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Male fetus susceptibility to maternal inflammation: C-reactive protein and brain development

Published online by Cambridge University Press:  02 December 2019

Sharon K Hunter ,
M. Camille Hoffman Open the ORCID record for M. Camille Hoffman [Opens in a new window] ,
Angelo D'Alessandro ,
Kathleen Noonan ,
Anna Wyrwa ,
Robert Freedman Open the ORCID record for Robert Freedman [Opens in a new window]  and
Amanda J. Law Open the ORCID record for Amanda J. Law [Opens in a new window]
Sharon K Hunter*
Affiliation:
Departments of Psychiatry, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
M. Camille Hoffman
Affiliation:
Departments of Psychiatry, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA Obstetrics and Gynecology, Division of Maternal and Fetal Medicine, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
Angelo D'Alessandro
Affiliation:
Biochemistry and Molecular Genetics, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
Kathleen Noonan
Affiliation:
Departments of Psychiatry, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
Anna Wyrwa
Affiliation:
Departments of Psychiatry, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
Robert Freedman
Affiliation:
Departments of Psychiatry, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
Amanda J. Law
Affiliation:
Departments of Psychiatry, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA Cell and Developmental Biology, University of Colorado Denver School of Medicine, Aurora, Colorado80045, USA
*
Author for correspondence: Sharon K. Hunter, E-mail: [email protected]
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Abstract

Background

Maternal inflammation in early pregnancy has been identified epidemiologically as a prenatal pathogenic factor for the offspring's later mental illness. Early newborn manifestations of the effects of maternal inflammation on human fetal brain development are largely unknown.

Methods

Maternal infection, depression, obesity, and other factors associated with inflammation were assessed at 16 weeks gestation, along with maternal C-reactive protein (CRP), cytokines, and serum choline. Cerebral inhibition was assessed by inhibitory P50 sensory gating at 1 month of age, and infant behavior was assessed by maternal ratings at 3 months of age.

Results

Maternal CRP diminished the development of cerebral inhibition in newborn males but paradoxically increased inhibition in females. Similar sex-dependent effects were seen in mothers' assessment of their infant's self-regulatory behaviors at 3 months of age. Higher maternal choline levels partly mitigated the effect of CRP in male offspring.

Conclusions

The male fetal-placental unit appears to be more sensitive to maternal inflammation than females. Effects are particularly marked on cerebral inhibition. Deficits in cerebral inhibition 1 month after birth, similar to those observed in several mental illnesses, including schizophrenia, indicate fetal developmental pathways that may lead to later mental illness. Deficits in early infant behavior follow. Early intervention before birth, including prenatal vitamins, folate, and choline supplements, may help prevent fetal development of pathophysiological deficits that can have life-long consequences for mental health.

Keywords

Child developmentcholineC-reactive proteinpregnancyprenatal exposure delayed effectssensory gating
Type
Original Articles
Information
Psychological Medicine , Volume 51 , Issue 3 , February 2021 , pp. 450 - 459
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Copyright
Copyright © Cambridge University Press 2019

