{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T14:50:12Z","timestamp":1788274212533,"version":"build-2803163510"},"reference-count":106,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,4,8]],"date-time":"2022-04-08T00:00:00Z","timestamp":1649376000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000199","name":"United States Department of Agriculture","doi-asserted-by":"publisher","award":["2017-67015-26567"],"award-info":[{"award-number":["2017-67015-26567"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Tryptophan, as the sole precursor of serotonin, mainly derived from diets, is essential for neurodevelopment and immunomodulation. Gestational tryptophan fluctuation may account for the maternal-fetal transmission in determining neuroembryogenesis with long-lasting effects on psychological development. Personality disorders and social exclusion are related to psychosocial problems, leading to impaired social functioning. However, it is not clear how the fluctuation in mother-child transmission regulates the neuroendocrine development and gut microbiota composition in progeny due to that tryptophan metabolism in pregnant women is affected by multiple factors, such as diets (tryptophan-enriched or -depleted diet), emotional mental states (anxiety, depression), health status (hypertension, diabetes), and social support as well as stresses and management skills. Recently, we have developed a non-mammal model to rationalize those discrepancies without maternal effects. This perspective article outlines the possibility and verified the hypothesis in bully-victim research with this novel model: (1). Summarizes the effects of the maternal tryptophan administration on the neuroendocrine and microbial development in their offspring; (2). Highlights the inconsistency and limitations in studying the relationship between gestational tryptophan exposure and psychosocial development in humans and viviparous animals; and (3). Evidences that embryonic exposure to tryptophan and its metabolite modify bullying interactions in the chicken model. With the current pioneer researches on the biomechanisms underlying the bully-victim interaction, the perspective article provides novel insights for developing appropriate intervention strategies to prevent psychological disorders among individuals, especially those who experienced prenatal stress, by controlling dietary tryptophan and medication therapy during pregnancy.<\/jats:p>","DOI":"10.3390\/cells11081270","type":"journal-article","created":{"date-parts":[[2022,4,8]],"date-time":"2022-04-08T12:11:14Z","timestamp":1649419874000},"page":"1270","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Perspective: Gestational Tryptophan Fluctuation Altering Neuroembryogenesis and Psychosocial Development"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3617-8911","authenticated-orcid":false,"given":"Xiaohong","family":"Huang","sequence":"first","affiliation":[{"name":"Department of Pathophysiology, Institute of Neuroregeneration & Neurorehabilitation, Qingdao University, Qingdao 266071, China"},{"name":"Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhendong","family":"Feng","sequence":"additional","affiliation":[{"name":"Department of Pathophysiology, Institute of Neuroregeneration & Neurorehabilitation, Qingdao University, Qingdao 266071, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0998-5294","authenticated-orcid":false,"given":"Heng-wei","family":"Cheng","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA"},{"name":"Livestock Behavior Research Unit, USDA-ARS, West Lafayette, IN 47907, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,8]]},"reference":[{"key":"ref_1","first-page":"1","article-title":"Death Rates Due to Suicide and Homicide Among Persons Aged 10-24: United States, 2000-2017","volume":"352","author":"Curtin","year":"2019","journal-title":"NCHS Data Brief"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1111\/sltb.12475","article-title":"Psychosocial Factors Correlated with Undisclosed Suicide Attempts to Significant Others: Findings from the Adolescence SEYLE Study","volume":"49","author":"Barzilay","year":"2019","journal-title":"Suicide Life-Threat. Behav."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1521\/pedi.16.5.437.22123","article-title":"Impaired social functioning and symptoms of personality disorders assessed by peer and self-report in a nonclinical population","volume":"16","author":"Oltmanns","year":"2002","journal-title":"J. Pers. Disord."