Alcohol Drugs 68 (2007), 317–326.
285. Williams, S.C., Gnotobiotics. Proc Natl Acad Sci U S A, 111, 2014, 1661.
286. Workman, A.D., Charvet, C.J., Clancy, B., Darlington, R.B., Finlay, B.L., Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci 33 (2013), 7368–7383.
287. Xu, M.Q., Sun, W.S., Liu, B.X., Feng, G.Y., Yu, L., Yang, L., He, G., Sham, P., Susser, E., St Clair, D., He, L., Prenatal malnutrition and adult schizophrenia: further evidence from the 1959–1961 Chinese famine. Schizophr Bull 35 (2009), 568–576.
288. Yang, J., Hou, C., Ma, N., Liu, J., Zhang, Y., Zhou, J., Xu, L., Li, L., Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiol Learn Mem 87 (2007), 257–263.
289. Yoshioka, H., Iseki, K., Fujita, K., Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 72 (1983), 317–321.
290. Zanobio, B., “The Work of Camillo Golgi in Neurology,” in Essays on the History of Italian Neurology. Proceedings of the International Symposium on the History of Neurology. Varenna—30. VIII/IX. 1961, 1963, Milan, 179–193.
291. Zhang, D., Huang, Y., Ye, D., Intestinal dysbiosis: an emerging cause of pregnancy complications?. Med Hypotheses 84 (2015), 223–226.
292. Zhou, L., Foster, J.A., Psychobiotics and the gut–brain axis: in the pursuit of happiness. Neuropsychiatr Dis Treat 11 (2015), 715–723.
293. Zijlmans, M.A., Korpela, K., Riksen-Walraven, J.M., de Vos, W.M., de Weerth, C., Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology 53 (2015), 233–245.
294. Zivkovic, A.M., German, J.B., Lebrilla, C.B., Mills, D.A., Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci U SA 108:Suppl. 1 (2011), 4653–4658.