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References

Abidin, R. R. (2012). Parenting stress index (3rd ed.). Odessa, FL: Psychological Assessment Resources.Google Scholar
Abratte, C. M., Wang, W., Li, R., Axume, J., Moriarty, D. J., & Caudill, M. A. (2009). Choline status is not a reliable indicator of moderate changes in dietary choline consumption in premenopausal women. The Journal of Nutritional Biochemistry, 20, 62–69.CrossRefGoogle Scholar
Adler, L. E., Pachtman, E., Franks, R. D., Pecevich, M., Waldo, M. C., & Freedman, R. (1982). Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biological Psychiatry, 17, 639–654.Google Scholar
Alkondon, M., Pereira, E. F. R., Cortes, W. S., Maelicke, A., & Albuquerque, E. X. (1997). Choline is a selective agonist at alpha7 nicotinic acetylcholine receptors in rat brain neurons. European Journal of Neuroscience, 9, 2734–2742.CrossRefGoogle ScholarPubMed
American Medical Association (2017). Proceedings of the 2017 Annual Meeting House of Delegates. Retrieved from https://www.ama-assn.org/about/proceedings-2017-annual-meeting-house-delegates. [Accessed 27th November 2017].Google Scholar
Anders, T., Emde, R., & Parmelee, A. (1971). A manual of standardized terminology, techniques and criteria for scoring of states of sleep and wakefulness in newborn infants. Los Angeles: UCLA Brain Information Service, NINDS Neurological Information Network.Google Scholar
Baumgartner, H. K., Trinder, K. M., Galimanis, C. E., Post, A., Phang, T., Ross, R. G., & Winn, V. D. (2015). Characterization of choline transporters in the human placenta over gestation. Placenta, 36, 1362–1369.CrossRefGoogle ScholarPubMed
Bayatti, N., Moss, J. A., Sun, L., Ambrose, P., Ward, J. F. H., Lindsay, L., & Clowry, G. J. (2008). A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cerebral Cortex 18, 1536–1548.CrossRefGoogle ScholarPubMed
Bosquet-Enlow, M., White, M. T., Hails, K., Cabrera, I., & Wright, R. J. (2016). The infant behavior questionnaire-revised: factor structure in a culturally and sociodemographically diverse sample in the United States. Infant Behavior and Development, 43, 24–35.CrossRefGoogle Scholar
Bronson, S. L., & Bale, T. L. (2014). Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal anti-inflammatory treatment. Endocrinology, 155, 2635–2646.CrossRefGoogle Scholar
Brown, A. S., & Derkits, E. J. (2010). Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. American Journal of Psychiatry, 167, 261–280.CrossRefGoogle ScholarPubMed
Brown, A. S., & Meyer, U. (2018). Maternal immune activation and neuropsychiatric illness: a translational research perspective. American Journal of Psychiatry, 175, 1073–1083.CrossRefGoogle ScholarPubMed
Brown, A. S., Sourander, A., Hinkka-Yli-Salomäki, S., McKeague, I. W., Sundvall, J., & Surcel, H. M. (2014). Elevated maternal C-reactive protein and autism in a national birth cohort. Molecular Psychiatry, 19, 259–264.CrossRefGoogle Scholar
Bui, Q., & Miller, C. C. (2018). The age that women have babies: how a gap divides America. New York Times. Retrieved from https://www.nytimes.com/interactive/2018/08/04/ upshot/up-birth-age-gap.html.Google Scholar
Canetta, S., Bolkan, S., Padilla-Coreano, N., Song, L. J., Sahn, R., Harrison, N. L., … Kellendonk, C. (2016). Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons. Molecular Psychiatry 21, 956–968.CrossRefGoogle ScholarPubMed
Canetta, S., Sourander, A., Surcel, H. M., Hinkka-Yli-Salomaki, S., Leiviska, J., Kellendonk, C., … Brown, A. S. (2014). Elevated maternal C-reactive protein and increased risk of schizophrenia in a national birth cohort. American Journal of Psychiatry, 171, 960–968.CrossRefGoogle Scholar