},{"key":"ref_4","first-page":"701","article-title":"Peer status in relation to psychotic experiences and psychosocial problems in adolescents: A longitudinal school-based study","volume":"27","author":"Schaefer","year":"2017","journal-title":"Eur. Child Adolesc. Psychiatry"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1111\/j.1469-7610.2007.01821.x","article-title":"Genetic and environmental influences on victims, bullies and bully-victims in childhood","volume":"49","author":"Ball","year":"2008","journal-title":"J. Child Psychol. Psychiatry"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1016\/j.jad.2011.10.007","article-title":"A longitudinal study of maternal prenatal, postnatal and concurrent depressive symptoms and adolescent well-being","volume":"136","author":"Korhonen","year":"2012","journal-title":"J. Affect. Disord."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1338","DOI":"10.1097\/S0890-8567(09)61916-X","article-title":"Smoking During Pregnancy and Attention-Deficit\/Hyperactivity Disorder, Predominantly Inattentive Type: A Case-Control Study","volume":"45","author":"Schmitz","year":"2006","journal-title":"J. Am. Acad. Child Adolesc. Psychiatry"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1111\/jcpp.12012","article-title":"Prenatal family adversity and maternal mental health and vulnerability to peer victimisation at school","volume":"54","author":"Lereya","year":"2013","journal-title":"J. Child Psychol. Psychiatry"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1159\/000455228","article-title":"Restraint Stress during Pregnancy Rapidly Raises Kynurenic Acid Levels in Mouse Placenta and Fetal Brain","volume":"38","author":"Notarangelo","year":"2016","journal-title":"Dev. Neurosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"143007","DOI":"10.1172\/jci.insight.143007","article-title":"Identifying a biological signature of prenatal maternal stress","volume":"6","author":"Keane","year":"2021","journal-title":"JCI Insight"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"21","DOI":"10.4137\/IJTR.S12715","article-title":"L-Tryptophan Metabolism in Pregnant Mice Fed a High L-Tryptophan Diet and the Effect on Maternal, Placental, and Fetal Growth","volume":"6","author":"Tsuji","year":"2013","journal-title":"Int. J. Tryptophan Res."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Edvinsson, \u00c5., Hellgren, C., Kallak, T.K., \u00c5kerud, H., Skalkidou, A., Stener-Victorin, E., Fornes, R., Spigset, O., Lager, S., and Olivier, J. (2019). The effect of antenatal depression and antidepressant treatment on placental tissue: A protein-validated gene expression study. BMC Pregnancy Childbirth, 19.","DOI":"10.1186\/s12884-019-2586-y"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1038\/nature09972","article-title":"A transient placental source of serotonin for the fetal forebrain","volume":"472","author":"Bonnin","year":"2011","journal-title":"Nature"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/15622970701513764","article-title":"Tryptophan as an evolutionarily conserved signal to brain serotonin: Molecular evidence and psychiatric implications","volume":"10","author":"Russo","year":"2007","journal-title":"World J. Biol. Psychiatry"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"249","DOI":"10.5468\/ogs.2014.57.4.249","article-title":"The tryptophan utilization concept in pregnancy","volume":"57","author":"Badawy","year":"2014","journal-title":"Obstet. Gynecol. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.cca.2017.02.018","article-title":"Tryptophan and purine metabolites are consistently upregulated in the urinary metabolome of patients diagnosed with gestational diabetes mellitus throughout pregnancy: A longitudinal metabolomics study of Chinese pregnant women part 2","volume":"468","author":"Law","year":"2017","journal-title":"Clin. Chim. Acta"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0193-953X(05)70358-0","article-title":"The New Epidemiology of Schizophrenia","volume":"21","author":"Jones","year":"1998","journal-title":"Psychiatr. Clin. N. Am."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.pnpbp.2012.06.014","article-title":"Schizophrenia: Linking prenatal infection to cytokines, the tryptophan catabolite (TRYCAT) pathway, NMDA receptor hypofunction, neurodevelopment and neuroprogression","volume":"42","author":"Anderson","year":"2013","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1500","DOI":"10.1016\/j.pnpbp.2010.08.013","article-title":"SRD5A2 is associated with increased cortisol metabolism in schizophrenia spectrum disorders","volume":"34","author":"Steen","year":"2010","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.neubiorev.2009.11.008","article-title":"Prenatal stress and the programming of the HPA axis","volume":"35","author":"Glover","year":"2010","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"113471","DOI":"10.1016\/j.bbr.2021.113471","article-title":"Prenatal stress-induced disruptions in microbial and host tryptophan metabolism and transport","volume":"414","author":"Galley","year":"2021","journal-title":"Behav. Brain Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/0165-3806(92)90059-6","article-title":"Administration of tryptophan-enriched diets to pregnant rats retards the development of the serotonergic system in their offspring","volume":"68","author":"Huether","year":"1992","journal-title":"Dev. Brain Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"971","DOI":"10.3109\/10641969109042103","article-title":"Effects of Tryptophane on Shrsp Offspring Growth","volume":"13","author":"Ito","year":"1991","journal-title":"Clin. Exp. Hypertens. Part A Theory Pract."