Perinatal Choline Effects on Neonatal Pathophysiology Related to Later Schizophrenia Risk
Open accessAbstract
OBJECTIVE: Deficient cerebral inhibition is a pathophysiological brain deficit related to poor sensory gating and attention in schizophrenia and other disorders. Cerebral inhibition develops perinatally, influenced by genetic and in utero factors. Amniotic choline activates fetal α7-nicotinic acetylcholine receptors and facilitates development of cerebral inhibition. Increasing this activation may protect infants from future illness by promoting normal brain development. The authors investigated the effects of perinatal choline supplementation on the development of cerebral inhibition in human infants. METHOD: A randomized placebo-controlled clinical trial of dietary phosphatidylcholine supplementation was conducted with 100 healthy pregnant women, starting in the second trimester. Supplementation to twice normal dietary levels for mother or newborn continued through the third postnatal month. All women received dietary advice regardless of treatment. Infants' electrophysiological recordings of inhibition of the P50 component of the cerebral evoked response to paired sounds were analyzed. The criterion for inhibition was suppression of the amplitude of the second P50 response by at least half, compared with the first response. RESULTS: No adverse effects of choline were observed in maternal health and delivery, birth, or infant development. At the fifth postnatal week, the P50 response was suppressed in more choline-treated infants (76%) compared with placebo-treated infants (43%) (effect size=0.7). There was no difference at the 13th week. A CHRNA7 genotype associated with schizophrenia was correlated with diminished P50 inhibition in the placebo-treated infants, but not in the choline-treated infants. CONCLUSIONS: Neonatal developmental delay in inhibition is associated with attentional problems as the child matures. Perinatal choline activates timely development of cerebral inhibition, even in the presence of gene mutations that otherwise delay it.
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A first randomized controlled trial confirmed the effect of perinatal phosphatidylcholine on an electrophysiological biomarker of foetal development.
“A first randomized controlled trial confirmed the effect of perinatal phosphatidylcholine on an electrophysiological biomarker of foetal development 164”
From Preventive psychiatry: a blueprint for improving the mental health of young people (2021) · cites this paper as [164]
Neurodevelopmental biomarkers have no available data on association with psychotic disorders.
“Neurodevelopmental biomarkers (data not available) 164,165,167 *”
From Preventive psychiatry: a blueprint for improving the mental health of young people (2021) · cites this paper as [164]
Perinatal phosphatidylcholine modulates biomarkers of neonatal brain development.
“Perinatal phosphatidylcholine (modulated biomarkers of neonatal brain development 164 *; fewer attention problems and less social withdrawal 165 *)”
From Preventive psychiatry: a blueprint for improving the mental health of young people (2021) · cites this paper as [164]
Perinatal phosphatidylcholine and N-acetylcysteine administration are effective universal prevention interventions to support infants' brain development and anti-inflammatory neuroprotection.
“perinatal phosphatidylcholine [54] and N-acetylcysteine [55] administration to support infants’ brain development and anti-inflammatory neuroprotection”
From Prevention and early intervention in youth mental health: is it time for a multidisciplinary and trans-diagnostic model for care? (2020) · cites this paper as [54]
Dietary supplementation of choline stimulates the development of cerebral inhibition as measured by P50 inhibition after birth.
“Dietary supplementation of choline stimulates the development of cerebral inhibition as measured by P50 inhibition after birth (44).”
From Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia (2015) · cites this paper as [44]
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Alpha7 Nicotinic Receptors as Therapeutic Targets in Schizophrenia
Tregellas, J. R., & Wylie, K. P. (2018) · Nicotine & Tobacco Research · doi:10.1093/ntr/nty034 · Cited by 87 · see citing works
Uher, R., Cumby, J., MacKenzie, L. E., Morash-Conway, J., Glover, J. M., Aylott, A., Propper, L., Abidi, S., Bagnell, A. L., Pavlová, B., et al. (2014) · BMC Psychiatry · doi:10.1186/s12888-014-0344-2 · Cited by 85 · see citing works
“Another type of safe and potentially effective interventions are dietary supplements, such as polyunsaturated fatty acids, vitamin D and choline, which have evidence for beneficial effects on neurodevelopment [25,143,144].”