Caudill, M. A., Strupp, B. J., Muscalu, L., Nevins, J. E. H., & Canfield, R. L. (2018). Maternal choline supplementation during the third trimester of pregnancy improves infant information processing speed: a randomized, double-blind, controlled feeding study. The FASEB Journal, 32, 2172–2180.CrossRefGoogle ScholarPubMed
Clarke, M. C., Tanskanen, A., Huttunen, M., Whittaker, J. C., & Cannon, M. (2009). Evidence for an interaction between familial liability and prenatal exposure to infection in the causation of schizophrenia. American Journal of Psychiatry, 166, 1025–1030.CrossRefGoogle ScholarPubMed
Clementz, B. A., Sweeney, J. A., Hamm, J. P., Ivleva, E. I., Ethridge, L. E., Pearlson, G. D., … Tamminga, C. A. (2016). Identification of distinct psychosis biotypes using brain-based biomarkers. American Journal of Psychiatry, 173, 373–384.CrossRefGoogle ScholarPubMed
Dada, T., Rosenzweig, J. M., Al Shammary, M., Firdaus, W., Al Rebh, S., Borbiev, T., … Burd, I. (2014). Mouse model of intrauterine inflammation: sex-specific differences in long-term neurologic and immune sequelae. Brain, Behavior, and Immunity, 38, 142–150.CrossRefGoogle ScholarPubMed
Debost, J. P., Larsen, J. T., Munk-Olsen, T., Mortensen, P. B., Meyer, U., & Petersen, L. (2017). Joint effects of exposure to prenatal infection and peripubertal psychological trauma in schizophrenia. Schizophrenia Bulletin, 43, 171–179.CrossRefGoogle Scholar
Erlenmeyer-Kimling, L., & Cornblatt, B. (1987). The New York High-Risk Project: a follow-up report. Schizophrenia Bulletin, 13, 451–461.CrossRefGoogle Scholar
Ernst, L. M., Grobman, W. A., Wolfe, K., Huang, M. H., McDade, T. W., Holl, J. L., & Borders, A. E. (2013). Biological markers of stress in pregnancy: associations with chronic placental inflammation at delivery. American Journal of Perinatology 30, 557–564.Google ScholarPubMed
Food and Drug Administration (2016). Food labeling: revision of the nutrition and supplement facts labels. Federal Register, 27, 903–904.Google Scholar
Freedman, R., Coon, H., Myles-Worsley, M., Orr-Urtreger, A., Olincy, A., Davis, A., … Byerley, W. (1997). Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proceedings of the National Academy of Science USA, 94, 587–592.CrossRefGoogle ScholarPubMed
Freedman, R., Hunter, S. K., Law, A. J., Wagner, B. D., D'Allesandro, A., Christians, U., … Hoffman, M. C. (2019). Higher gestational choline levels in maternal infection are protective for infant brain development. Journal of Pediatrics, 208, 198–206e2.CrossRefGoogle ScholarPubMed
Ganapathi, R., & Manda, K. (2017). Later life changes in hippocampal neurogenesis and behavioral functions after low-dose prenatal irradiation at early organogenesis stage. International Journal of Radiation Oncology, Biology, Physics, 98, 63–74.CrossRefGoogle ScholarPubMed
Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the revised infant behavior questionnaire. Infant Behavior and Development, 26, 64–86.CrossRefGoogle Scholar
Ghassabian, A., Albert, P. S., Hornig, M., Yeung, E., Cherkerzian, S., Goldstein, R. B., … Gilman, S. E. (2018). Gestational cytokine concentrations and neurocognitive development at 7 years. Translational Psychiatry, 13, 64. doi: 10.1038/s41398-018-0112-zCrossRefGoogle Scholar
Giovanoli, S., Engler, H., Engler, A., Richetto, J., Voget, M., Willi, R., … Meyer, U. (2013). Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science, 339, 1095–1099.CrossRefGoogle ScholarPubMed
Giovanoli, S., Werge, T. M., Mortensen, P. B., Didriksen, M., & Meyer, U. (2019). Interactive effects between hemizygous 15q13.3 microdeletion and peripubertal stress on adult behavioral functions. Neuropsychopharmacology 44, 703–710.CrossRefGoogle ScholarPubMed
Goldstein, J. M., Cherkerzian, S., Seidman, L. J., Donatelli, J. A., Remington, A., Tsuang, M. T., … Buka, S. L. (2014). Prenatal maternal immune disruption and sex dependent risk for psychoses. Psychological Medicine, 44, 3249–3261.CrossRefGoogle ScholarPubMed