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/0002-9378(86)90096-7","article-title":"Maternal dietary substrates and human fetal biophysical activity","volume":"155","author":"Devoe","year":"1986","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0024-3205(91)90579-Z","article-title":"Fetal brain serotonin synthesis and catabolism is under control by mother intake of tryptophan","volume":"49","author":"Arevalo","year":"1991","journal-title":"Life Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0006-8993(97)81718-0","article-title":"Tryptophan ingestion by gestant mothers alters prolactin and luteinizing hormone release in the adult male offspring","volume":"774","author":"Martin","year":"1997","journal-title":"Brain Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1111\/j.1471-4159.1981.tb04467.x","article-title":"Tryptophan Overload in the Pregnant Rat: Effect on Brain Amino Acid Levels and In Vitro Protein Synthesis","volume":"37","author":"Fando","year":"1981","journal-title":"J. Neurochem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1007\/s10735-008-9188-8","article-title":"Embryonic and postnatal development in experimental tryptophan deprived rats. A preliminary study","volume":"39","author":"Imbesi","year":"2008","journal-title":"Histochem. J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1111\/j.1439-0264.2009.00955.x","article-title":"Is Tryptophan \u2018more\u2019 Essential than Other Essential Aminoacids in Development? A Morphologic Study","volume":"38","author":"Imbesi","year":"2009","journal-title":"Anat. Histol. Embryol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.ijdevneu.2012.01.002","article-title":"Reduction of serotonergic neurons in the dorsal raphe due to chronic prenatal administration of a tryptophan-free diet","volume":"30","author":"Escobar","year":"2012","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Hsu, C.-N., Lin, I.-C., Yu, H.-R., Huang, L.-T., Tiao, M.-M., and Tain, Y.-L. (2020). Maternal Tryptophan Supplementation Protects Adult Rat Offspring against Hypertension Programmed by Maternal Chronic Kidney Disease: Implication of Tryptophan-Metabolizing Microbiome and Aryl Hydrocarbon Receptor. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21124552"},{"key":"ref_32","first-page":"297","article-title":"Effects of high-tryptophan diet on pre- and postnatal development in rats: A morphological study","volume":"53","author":"Castrogiovanni","year":"2013","journal-title":"Z. f\u00fcr Ern\u00e4hrungswissenschaft"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1093\/jn\/106.2.222","article-title":"Lenticular Opacities in Young Rats as a Consequence of Maternal Diets Low in Tryptophan and\/or Vitamin E","volume":"106","author":"Bunce","year":"1976","journal-title":"J. Nutr."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1152\/japplphysiol.00788.2010","article-title":"Maternal dietary tryptophan deficiency alters cardiorespiratory control in rat pups","volume":"110","author":"Penatti","year":"2011","journal-title":"J. Appl. Physiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"3005","DOI":"10.1002\/jsfa.9514","article-title":"Negative effects on newborn piglets caused by excess dietary tryptophan in the morning in sows","volume":"99","author":"Xu","year":"2019","journal-title":"J. Sci. Food Agric."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1479","DOI":"10.1016\/j.pnpbp.2011.02.016","article-title":"Effects of maternal l-tryptophan depletion and corticosterone administration on neurobehavioral adjustments in mouse dams and their adolescent and adult daughters","volume":"35","author":"Zoratto","year":"2011","journal-title":"Prog. Neuro-Psychopharmacology Biol. Psychiatry"},{"key":"ref_37","unstructured":"Baumgarten, H.G., and G\u00f6thert, M. (2012). Serotoninergic Neurons and 5-HT Receptors in the CNS, Springer Science & Business Media."