The Duplicated α7 Subunits Assemble and Form Functional Nicotinic Receptors with the Full-length α7
Wang, Y., Xiao, C., Indersmitten, T., Freedman, R., Leonard, S. S., & Lester, H. A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.582858 · Cited by 85 · see citing works
“Genetic and neurobiological studies suggest that choline availability may contribute to the development of schizophreniaassociated sensory gating deficits (62), and perinatal dietary choline supplementation has been tested for lowering schizophrenia risk, with positive results (63).”
BackgroundSelf-citationAdams, J. B., Kirby, J. K., Sorensen, J. C., Pollard, E. L., & AUDHYA, T. K. (2022) · Maternal Health Neonatology and Perinatology · doi:10.1186/s40748-022-00139-9 · Cited by 93 · see citing works
“One study [128] that involved supplementing pregnant women with 900 mg/day of choline (as phosphatidylcholine) found it was safe, and helped increase cerebral inhibition in the infant at 5 weeks (but not at 13 weeks), which may be relevant to risk of schizophrenia.”
BackgroundFetal programming of schizophrenia: Select mechanisms
Debnath, M., Venkatasubramanian, G., & Berk, M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.003 · Cited by 84 · see citing works
“After birth, infants were given 00 mg of phosphatidylcholine in an oral suspension once daily r placebo (Ross et al., 2013).”
MethodChuhma, N., Mingote, S., Kalmbach, A., Yetnikoff, L., & Rayport, S. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.07.002 · Cited by 82 · see citing works
“Evidence for the extends from linkage to the α7 nicotinic receptor (80), extensive use of nicotine by patients (81), therapeutic potential of nicotinic cholinergic agonists (82), etiologic evidence for early developmental alterations in cholinergic balance (83), and postmortem evidence for altered cholinergic signalin…”
BackgroundNeurodevelopmental Factors in Schizophrenia
Jaaro-Peled, H., & Sawa, A. (2020) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2020.02.010 · Cited by 78 · see citing works
Prenatal Amino Acid Supplementation to Improve Fetal Growth: A Systematic Review and Meta-Analysis
Terstappen, F., Tol, A. J. C., Gremmels, H., Wever, K. E., Paauw, N. D., Joles, J. A., van der Beek, E. M., & Lely, A. T. (2020) · Nutrients · doi:10.3390/nu12092535 · Cited by 82 · see citing works
“Effect of Prenatal Methyl Donors on Prevention of Pregnancy Complications in Risk Population Study Characteristics Prevention of pregnancy complications in a human risk population was studied using choline (n = 2, USA and South Africa) [135,138] and cysteine (n = 2, Egypt and The Netherlands) [134,137] (Table A7).”
BackgroundMethodInfluentialIrvine, N., England-Mason, G., Field, C. J., Dewey, D., & Aghajafari, F. (2022) · Nutrients · doi:10.3390/nu14020364 · Cited by 71 · see citing works
Obeid, R., Derbyshire, E. J., & Schön, C. (2022) · Advances in Nutrition · doi:10.1093/advances/nmac082 · Cited by 70 · see citing works
“The inhibition of the auditory P50 cerebral evoked response was defined as the amplitude of the P50 response to the second of paired auditory stimuli divided by the amplitude of the response to the first stimulus (40).”
BackgroundMethodInfluentialNew Targets for Prevention of Schizophrenia: Is It Time for Interventions in the Premorbid Phase?
Seidman, L. J., & Nordentoft, M. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv050 · Cited by 65 · see citing works
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Changes in Human Milk Fat Globule Composition Throughout Lactation: A Review
Thum, C., Wall, C. R., Day, L., Szeto, I. M. Y., Li, F., Yan, Y., & Barnett, M. P. G. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.835856 · Cited by 60 · see citing works
Mellott, T. J., Huleatt, O. M., Shade, B. N., Pender, S. M., Liu, Y. B., Slack, B. E., & Blusztajn, J. K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170450 · Cited by 53 · see citing works
Male fetus susceptibility to maternal inflammation: C-reactive protein and brain development
Hunter, S. K., Hoffman, M. C., D’Alessandro, A., Noonan, K., Wyrwa, A., Freedman, R., & Law, A. J. (2019) · Psychological Medicine · doi:10.1017/s0033291719003313 · Cited by 57 · see citing works
“Increased maternal choline promotes the development of newborn P50 inhibitory gating, and therefore, we also assessed the possible interaction of the maternal inflammatory response with choline in this study (Ross et al., 2013).”