Graham, A. M., Rasmussen, J. M., Rudolph, M. D., Heim, C. M., Gilmore, J. H., Styner, M., … Buss, C. (2018). Maternal systemic interleukin-6 during pregnancy is associated with newborn amygdala phenotypes and subsequent behavior at 2 years of age. Biological Psychiatry, 83, 109–119.CrossRefGoogle ScholarPubMed
Griffith, J. M., & Freedman, R. (1995). Normalization of the auditory P50 gating deficit of schizophrenic patients after non-REM but not REM sleep. Psychiatry Research, 56, 271–278.CrossRefGoogle Scholar
Hall, M. H., Taylor, G., Salisbury, D. F., & Levy, D. L. (2011). Sensory gating event-related potentials and oscillations in schizophrenia patients and their unaffected relatives. Schizophrenia Bulletin, 37, 1187–1199.CrossRefGoogle ScholarPubMed
Hoffman, M. C., Hunter, S. K., D'Alessandro, A., Noonan, K., Wyrwa, A., & Freedman, R. (2019a). Interaction of maternal choline levels and prenatal marijuana's effects on the offspring. Psychological Medicine, 31, 1–11. doi: 10.1017/S003329171900179X, [Epub ahead of print].Google Scholar
Hoffman, M. C., Olincy, A., D'Alessandro, A., Reisz, J. A., Hansen, K. C., Hunter, S. K., … Ross, R. G. (2019b). Effects of phosphatidylcholine and betaine supplements on women's serum choline. Journal of Nutrition & Intermediary Metabolism 16, 100094. doi.org/10.1016/j.jnim.2019.100094.CrossRefGoogle Scholar
Holm, P. I., Ueland, P. M., Kvalheim, G., & Lien, E. A. (2003). Determination of choline, betaine, and dimethylglycine in plasma by a high-throughput method based on normal-phase chromatography-tandem mass spectrometry. Clinical Chemistry, 49, 286–294.CrossRefGoogle ScholarPubMed
Hunter, S. K., Corral, N., Ponicsan, H., & Ross, R. G. (2008). Reliability of P50 auditory sensory gating measures in infants during active sleep. Neuroreport, 19, 79–82.CrossRefGoogle ScholarPubMed
Hunter, S. K., Gillow, S. J., & Ross, R. G. (2015). Stability of P50 auditory sensory gating during sleep from infancy to 4 years of age. Brain Cognition, 94, 4–9.CrossRefGoogle ScholarPubMed
Hunter, S. K., Kisley, M. A., McCarthy, L., Freedman, R., & Ross, R. G. (2011). Diminished cerebral inhibition in neonates associated with risk factors for schizophrenia: parental psychosis, maternal depression, and nicotine use. Schizophrenia Bulletin, 37, 1200–1208.CrossRefGoogle ScholarPubMed
Hutchison, A. K., Hunter, S. K., Wagner, B. D., Calvin, E. A., Zerbe, G. O., & Ross, R. G. (2007). Diminished infant P50 sensory gating predicts increased 40-month-old attention, anxiety/depression, and externalizing symptoms. Journal of Attention Disorders, 21, 209–218.CrossRefGoogle Scholar
Ilcol, Y. O., Uncu, G., & Ulus, I. H. (2002). Free and phospholipid-bound choline concentrations in serum during pregnancy, after delivery, and in newborns. Archives of Physiology and Biochemistry, 110, 393–399.CrossRefGoogle Scholar
Iwao, B., Yara, M., Hara, N., Kawai, Y., Yamanaka, T., Nishihara, H., … Inazu, M. (2016). Functional expression of choline transporter like-protein 1 (CTL1) and CTL2 in human brain microvascular endothelial cells. Neurochemistry International, 93, 40–50.CrossRefGoogle ScholarPubMed
Jacobson, S. W., Carter, R. C., Molteno, C. D., Stanton, M. E., Herbert, J. S., Lindinger, N. M., Jacobson, J. L. (2018). Efficacy of maternal choline supplementation during pregnancy in mitigating adverse effects of prenatal alcohol exposure on growth and cognitive function: a randomized, double-blind, placebo-controlled clinical trial. Alcoholism: Clinical and Experimental Research, 42, 1327–1341.CrossRefGoogle ScholarPubMed
Kim, D.-J., Davis, E. P., Sandman, C. A., Sporns, O., O'Donnell, B. F., Buss, C., & Hetrick, W. P. (2017). Prenatal maternal cortisol has sex-specific associations with child brain network properties. Cerebral Cortex, 27, 5230–5241.Google ScholarPubMed