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1038\/mp.2014.10","article-title":"Dopamine and serotonin signaling during two sensitive developmental periods differentially impact adult aggressive and affective behaviors in mice","volume":"19","author":"Yu","year":"2014","journal-title":"Mol. Psychiatry"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"186","DOI":"10.3389\/fimmu.2020.00186","article-title":"Serotonin: A Potent Immune Cell Modulator in Autoimmune Diseases","volume":"11","author":"Wan","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_40","first-page":"269","article-title":"The respective roles of tryptophan uptake and tryptophan hydroxylase in the regulation of serotonin synthesis in the central nervous system","volume":"77","author":"Hamon","year":"1981","journal-title":"J. Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"S66","DOI":"10.1016\/j.placenta.2015.11.013","article-title":"Effects of prenatal maternal stress on serotonin and fetal development","volume":"48","author":"Laurent","year":"2016","journal-title":"Placenta"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/npp.2014.231","article-title":"Monoamine-Sensitive Developmental Periods Impacting Adult Emotional and Cognitive Behaviors","volume":"40","author":"Suri","year":"2015","journal-title":"Neuropsychopharmacology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.infbeh.2010.09.008","article-title":"Prenatal depression effects on early development: A review","volume":"34","author":"Field","year":"2011","journal-title":"Infant Behav. Dev."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1016\/j.neuropharm.2011.09.015","article-title":"Prenatal fluoxetine exposure induces life-long serotonin 5-HT3 receptor-dependent cortical abnormalities and anxiety-like behaviour","volume":"62","author":"Noorlander","year":"2012","journal-title":"Neuropharmacology"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e842","DOI":"10.4088\/JCP.14m09240","article-title":"Neurodevelopment of Children Prenatally Exposed to Selective Reuptake Inhibitor Antidepressants","volume":"76","author":"Nulman","year":"2015","journal-title":"J. Clin. Psychiatry"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.jpsychires.2011.12.004","article-title":"The interaction of social risk factors and HPA axis dysregulation in predicting emotional symptoms of five- and six-year-old children","volume":"46","author":"Perren","year":"2012","journal-title":"J. Psychiatr. Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/S0006-8993(99)02271-4","article-title":"Colocalization of arginine-vasotocin and chicken luteinizing hormone-releasing hormone-I (cLHRH-I) in the preoptic-hypothalamic region of the chicken","volume":"856","author":"Eelen","year":"2000","journal-title":"Brain Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"110472","DOI":"10.1016\/j.mce.2019.110472","article-title":"The development of the serotonergic and dopaminergic systems during chicken mid-late embryogenesis","volume":"493","author":"Huang","year":"2019","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_49","first-page":"189","article-title":"The Role of Serotonin, Vasopressin, and Serotonin\/Vasopressin Interactions in Aggressive Behavior","volume":"Volume 17","author":"Morrison","year":"2014","journal-title":"Behavioral Neurobiology of Alcohol Addiction"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"177","DOI":"10.3389\/fonc.2012.00177","article-title":"Selective Serotonin Reuptake Inhibitor (SSRI) Antidepressants, Prolactin and Breast Cancer","volume":"2","author":"Ashbury","year":"2012","journal-title":"Front. Oncol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1016\/j.psyneuen.2011.04.007","article-title":"Prolactin in response to acute psychosocial stress in healthy men and women","volume":"36","author":"Lennartsson","year":"2011","journal-title":"Psychoneuroendocrinology"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2593","DOI":"10.1210\/en.2017-00341","article-title":"Exposure to Acute Psychosocial Stress Disrupts the Luteinizing Hormone Surge Independent of Estrous Cycle Alterations in Female Mice","volume":"158","author":"Wagenmaker","year":"2017","journal-title":"Endocrinology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"332","DOI":"10.3389\/fpsyt.2019.00332","article-title":"Initiation of the Hypothalamic\u2013Pituitary\u2013Gonadal Axis in Young Girls Undergoing Central Precocious Puberty Exerts Remodeling Effects on the Prefrontal Cortex","volume":"10","author":"Yang","year":"2019","journal-title":"Front. Psychiatry"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Usui, N., Matsuzaki, H., and Shimada, S. (2021). Characterization of Early Life Stress-Affected Gut Microbiota. Brain Sci., 11.","DOI":"10.3390\/brainsci11070913"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.bbi.2019.03.006","article-title":"Multi-hit early life adversity affects gut microbiota, brain and behavior in a sex-dependent manner","volume":"80","author":"Rincel","year":"2019","journal-title":"Brain Behav. Immun."