BackgroundInfluentialSelf-citationNutritional Factors in Fetal and Infant Brain Development
Cheatham, C. L. (2019) · Annals of Nutrition and Metabolism · doi:10.1159/000508052 · Cited by 56 · see citing works
Bahnfleth, C. L., Strupp, B. J., Caudill, M. A., & Canfield, R. L. (2021) · The FASEB Journal · doi:10.1096/fj.202101217r · Cited by 55 · see citing works
Prenatal Primary Prevention of Mental Illness by Micronutrient Supplements in Pregnancy
Freedman, R., Hunter, S. K., & Hoffman, M. C. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2018.17070836 · Cited by 56 · see citing works
“(29, 30) 100 women United States 6,300 mg of”
Self-citationA Comprehensive Review of Eggs, Choline, and Lutein on Cognition Across the Life-span
Wallace, T. C. (2018) · Journal of the American College of Nutrition · doi:10.1080/07315724.2017.1423248 · Cited by 54 · see citing works
“A CHRNA7 genotype associated with schizophrenia diminished P50 inhibition in the placebo-treated infants, but not the choline-treated infants (50).”
BackgroundCholine: The Neurocognitive Essential Nutrient of Interest to Obstetricians and Gynecologists
Wallace, T. C., Blusztajn, J. K., Caudill, M. A., Klatt, K. C., & Zeisel, S. H. (2019) · Journal of Dietary Supplements · doi:10.1080/19390211.2019.1639875 · Cited by 54 · see citing works
Common Genetic Variants Alter Metabolism and Influence Dietary Choline Requirements
Ganz, A. B., Klatt, K. C., & Caudill, M. A. (2017) · Nutrients · doi:10.3390/nu9080837 · Cited by 53 · see citing works
“For example, dietary choline intakes higher than the current AI consumed during pregnancy may improve infant cognition [29,30] and positively influence pregnancy-related biomarkers [31,32].”
BackgroundCholine and the Brain: An Epigenetic Perspective
Bekdash, R. A. (2016) · Advances in neurobiology · doi:10.1007/978-3-319-28383-8_21 · Cited by 50 · see citing works
Higher Gestational Choline Levels in Maternal Infection Are Protective for Infant Brain Development
Freedman, R., Hunter, S. K., Law, A. J., Wagner, B. D., D’Alessandro, A., Christians, U., Noonan, K., Wyrwa, A., & Hoffman, M. C. (2019) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2018.12.010 · Cited by 47 · see citing works
“auditory-evoked response inhibition, a biomarker of the prenatal development of inhibitory neurocircuits that showed negative effects of familial risk and positive effects of choline in previous studies, and then infant behavior.(27,31)”
InfluentialSelf-citationHeland, S., Fields, N. J., Ellery, S. J., Fahey, M. C., & Palmer, K. R. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.992120 · Cited by 49 · see citing works
“A study with maternal and infant choline supplementation from the second trimester through to the third month postpartum showed that supplementation may be associated with better sensory gating (52).”
BackgroundPrenatal and Postnatal Choline Supplementation in Fetal Alcohol Spectrum Disorder
Ernst, A. M., Gimbel, B. A., de Water, E., Eckerle, J. K., Radke, J. P., Georgieff, M., & Wozniak, J. R. (2022) · Nutrients · doi:10.3390/nu14030688 · Cited by 46 · see citing works
Schulz, K. M., Pearson-Smith, J. N., Gasparrini, M. E., Brooks, K. F., Drake-Frazier, C., Zajkowski, M. E., Kreisler, A. D., Adams, C. E., Leonard, S. S., & Stevens, K. E. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.03.031 · Cited by 41 · see citing works
“First, perinatal choline supplementation facilitates alpha7*-dependent brain inhibitory function in infants [21].”