Kim, E. N., Yoon, B. H., Jeon, E. J., Lee, J. B., Hong, J. S., Lee, J. Y., … Kim, C. J. (2015). Placental deposition of C-reactive protein is a common feature of human pregnancy. Placenta, 36, 704–707.CrossRefGoogle ScholarPubMed
Kim-Fine, S., Regnault, T. R., Lee, J. S., Gimbel, S. A., Greenspoon, J. A., Fairbairn, J., … de Vrijer, B. (2012). Male gender promotes an increased inflammatory response to lipopolysaccharide in umbilical vein blood. Journal of Maternal-Fetal and Neonatal Medicine, 25, 2470–2474.CrossRefGoogle ScholarPubMed
King, J. H., Kwan, S. T. C., Yan, J., Jiang, X., Fomin, V. G., Levine, S. P., … Caudill, M. A. (2019). Maternal choline supplementation modulates placental markers of inflammation, angiogenesis, and apoptosis in a mouse model of placental insufficiency. Nutrients, 12, E374. doi: 10.3390/nu11020374CrossRefGoogle Scholar
Kisley, M. A., Polk, S. D., Ross, R. G., Levisohn, P. M., & Freedman, R. (2003). Early postnatal development of sensory gating. Neuroreport, 14, 693–697.CrossRefGoogle ScholarPubMed
Koks, N., Ghassabian, A., Greaves-Lord, K., Hofman, A., Jaddoe, V. W. V., Verhulst, F., & Tiemeier, H. (2016). Maternal C-reactive protein concentration in early pregnancy and child autistic traits in the general population. Pediatric Perinatal Epidemiology, 30, 181–189.CrossRefGoogle ScholarPubMed
Lacaille, H., Vacher, C. M., Bakalar, D., O'Reilly, J. J., Salzbank, J., & Penn, A. A. (2019). Impaired interneuron development in a novel model of neonatal brain injury. eNeuro, 6. doi: 10.1523/ENEURO.0300-18.2019CrossRefGoogle Scholar
Liu, Z., Neff, R. A., & Berg, D. K. (2006). Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science, 314, 1610–1613.CrossRefGoogle ScholarPubMed
Madan, J. C., Davis, J. M., Craig, W. Y., Collins, M., Allan, W., Quinn, R., & Dammann, O. (2009). Maternal obesity and markers of inflammation in pregnancy. Cytokine, 47, 61–64.CrossRefGoogle Scholar
Malek, A., Bersinger, N. A., Di Santo, S., Mueller, M. D., Sager, R., Schneider, H., … Raio, L. (2006). C-reactive protein production in term human placental tissue. Placenta, 27, 619–625.CrossRefGoogle ScholarPubMed
Melbye, H., Hvidsten, D., Holm, A., Nordbø, S. A., & Brox, J. (2004). The course of C-reactive protein response in untreated upper respiratory tract infection. British Journal of General Practice, 54, 653–658.Google ScholarPubMed
Miller, C. L., & Freedman, R. (1995). The activity of hippocampal interneurons and pyramidal cells during the response of the hippocampus to repeated auditory stimuli. Neuroscience, 69, 371–381.CrossRefGoogle ScholarPubMed
Nugent, B. M., O'Donnell, C. M., Epperson, C. N., & Bale, T. L. (2018). Placental HEK27me3 establishes female resilience to prenatal insults. Nature Communications, 9, 2555. doi: 10.1038/s41467-018-04992-1CrossRefGoogle Scholar
Olincy, A., Blakeley-Smith, A., Johnson, L., Kem, W. R., & Freedman, R. (2016). Brief report: initial trial of alpha7-nicotinic receptor stimulation in two adult patients with autism spectrum disorder. Journal of Autism and Developmental Disorders, 46, 3812–3817.CrossRefGoogle ScholarPubMed
Olincy, A., Braff, D. L., Adler, L. E., Cadenhead, K. S., Calkins, M. E., Dobie, D. J., … Freedman, R. (2010). Inhibition of the P50 cerebral evoked response to repeated auditory stimuli: results from the consortium on genetics of schizophrenia. Schizophrenia Research, 119, 175–182.CrossRefGoogle Scholar
Orekhova, E. V., Stroganova, T. A., Prokofyev, A. O., Nygren, G., Gillberg, C., & Elam, M. (2008). Sensory gating in young children with autism: relation to age, IQ, and EEG gamma oscillations. Neuroscience Letters, 434, 218–223.CrossRefGoogle ScholarPubMed
Osborne, L. M., & Monk, C. (2013). Perinatal depression – the fourth inflammatory morbidity of pregnancy?: theory and literature review. Psychoneuroendocrinology, 38, 1929–1952.CrossRefGoogle ScholarPubMed