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Mahmoudi, R., Moosazad, S., and Aghaei, K. (2019). Gut-Brain Axis: Probiotic, Bacillus subtilis, Prevents Aggression via the Modification of the Central Serotonergic System. Oral Health by Using Probiotic Products, IntechOpen.","DOI":"10.5772\/intechopen.86714"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1002\/(SICI)1098-2302(199909)35:2<146::AID-DEV7>3.0.CO;2-G","article-title":"Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys","volume":"35","author":"Bailey","year":"1999","journal-title":"Dev. Psychobiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1111\/nmo.12804","article-title":"Probiotic Lactobacillus casei strain Shirota relieves stress-associated symptoms by modulating the gut\u2013brain interaction in human and animal models","volume":"28","author":"Takada","year":"2016","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41398-019-0389-6","article-title":"Altered composition and function of intestinal microbiota in autism spectrum disorders: A systematic review","volume":"9","author":"Liu","year":"2019","journal-title":"Transl. Psychiatry"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2064","DOI":"10.1038\/s41564-019-0540-4","article-title":"Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut","volume":"4","author":"Fung","year":"2019","journal-title":"Nat. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"2591","DOI":"10.1039\/D0FO02375B","article-title":"Daily intake of Lactobacillus alleviates autistic-like behaviors by ameliorating the 5-hydroxytryptamine metabolic disorder in VPA-treated rats during weaning and sexual maturation","volume":"12","author":"Kong","year":"2021","journal-title":"Food Funct."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"e00261","DOI":"10.1042\/BSR20150197","article-title":"Tryptophan metabolism, disposition and utilization in pregnancy","volume":"35","author":"Badawy","year":"2015","journal-title":"Biosci. Rep."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.resp.2010.08.017","article-title":"The role of serotonin in respiratory function and dysfunction","volume":"174","author":"Hilaire","year":"2010","journal-title":"Respir. Physiol. Neurobiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1093\/oxfordjournals.schbul.a033455","article-title":"The Relationship of Prenatal and Perinatal Complications to Cognitive Functioning at Age 7 in the New England Cohorts of the National Collaborative Perinatal Project","volume":"26","author":"Seidman","year":"2000","journal-title":"Schizophr. Bull."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1093\/eurpub\/cki187","article-title":"Socioeconomic, psychosocial, behavioural, and psychological determinants of BMI among young women: Differing patterns for underweight and overweight\/obesity","volume":"16","author":"Ali","year":"2005","journal-title":"Eur. J. Public Health"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1080\/15622975.2020.1769189","article-title":"Seasonality of plasma tryptophan and kynurenine in pregnant mothers with a history of seasonal affective disorder: Vulnerability or adaptation?","volume":"21","author":"Levitan","year":"2020","journal-title":"World J. Biol. Psychiatry"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1017\/S0965539500001005","article-title":"The fetal origins of adult disease","volume":"6","author":"Barker","year":"1994","journal-title":"Fetal Matern. Med. Rev."},{"key":"ref_68","first-page":"2217","article-title":"Understanding Bullying: Roles, Types, Gender Difference and Effect on Mental Health","volume":"9","author":"Balayan","year":"2021","journal-title":"Int. J. Indian Psychol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1038\/mi.2016.141","article-title":"Does a prenatal bacterial microbiota exist?","volume":"10","author":"Hornef","year":"2017","journal-title":"Mucosal Immunol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"International Chicken Genome Sequencing Consortium (2004). Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature, 432, 695\u2013716.","DOI":"10.1038\/nature03154"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1139\/gen-2020-0129","article-title":"The chicken model organism for epigenomic research","volume":"64","author":"Beacon","year":"2021","journal-title":"Genome"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.yhbeh.2013.12.002","article-title":"Embryonic exposure to corticosterone modifies aggressive behavior through alterations of the hypothalamic pituitary adrenal axis and the serotonergic system in the chicken","volume":"65","author":"Ahmed","year":"2014","journal-title":"Horm. Behav."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.physbeh.2013.07.013","article-title":"Strain vulnerability and resiliency in the chick anxiety\u2013depression model","volume":"120","author":"Hymel","year":"2013","journal-title":"Physiol. Behav."