In utero MRI identifies consequences of early-gestation alcohol drinking on fetal brain development in rhesus macaques
Open accessAbstract
One factor that contributes to the high prevalence of fetal alcohol spectrum disorder (FASD) is binge-like consumption of alcohol before pregnancy awareness. It is known that treatments are more effective with early recognition of FASD. Recent advances in retrospective motion correction for the reconstruction of three-dimensional (3D) fetal brain MRI have led to significant improvements in the quality and resolution of anatomical and diffusion MRI of the fetal brain. Here, a rhesus macaque model of FASD, involving oral self-administration of 1.5 g/kg ethanol per day beginning prior to pregnancy and extending through the first 60 d of a 168-d gestational term, was utilized to determine whether fetal MRI could detect alcohol-induced abnormalities in brain development. This approach revealed differences between ethanol-exposed and control fetuses at gestation day 135 (G135), but not G110 or G85. At G135, ethanol-exposed fetuses had reduced brainstem and cerebellum volume and water diffusion anisotropy in several white matter tracts, compared to controls. Ex vivo electrophysiological recordings performed on fetal brain tissue obtained immediately following MRI demonstrated that the structural abnormalities observed at G135 are of functional significance. Specifically, spontaneous excitatory postsynaptic current amplitudes measured from individual neurons in the primary somatosensory cortex and putamen strongly correlated with diffusion anisotropy in the white matter tracts that connect these structures. These findings demonstrate that exposure to ethanol early in gestation perturbs development of brain regions associated with motor control in a manner that is detectable with fetal MRI.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MRI studies showed reductions in brainstem as well as cerebellum volume in a primate FAS model and a sex-dependent change in functional connectivity and metabolism in prefrontal areas in a rat FAS model.
“MRI studies showed reductions in brainstem as well as cerebellum volume in a primate FAS model and a sex-dependent change in functional connectivity and metabolism in prefrontal areas in a rat FAS model [317, 318].”
From Development of prefrontal cortex (2022) · cites this paper as [318]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.015 · Cited by 11,314 · see citing works
Adjusting batch effects in microarray expression data using empirical Bayes methods
Johnson, W. E., Li, C., & Rabinovic, A. (2007) · Biostatistics · doi:10.1093/biostatistics/kxj037 · Cited by 8,658 · see citing works
Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C., Watkins, K., Ciccarelli, O., Cader, M., Matthews, P., et al. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.02.024 · Cited by 6,035 · see citing works
Avants, B., Epstein, C. L., Grossman, M., & Gee, J. C. (2007) · Medical Image Analysis · doi:10.1016/j.media.2007.06.004 · Cited by 5,618 · see citing works
SMITH, S., & NICHOLS, T. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.061 · Cited by 5,250 · see citing works
A reproducible evaluation of ANTs similarity metric performance in brain image registration
Avants, B. B., Tustison, N. J., Song, G., Cook, P. A., Klein, A., & Gee, J. C. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.09.025 · Cited by 4,796 · see citing works
Permutation inference for the general linear model
Winkler, A. M., Ridgway, G. R., Webster, M. A., Smith, S. M., & Nichols, T. E. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.01.060 · Cited by 3,563 · see citing works
Declines in Unintended Pregnancy in the United States, 2008–2011
Finer, L. B., & Zolna, M. R. (2016) · New England Journal of Medicine · doi:10.1056/nejmsa1506575 · Cited by 1,989 · see citing works
Risk Factors for Adverse Life Outcomes in Fetal Alcohol Syndrome and Fetal Alcohol Effects
STREISSGUTH, A. P., BOOKSTEIN, F. L., BARR, H. M., SAMPSON, P. D., O'MALLEY, K., & YOUNG, J. K. (2004) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/00004703-200408000-00002 · Cited by 1,195 · see citing works
Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood
Lebel, C., & Beaulieu, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5302-10.2011 · Cited by 1,193 · see citing works
Deterministic diffusion fiber tracking improved by quantitative anisotropy
Yeh, F.-C., Verstynen, T. D., Wang, Y., Fernández-Miranda, J. C., & Tseng, W.-Y. I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080713 · Cited by 1,121 · see citing works
The Corsini encyclopedia of psychology
(2010) · Choice Reviews Online · doi:10.5860/choice.47-6008 · Cited by 1,082 · see citing works
Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P. S., & Hertz-Pannier, L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.044 · Cited by 851 · see citing works
Modeling transformations of neurodevelopmental sequences across mammalian species
Workman, A. D., Charvet, C. J., Clancy, B., Darlington, R. B., & Finlay, B. L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5746-12.2013 · Cited by 833 · see citing works
Prevalence of Fetal Alcohol Spectrum Disorders in 4 US Communities
May, P. A., Chambers, C., Kalberg, W. O., Zellner, J. A., Feldman, H. S., Buckley, D. G., Kopald, D., Hasken, J. M., Xu, R., Honerkamp‐Smith, G., et al. (2018) · JAMA · doi:10.1001/jama.2017.21896 · Cited by 810 · see citing works
Global Prevalence of Fetal Alcohol Spectrum Disorder Among Children and Youth