BackgroundSelf-citationCholine the brain and neurodegeneration insights from epigenetics
Bekdash, R. A. (2017) · Frontiers in bioscience · doi:10.2741/4636 · Cited by 41 · see citing works
“Prenatal or perinatal choline supplementation may mitigate some of the symptoms that are often associated with neurological disorders including Schizophrenia (15,16), Down’s syndrome (17), Rett syndrome (18–21) and Alzheimer’s disease (22) and have neuroprotective effects against brain insults including seizures (23–2…”
BackgroundCao, M., ChunJin, L., Liu, Y., Cai, K., Chen, L., Yuan, C., Zhao, Z., Zhang, B., Hou, R., & Zhou, X. Z. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00215 · Cited by 41 · see citing works
“Infant brain development can be improved bymaternal supplementation with phosphatidylcholine, a choline metabolite, during pregnancy (33).”
BackgroundSørensen, H. J., Debost, J.-C., Agerbo, E., Benros, M. E., McGrath, J. J., Mortensen, P. B., Ranning, A., Hjorthøj, C. R., Mors, O. N., Nordentoft, M., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.04.012 · Cited by 38 · see citing works
Grothe, M. J., Scheef, L., Bäuml, J., Meng, C., Daamen, M., Baumann, N., Zimmer, C., Teipel, S. J., Bartmann, P., Boecker, H., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.12.008 · Cited by 37 · see citing works
“Interestingly, a recent placebo-controlled trial of perinatal dietary choline supplementation in healthy women demonstrated a positive effect on a psychophysiologic outcome marker related to cholinergic system development and schizophrenia risk (46).”
Systematic review and meta-analysis: Season of birth and schizophrenia risk
Coury, S. M., Lombroso, A., Avila-Quintero, V. J., Taylor, J. H., Flores, J. M., Szejko, N., & Bloch, M. H. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2022.12.016 · Cited by 37 · see citing works
Choline, folic acid, Vitamin D, and fetal brain development in the psychosis spectrum
Freedman, R., Hunter, S. K., Law, A. J., Clark, A. M., Roberts, A., & Hoffman, M. C. (2021) · Schizophrenia Research · doi:10.1016/j.schres.2021.03.008 · Cited by 36 · see citing works
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Lower cholinergic basal forebrain volumes link with cognitive difficulties in schizophrenia
Avram, M., Grothe, M. J., Meinhold, L., Leucht, C., Leucht, S., Borgwardt, S., Brandl, F., & Sorg, C. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01070-x · Cited by 34 · see citing works
Nutrition and Brain Development
Cusick, S. E., Barks, A. K., & Georgieff, M. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_244 · Cited by 37 · see citing works
Hall, M., Chen, C., Cohen, B. M., Spencer, K., Levy, D. L., Öngür, D., & Smoller, J. W. (2015) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32298 · Cited by 33 · see citing works
Effects of Maternal Prenatal Stress: Mechanisms, Implications, and Novel Therapeutic Interventions
Tobón, A. L., Diaz‐Stransky, A., Ross, D. A., & Stevens, H. E. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.09.011 · Cited by 31 · see citing works
Socha, M. W., Flis, W., & Wartęga, M. (2024) · Nutrients · doi:10.3390/nu16050678 · Cited by 32 · see citing works
“It is hypothesized that perinatal choline supplementation may prevent the occurrence of cognitive disorders (such as ASD) or mental illnesses such as schizophrenia [103].”
BackgroundSmucny, J., Stevens, K. E., Olincy, A., & Tregellas, J. R. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.77 · Cited by 28 · see citing works
Self-citationRaising attention to attention deficit hyperactivity disorder in schizophrenia
Pallanti, S. (2015) · World Journal of Psychiatry · doi:10.5498/wjp.v5.i1.47 · Cited by 31 · see citing works
Alldred, M. J., Chao, H. M., Lee, S. H., Beilin, J., Powers, B. E., Petkova, E., Strupp, B. J., & Ginsberg, S. D. (2019) · The FASEB Journal · doi:10.1096/fj.201802669rr · Cited by 29 · see citing works
“Another human trial utilized the choline metabolite PC as a perinatal supplement, which also showed cognitive improvement in infants (17).”