Oskvig, D. B., Elkahloun, A. G., Johnson, K. R., Phillips, T. M., & Herkenham, M. (2012). Maternal immune activation by LPS selectively alters specific gene expression profiles of interneuron migration and oxidative stress in the fetus without triggering a fetal immune response. Brain, Behavior & Immunity, 26, 623–634.CrossRefGoogle ScholarPubMed
Owen, D., Setiawan, E., Li, A., McCabe, L., & Matthews, S. G. (2004). Regulation of N-methyl-D-aspartate receptor subunit expression in the fetal guinea pig brain. Biology of Reproduction, 71, 676–683.CrossRefGoogle ScholarPubMed
Pine, D. S., & Fox, N. A. (2015). Childhood antecedents and risk for adult mental disorders. Annual Review of Psychology, 66, 459–485.CrossRefGoogle ScholarPubMed
Putnam, S. P., Helbig, A. L., Gartstein, M. A., Rothbart, M. K., & Leerkes, E. (2014). Development and assessment of short and very short forms of the infant behavior questionnaire-revised. Journal of Personality Assessment, 96, 445–458.CrossRefGoogle Scholar
Quednow, B. B., Brinkmeyer, J., Mobascher, A., Nothnagel, M., Musso, F., Gründer, G., … Winterer, G. (2012). Schizophrenia risk polymorphisms in the TCF4 gene interact with smoking in the modulation of auditory sensory gating. Proceedings of the National Academy of Science USA, 109, 6271–6276.CrossRefGoogle ScholarPubMed
Ross, R. G., & Freedman, R. (2015). Endophenotypes in schizophrenia for the perinatal period: criteria for validation. Schizophrenia Bulletin, 41, 824–834.CrossRefGoogle ScholarPubMed
Ross, R. G., Hunter, S. K., Hoffman, M. C., McCarthy, L., Chambers, B. M., Law, A. J., … Freedman, R. (2016). Perinatal phosphatidylcholine supplementation and early childhood behavior problems: evidence for CHRNA7 moderation. American Journal of Psychiatry, 173, 509–516.CrossRefGoogle ScholarPubMed
Ross, R. G., Hunter, S. K., McCarthy, L., Beuler, J., Hutchison, A. K., Wagner, B. D., … Freedman, R. (2013). Perinatal choline effects on neonatal pathophysiology related to later schizophrenia risk. American Journal of Psychiatry, 170, 290–298.CrossRefGoogle ScholarPubMed
Rossi, A., Pollice, R., Daneluzzo, E., Marinangeli, M. G., & Stratt, P. (2000). Behavioral neurodevelopmental abnormalities and schizophrenic disorder: a retrospective evaluation with the Child Behavior Checklist (CBCL). Schizophrenia Research, 44, 121–128.CrossRefGoogle Scholar
Rudolph, M. D., Graham, A. M., Feczko, E., Miranda-Dominguez, O., Rasmussen, J. M., Nardos, R., … Fair, D. A. (2018). Maternal IL-6 during pregnancy can be estimated from newborn brain connectivity and predicts future working memory in offspring. Nature Neuroscience, 21, 765–772.CrossRefGoogle ScholarPubMed
Rutter, M., Kim-Cohen, J., & Maughan, B. (2006). Continuities and discontinuities in psychopathology between childhood and adult life. Journal of Child Psychology and Psychiatry, 47, 276–295.CrossRefGoogle ScholarPubMed
Schubring, D., Tzvetan, P., Miller, G. A., & Rockstroh, B. (2018). Consistency of abnormal sensory gating in first-admission and chronic schizophrenia across quantification methods. Psychophysiology, 55, e13006.CrossRefGoogle ScholarPubMed
Slobodskaya, H. R., & Kozlova, E. A. (2016). Early temperament as a predictor of later personality. Personality and Individual Differences, 99, 127–132.CrossRefGoogle Scholar
Smith, D. A., Boutros, N. N., & Schwarzkopf, S. B. (1994). Reliability of P50 auditory event-related potential indices of sensory gating. Psychophysiology, 31, 495–502.CrossRefGoogle ScholarPubMed
Smith, E., Crawford, T., Thomas, M., & Reid, V. (2018). Schizotypy and sensory gating: a 6-month-old EEG study. Schizophrenia Bulletin, 44, S301–S302.CrossRefGoogle Scholar