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/S0306-4530(02)00044-6","article-title":"Social stress differentially regulates neuroendocrine responses in laying hens: I. Genetic basis of dopamine responses under three different social conditions","volume":"28","author":"Cheng","year":"2003","journal-title":"Psychoneuroendocrinology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1016\/j.psyneuen.2003.09.002","article-title":"Chronic social stress differentially regulates neuroendocrine responses in laying hens: II. Genetic basis of adrenal responses under three different social conditions","volume":"29","author":"Cheng","year":"2004","journal-title":"Psychoneuroendocrinology"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"501","DOI":"10.3389\/fphys.2019.00501","article-title":"Embryonic Exposure to Valproic Acid Affects Social Predispositions for Dynamic Cues of Animate Motion in Newly-Hatched Chicks","volume":"10","author":"Lorenzi","year":"2019","journal-title":"Front. Physiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1007\/s00213-013-2979-y","article-title":"Impaired social behavior in chicks exposed to sodium valproate during the last week of embryogenesis","volume":"227","author":"Nishigori","year":"2013","journal-title":"Psychopharmacology"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"5919","DOI":"10.1038\/s41598-018-24202-8","article-title":"Embryonic Exposure to Valproic Acid Impairs Social Predispositions of Newly-Hatched Chicks","volume":"8","author":"Versace","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"6838","DOI":"10.1038\/s41598-019-43280-w","article-title":"Characterization of microbial communities in the chicken oviduct and the origin of chicken embryo gut microbiota","volume":"9","author":"Lee","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Huang, X., Hu, J., Peng, H., and Cheng, H.-W. (2022). Embryonic Exposure to Tryptophan Yields Bullying Victimization via Reprogramming the Microbiota-Gut-Brain Axis in a Chicken Model. Nutrients, 14.","DOI":"10.3390\/nu14030661"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"01315","DOI":"10.1128\/mBio.01315-19","article-title":"Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients","volume":"10","author":"Saffarian","year":"2019","journal-title":"mBio"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"541","DOI":"10.3389\/fpsyt.2020.00541","article-title":"Altered Composition of Gut Microbiota in Depression: A Systematic Review","volume":"11","author":"Barandouzi","year":"2020","journal-title":"Front. Psychiatry"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"101874","DOI":"10.1016\/j.ajp.2019.101874","article-title":"Microbiota and gut-brain axis dysfunction in autism spectrum disorder: Evidence for functional gastrointestinal disorders","volume":"47","author":"Lasheras","year":"2020","journal-title":"Asian J. Psychiatry"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1111\/1462-2920.13658","article-title":"Oscillospiraand related bacteria\u2014From metagenomic species to metabolic features","volume":"19","author":"Gophna","year":"2017","journal-title":"Environ. Microbiol."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Osadchiy, V., Labus, J.S., Gupta, A., Jacobs, J., Ashe-McNalley, C., Hsiao, E.Y., and Mayer, E.A. (2018). Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0201772"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.bandc.2011.06.011","article-title":"Worse than sticks and stones? Bullying is associated with altered HPA axis functioning and poorer health","volume":"77","author":"Knack","year":"2011","journal-title":"Brain Cogn."},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Berthoud, H.-R., Albaugh, V.L., and Neuhuber, W.L. (2021). Gut-brain communication and obesity: Understanding functions of the vagus nerve. J. Clin. Investig., 131.","DOI":"10.1172\/JCI143770"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1016\/j.bbr.2016.10.035","article-title":"Bicuculline, a GABAA-receptor antagonist, blocked HPA axis activation induced by ghrelin under an acute stress","volume":"320","author":"Cid","year":"2017","journal-title":"Behav. Brain Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"7129","DOI":"10.1038\/s41598-019-43584-x","article-title":"Unpredictable Chronic Mild Stress Suppresses the Incorporation of New Neurons at the Caudal Pole of the Chicken Hippocampal Formation","volume":"9","author":"Gualtieri","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1159\/000477654","article-title":"The Avian Hippocampal Formation and the Stress Response","volume":"90","author":"Smulders","year":"2017","journal-title":"Brain