MethodPrenatal choline and the development of schizophrenia.
Freedman, R., & Ross, R. G. (2015) · Europe PMC (PubMed Central) · doi:10.11919/j.issn.1002-0829.215006 · Cited by 29 · see citing works
“All women who participated in the randomized clinical trial of choline supplementation discussed in this review([17]) provided written informed consent to participate in the project.”
BackgroundMethodResultInfluentialSelf-citationDeutsch, S. I., & Burket, J. A. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_136 · Cited by 27 · see citing works
Knott, V., Smith, D., de la Salle, S., Impey, D., Choueiry, J., Beaudry, E., Smith, M. K., Saghir, S., Ilivitsky, V., & Labelle, A. (2014) · Journal of Psychopharmacology · doi:10.1177/0269881114553254 · Cited by 27 · see citing works
“infants whose mothers were treated with choline during pregnancy (beginning in the second trimester and continuing with the newborn through the third postnatal month) also showed an increased rate of efficient P50 suppression compared to infants of mothers treated with placebo (Ross et al., 2013).”
ResultCharacterization of choline transporters in the human placenta over gestation
Baumgartner, H. K., Trinder, K. M., Galimanis, C. E., Post, A. L., Phang, T. L., Ross, R. G., & Winn, V. D. (2015) · Placenta · doi:10.1016/j.placenta.2015.10.001 · Cited by 27 · see citing works
“Infants from mothers supplemented with phosphatidylcholine, as a choline source, during pregnancy showed improved cerebral inhibition as measured by electroencephalographic P50 ratio [16].”
MethodSelf-citationStevens, K. E., Choo, K. S., Stitzel, J. A., Marks, M. J., & Adams, C. E. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.022 · Cited by 26 · see citing works
“In both cases, gestational choline supplementation improved sensory inhibition in supplemented offspring (Stevens et al 2008; Ross et al 2013, respectively).”
BackgroundInfluentialSelf-citationHunter, S. K., Hoffman, M. C., D’Alessandro, A., Wyrwa, A., Noonan, K., Zeisel, S. H., Law, A. J., & Freedman, R. (2021) · Psychological Medicine · doi:10.1017/s0033291720005061 · Cited by 26 · see citing works
“…trial of prenatal choline supplementation beginning by 15 weeks of gestation that compared 7300mg phosphatidylcholine, equivalent to 900mg choline, to placebo to test the hypothesis that choline supplementation would enhance the development of cerebral inhibitory function (Ross et al., 2013).”
MethodSelf-citationKnott, V., Impey, D., Choueiry, J., Smith, D., de la Salle, S., Saghir, S., Smith, M. K., Beaudry, E., Ilivitsky, V., & Labelle, A. (2015) · Neuropsychiatric Electrophysiology · doi:10.1186/s40810-014-0002-4 · Cited by 26 · see citing works
“human infants whose mothers’ diets during pregnancy were supplemented with choline (Ross et al. 2013), dietary choline supplementation has been promoted as a possible pre-”
BackgroundBuhusi, M. C., Scripa, I., Williams, C. L., & Buhusi, C. V. (2013) · Timing & Time Perception · doi:10.1163/22134468-00002003 · Cited by 24 · see citing works
“…(prepulse inhibition) (Irintchev, Koch, Needham, Maness, & Schachner, 2004; Morellini, Lepsveridze, Kahler, Dityatev, & Schachner, 2007) as also reported in schizophrenia patients (Delerue & Boucart, 2012a, 2012b; Hammer et al., 2013; Ross et al., 2013; Velasques et al., 2011; Wang et al., 2013).”