Sobue, A., Ito, N., Nagai, T., Shan, W., Hada, K., Nakajima, A., … Yamada, K. (2018). Astroglial major histocompatibility complex class I following immune activation leads to behavioral and neuropathological changes. Glia, 66, 1034–1052.CrossRefGoogle Scholar
Spann, M. N., Monk, C., Scheinost, D., & Peterson, B. S. (2018). Maternal immune activation during the third trimester is associated with neonatal functional connectivity of the salience network and fetal to toddler behavior. Journal of Neuroscience, 38, 2877–2886.CrossRefGoogle ScholarPubMed
Stevens, K. E., Choo, K. S., Stitzel, J. A., Marks, M. J., & Adams, C. E. (2014). Long-term improvements in sensory inhibition with gestational choline supplementation linked to α7 nicotinic receptors through studies in Chrna7 null mutation mice. Brain Research, 1552, 26–33.CrossRefGoogle ScholarPubMed
Ursini, G., Punzi, G., Chen, Q., Marenco, S., Robinson, J. F., Porcelli, A., … Weinberger, D. R. (2018). Convergence of placenta biology and genetic risk for schizophrenia. Nature Medicine, 24, 792–801.CrossRefGoogle ScholarPubMed
van den Hooven, E. H., de Kluizenaar, Y., Pierik, F. H., Hofman, A., van Ratingen, S. W., Zandveld, P. Y., … Jaddoe, V. W. (2012). Chronic air pollution exposure during pregnancy and maternal and fetal C-reactive protein levels: the Generation R Study. Environmental Health Perspectives, 12, 746–751.CrossRefGoogle Scholar
Vasistha, M. N., Pardo-Navarro, M., Gasthaus, J., Weijers, D., Müller, M. K., García-González, D., … Khodosevich, K. (2019). Maternal inflammation has a profound effect on cortical interneuron development in a stage and subtype-specific manner. Molecular Psychiatry. doi: 10.1038/s41380-019-0539-5.Google Scholar
Walker, E. F., Savoie, T., & Davis, D. (1994). Neuromotor precursors of schizophrenia. Schizophrenia Bulletin, 20, 441–451.CrossRefGoogle ScholarPubMed
Wang, H., Yu, M., Ochani, M., Amella, C. A., Tanovic, M., Susarla, S., … Tracey, K. J. (2003). Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature, 421, 384–388.CrossRefGoogle ScholarPubMed
Wu, B. T. F., Dyer, R. A., King, D. J. J., Richardson, K. J., & Innis, S. M. (2012). Early second trimester maternal plasma choline and betaine are related to measures of early cognitive development in term infants. PLoS ONE, 7, e43448.CrossRefGoogle ScholarPubMed
Wu, W. L., Adams, C. E., Stevens, K. E., Chow, K. H., Freedman, R., & Patterson, P. H. (2015). The interaction between maternal immune activation and alpha 7 nicotinic acetylcholine receptor in regulating behaviors in the offspring. Brain, Behavior, & Immunity, 46, 192–202.CrossRefGoogle ScholarPubMed
Zecevic, N., Hu, F., & Jakovcevski, I. (2011). Interneurons in the developing human neocortex. Developmental Neurobiology, 7, 18–33.CrossRefGoogle Scholar
Zeisel, S. H., Growden, J. H., Wurtman, R. J., Magil, S. G., & Logue, M. (1980). Normal plasma choline responses to ingested lecithin. Neurology, 30, 1226–1229.CrossRefGoogle ScholarPubMed
Zerbo, O., Traglia, M., Yoshida, C., Heuer, L. S., Ashwood, P., Delorenze, G. N., … Croen, L. A. (2016). Maternal mid-pregnancy C-reactive protein and risk of autism spectrum disorders: the early markers for autism study. Translational Psychiatry 6, e783.CrossRefGoogle ScholarPubMed
Zhang, M., Han, X., Bao, J., Yang, J., Shi, S. Q., Garfield, R. E., & Liu, H. (2018). Choline supplementation during pregnancy protects against gestational lipopolysaccharide-induced inflammatory responses. Reproductive Sciences, 25, 74–85.CrossRefGoogle ScholarPubMed
Zuloaga, D. G., Carbone, D. L., Quihuis, A., Hiroi, R., Chong, D. L., & Handa, R. J. (2012). Perinatal dexamethasone-induced alterations in apoptosis within the hippocampus and paraventricular nucleus of the hypothalamus are influenced by age and sex. Journal of Neuroscience Research, 90, 1403–1412.CrossRefGoogle ScholarPubMed
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