Behav. Evol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"100351","DOI":"10.1016\/j.ynstr.2021.100351","article-title":"Telencephalic regulation of the HPA axis in birds","volume":"15","author":"Smulders","year":"2021","journal-title":"Neurobiol. Stress"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1099\/ijs.0.000083","article-title":"Olsenella scatoligenes sp. nov., a 3-methylindole- (skatole) and 4-methylphenol- (p-cresol) producing bacterium isolated from pig faeces","volume":"65","author":"Li","year":"2015","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/j.neubiorev.2015.08.017","article-title":"The basolateral amygdala in reward learning and addiction","volume":"57","author":"Wassum","year":"2015","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1093\/neuros\/nyy635","article-title":"Amygdala and Hypothalamus: Historical Overview With Focus on Aggression","volume":"85","author":"Gouveia","year":"2019","journal-title":"Neurosurgery"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1016\/S0006-3223(99)00237-1","article-title":"The role of corticotropin-releasing factor\u2013norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress","volume":"46","author":"Francis","year":"1999","journal-title":"Biol. Psychiatry"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s10519-019-09987-2","article-title":"On the Nature of Monozygotic Twin Concordance and Discordance for Autistic Trait Severity: A Quantitative Analysis","volume":"50","author":"Castelbaum","year":"2020","journal-title":"Behav. Genet."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"830","DOI":"10.1016\/j.jaac.2010.01.024","article-title":"Serotonin Transporter Gene Moderates the Development of Emotional Problems Among Children Following Bullying Victimization","volume":"49","author":"Sugden","year":"2010","journal-title":"J. Am. Acad. Child Adolesc. Psychiatry"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1016\/S0306-4522(96)00452-6","article-title":"Quantitative and morphometric data indicate precise cellular interactions between serotonin terminals and postsynaptic targets in rat substantia nigra","volume":"76","author":"Moukhles","year":"1997","journal-title":"Neuroscience"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1007\/s00213-010-2029-y","article-title":"Presynaptic control of serotonin on striatal dopamine function","volume":"213","author":"Navailles","year":"2010","journal-title":"Psychopharmacology"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.pneurobio.2016.03.004","article-title":"Serotonergic modulation of the activity of mesencephalic dopaminergic systems: Therapeutic implications","volume":"151","year":"2017","journal-title":"Prog. Neurobiol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"16889","DOI":"10.1523\/JNEUROSCI.1398-13.2013","article-title":"The Impact of Dopamine on Aggression: An [18F]-FDOPA PET Study in Healthy Males","volume":"33","author":"Winz","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1002\/ab.21459","article-title":"Alterations to Embryonic Serotonin Change Aggression and Fearfulness","volume":"39","author":"Dennis","year":"2013","journal-title":"Aggress. Behav."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"2440","DOI":"10.3382\/ps.2011-01513","article-title":"The dopaminergic system and aggression in laying hens","volume":"90","author":"Dennis","year":"2011","journal-title":"Poult. Sci."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.neuroscience.2021.08.011","article-title":"Prenatal Serotonin Fluctuation Affects Serotoninergic Development and Related Neural Circuits in Chicken Embryos","volume":"473","author":"Huang","year":"2021","journal-title":"Neuroscience"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1186\/2040-2392-5-32","article-title":"Autism-associated gene Dlgap2 mutant mice demonstrate exacerbated aggressive behaviors and orbitofrontal cortex deficits","volume":"5","author":"Liao","year":"2014","journal-title":"Mol. Autism"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1246","DOI":"10.1001\/jamapsychiatry.2020.2453","article-title":"Maternal Use of Specific Antidepressant Medications During Early Pregnancy and the Risk of Selected Birth Defects","volume":"77","author":"Anderson","year":"2020","journal-title":"JAMA Psychiatry"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/8\/1270\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:50:50Z","timestamp":1760136650000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/8\/1270"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,8]]},"references-count":106,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,4]]}},"alternative-id":["cells11081270"],"URL":"https:\/\/doi.org\/10.3390\/cells11081270","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,8]]}}}