BackgroundFood Insecurity as a Social Determinant of Mental Health
Compton, M. T. (2014) · Psychiatric Annals · doi:10.3928/00485713-20140108-08 · Cited by 28 · see citing works
Interaction of maternal choline levels and prenatal Marijuana's effects on the offspring
Hoffman, M. C., Hunter, S. K., D’Alessandro, A., Noonan, K., Wyrwa, A., & Freedman, R. (2019) · Psychological Medicine · doi:10.1017/s003329171900179x · Cited by 24 · see citing works
Self-citationLouck, L. E., Cara, K. C., Klatt, K. C., Wallace, T. C., & Chung, M. C. (2023) · Advances in Nutrition · doi:10.1016/j.advnut.2023.100164 · Cited by 22 · see citing works
Choline in pregnant women: a systematic review and meta-analysis
Nguyen, H. T., Oktayani, P. P. I., Lee, S., & Huang, L. (2024) · Nutrition Reviews · doi:10.1093/nutrit/nuae026 · Cited by 22 · see citing works
The Importance of Gut Microbiota on Choline Metabolism in Neurodegenerative Diseases
Eslami, M., Alibabaei, F., Babaeizad, A., Banihashemian, S. Z., Mazandarani, M., Hoseini, A., Ramezankhah, M., Oksenych, V., & Yousefi, B. (2024) · Biomolecules · doi:10.3390/biom14111345 · Cited by 22 · see citing works
Advances in clinical staging, early intervention, and the prevention of psychosis
Gupta, T., & Mittal, V. A. (2019) · F1000Research · doi:10.12688/f1000research.20346.1 · Cited by 22 · see citing works
“Growing research indicates that choline-enhancing diets (which may decrease effects of mother’s infections on fetal brain development) for pregnant women may be a means to protect against neural and cognitive deficits in offspring 73,74 .”
BackgroundFalk, E. N., Norman, K. J., Garkun, Y., Demars, M. P., Im, S., Taccheri, G., Short, J., Caro, K., McCraney, S. E., Cho, C., et al. (2021) · Science Advances · doi:10.1126/sciadv.abe1527 · Cited by 22 · see citing works
Development of a Choline Database to Estimate Australian Population Intakes
Probst, Y., Guan, V. X., & Neale, E. P. (2019) · Nutrients · doi:10.3390/nu11040913 · Cited by 21 · see citing works
“The literature suggests that maternal choline supplementation is positively related to offspring neurocognitive outcomes [6,7].”
Inadequate Choline Intake in Pregnant Women in Germany
Roeren, M., Kordowski, A., Sina, C., & Smollich, M. (2022) · Nutrients · doi:10.3390/nu14224862 · Cited by 21 · see citing works
Choline – a scoping review for Nordic Nutrition Recommendations 2023
Obeid, R., & Karlsson, T. (2023) · Food & Nutrition Research · doi:10.29219/fnr.v67.10359 · Cited by 21 · see citing works
“RCTs support positive effects of maternal choline supply on some domains of child neurodevelopment (self-regulation) and neurocognition (learning and memory) (57–59).”
BackgroundPresent and future of developmental neuropsychopharmacology
Arango, C. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.11.003 · Cited by 21 · see citing works
“Therefore the administration of choline would prevent the neonatal developmental delay in inhibition associated with attentional problems as the child matures (Ross et al., 2013).”
BackgroundChoueiry, J., Blais, C. M., Shah, D. K., Smith, D., Fisher, D. J., Labelle, A., & Knott, V. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2019.02.005 · Cited by 20 · see citing works
Dhavamani, S., Park, J. C., McAnany, J. J., Kim, T.-H., Ma, G., Yao, X., Antharavally, B. S., Oroskar, A. R., Oroskar, A. A., Layden, B. T., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-36268-0 · Cited by 20 · see citing works
Maternal Nutrition during Pregnancy and Offspring Brain Development: Insights from Neuroimaging
Na, X., Mackean, P. P., Cape, G. A., Johnson, J. W., & Ou, X. (2024) · Nutrients · doi:10.3390/nu16193337 · Cited by 22 · see citing works
“Another study found that in the presence of gene mutations that may delay infant inhibition, choline-treated infants aged ~1 month showed better outcomes as reflected by P50 inhibition suppression ratio [47].”
BackgroundCholinergic modulation of sensory perception and plasticity
Kunnath, A. J., Gifford, R. H., & Wallace, M. T. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105323 · Cited by 19 · see citing works
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Syndrome of High Academic Loads in School-Aged Children and Adolescents
Karkashadze, G. A., Namazova-Baranova, L. S., Zakharova, I. N., Makarova, S. G., & Маслова, О. И. (2017) · Педиатрическая фармакология · doi:10.15690/pf.v14i1.1697 · Cited by 18 · see citing works
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Christifano, D. N., Chollet‐Hinton, L., Hoyer, D., Schmidt, A., & Gustafson, K. M. (2022) · Nutritional Neuroscience · doi:10.1080/1028415x.2022.2088944 · Cited by 16 · see citing works
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Endophenotypes in Schizophrenia for the Perinatal Period: Criteria for Validation
Ross, R. G., & Freedman, R. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv054 · Cited by 15 · see citing works
Self-citationAllen, S. J., & Morishita, H. (2024) · Science Advances · doi:10.1126/sciadv.adh3920 · Cited by 13 · see citing works
“…is tightly balanced through a multilayered set of mechanisms across early development: regulation of developing cortex through fetal choline level ( 66 ), cholinergic innervation from basal forebrain ( 67 ), and the expression level of nAChRs ( 68 ) during the first three postnatal weeks in…”
BackgroundHunter, S. K., Hoffman, M. C., D’Alessandro, A., Walker, V. K., Balser, M., Noonan, K., Law, A. J., & Freedman, R. (2021) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2021.06.037 · Cited by 14 · see citing works
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“Since Ross et al. had conducted a randomized placebo-controlled clinical trial using supplementation of phosphatidylcholine successfully (Ross et al. 2013), the boy was put on a daily supplement of one capsule of the supplement (1000 mg) containing the following: phosphatidylcholine 600 mg, Vitamin…”
MethodInfluentialRomano, E., Angelis, F. D., Ulbrich, L., Jaco, A. D., Fuso, A., & Giovanni Laviola, A. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3388-y · Cited by 12 · see citing works
Future Directions in Choline: From Neurodevelopment to Cardiometabolic Health
Paules, E. M., Petry, H. G., Sprinkles, J., & Trujillo‐Gonzalez, I. (2025) · Nutrients · doi:10.3390/nu17223618 · Cited by 9 · see citing works
“Current trials vary widely in design, with some comparing 930 mg/day to 480 mg/day during the third trimester of pregnancy [7] and others providing 900 mg/day from week 16 of gestation through delivery, followed by 100 mg/day to infants [50,51].”
- Authors
- Ross, R. G., Hunter, S. K., McCarthy, L., Beuler, J., Hutchison, A. K., Wagner, B. D., Leonard, S., Stevens, K. E., & Freedman, R.
- Affiliations
- University of Colorado Denver (US)
- Venue
- American Journal of Psychiatry
- Published
- 2013-03
- Volume
- 170
- Issue
- 3
- Pages
- 290-298
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- PMC
- PMC3640283
- OpenAlex
- W2170922033
- Cited by
- 165
- References
- 45
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 7 · 2023: 10 · 2022: 14 · 2021: 17 · 2020: 17 · 2019: 17 · 2018: 6 · 2017: 9 · 2016: 11 · 2015: 16 · 2014: 13 · 2013: 11
- FWCI
- 12.05
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- American Journal of Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (P50MH086383, R01MH056539)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Keywords
- phosphatidylcholine, schizophrenia risk, sensory gating, alpha7 nicotinic acetylcholine receptor, maternal nutrition, infant brain development, attention
- MeSH terms
- Attention, Brain, Child, Preschool, Choline, DNA Mutational Analysis, Electroencephalography, Female, Follow-Up Studies, Genotype, Humans, Infant, Infant, Newborn, Male, Neural Inhibition, Phosphorylcholine, Pregnancy, Receptors, Nicotinic, Schizophrenia, Signal Processing, Computer-Assisted, Randomized Controlled Trials as Topic, Nootropic Agents, Perinatal Care, Genetic Predisposition to Disease, Sensory Gating, alpha7 Nicotinic Acetylcholine Receptor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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