Lange, S., Probst, C., Gmel, G. E., Rehm, J. T., Burd, L., & Popova, S. (2017) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2017.1919 · Cited by 675 · see citing works
Neil, J. J., Shiran, S. I., McKinstry, R. C., Schefft, G. L., Snyder, A. Z., Almli, C. R., Akbudak, E., Aronovitz, J. A., Miller, J. P., Lee, B. C., et al. (1998) · Radiology · doi:10.1148/radiology.209.1.9769812 · Cited by 645 · see citing works
Brain dysmorphology in individuals with severe prenatal alcohol exposure
Archibald, S. L., Fennema‐Notestine, C., Gamst, A. C., Riley, E. P., Mattson, S. N., & Jernigan, T. L. (2001) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2001.tb00179.x · Cited by 510 · see citing works
Ketamine-induced Neuroapoptosis in the Fetal and Neonatal Rhesus Macaque Brain
Brambrink, A. M., Evers, A. S., Avidan, M. S., Farber, N. B., Smith, D. J., Martin, L. D., Dissen, G. A., Creeley, C. E., & Olney, J. W. (2012) · Anesthesiology · doi:10.1097/aln.0b013e318242b2cd · Cited by 427 · see citing works
Mukherjee, P., Miller, J. H., Shimony, J. S., Conturo, T. E., Lee, B. C. P., Almli, C. R., & McKinstry, R. C. (2001) · Radiology · doi:10.1148/radiol.2212001702 · Cited by 426 · see citing works
Bauer-Moffett, C., & Altman, J. (1977) · Brain Research · doi:10.1016/0006-8993(77)90310-9 · Cited by 268 · see citing works
Isoflurane‐induced apoptosis of oligodendrocytes in the neonatal primate brain
Brambrink, A. M., Back, S. A., Riddle, A., Gong, X., Moravec, M. D., Dissen, G. A., Creeley, C. E., Dikranian, K. T., & Olney, J. W. (2012) · Annals of Neurology · doi:10.1002/ana.23652 · Cited by 264 · see citing works
Astley, S. J., Aylward, E., Olson, H. C., Kerns, K. A., Brooks, A., Coggins, T. E., Davies, J. K., Dorn, S., Gendler, B., Jirikowic, T., et al. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.01004.x · Cited by 243 · see citing works
Sowell, E. R., Jernigan, T. L., Mattson, S. N., Riley, E. P., Sobel, D. F., & Jones, K. L. (1996) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1996.tb01039.x · Cited by 241 · see citing works
Explicit B-spline regularization in diffeomorphic image registration
Tustison, N. J., & Avants, B. (2013) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2013.00039 · Cited by 224 · see citing works
Goodlett, C. R., Marcussen, B. L., & West, J. R. (1990) · Alcohol · doi:10.1016/0741-8329(90)90070-s · Cited by 220 · see citing works
In utero tractography of fetal white matter development
Kasprian, G. J., Brugger, P. C., Weber, M., Krššák, M., Krampl, E., Herold, C., & Prayer, D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.07.026 · Cited by 218 · see citing works
Brain Diffusion Abnormalities in Children With Fetal Alcohol Spectrum Disorder
Lebel, C. A., Rasmussen, C., Wyper, K., Walker, L., Andrew, G., Yager, J. Y., & Beaulieu, C. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00750.x · Cited by 215 · see citing works
Grant, K. A., Leng, X., Green, H. L., Szeliga, K. T., Rogers, L. S. M., & Gonzales, S. W. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00765.x · Cited by 204 · see citing works
Self-citationZika virus infection in pregnant rhesus macaques causes placental dysfunction and immunopathology
Hirsch, A. J., Roberts, V. H. J., Grigsby, P. L., Haese, N. N., Schabel, M. C., Wang, X., Lo, J. O.-T., Liu, Z., Kroenke, C. D., Smith, J. L., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02499-9 · Cited by 203 · see citing works
Self-citationSowell, E. R., Johnson, A., Kan, E., Lu, L. H., Horn, J. D. V., Toga, A. W., O’Connor, M. J., & Bookheimer, S. Y. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5067-07.2008 · Cited by 190 · see citing works
Prenatal stress has long‐term effects on behavioral responses to stress in juvenile rhesus monkeys
Clarke, A. S., & Schneider, M. L. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260506 · Cited by 187 · see citing works
Donald, K. A., Eastman, E., Howells, F. M., Adnams, C., Riley, E. P., Woods, R. P., Narr, K. L., & Stein, D. J. (2015) · Acta Neuropsychiatrica · doi:10.1017/neu.2015.12 · Cited by 185 · see citing works
MRI findings in children with school problems who had been exposed prenatally to alcohol
Autti‐Rämö, I., Autti, T. H., Korkman, M., Kettunen, S., Salonen, O. L. M., & Valanne, L. K. (2002) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162201001748 · Cited by 177 · see citing works
Vivian, J. A., Green, H. L., Young, J. E., Majerksy, L. S., Thomas, B. W., Shively, C. A., Tobin, J. R., Nader, M. A., & Grant, K. A. (2001) · Alcoholism Clinical and Experimental Research · doi:10.1097/00000374-200108000-00001 · Cited by 176 · see citing works
Self-citationIntersection Based Motion Correction of Multislice MRI for 3-D in Utero Fetal Brain Image Formation
Kim, K., Habas, P. A., Rousseau, F., Glenn, O. A., Barkovich, A. J., & Studholme, C. (2009) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2009.2030679 · Cited by 171 · see citing works
Self-citationComplex Trajectories of Brain Development in the Healthy Human Fetus
Andescavage, N. N., du Plessis, A., McCarter, R., Serag, A., Evangelou, I., Vezina, G., Robertson, R., & Limperopoulos, C. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw306 · Cited by 163 · see citing works
Maier, S. E., & West, J. R. (2001) · Alcohol · doi:10.1016/s0741-8329(00)00133-6 · Cited by 159 · see citing works
Parnell, S. E., O’Leary‐Moore, S. K., Godin, E. A., Dehart, D. B., Johnson, B. W., Johnson, G. A., Styner, M. A., & Sulik, K. K. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.00921.x · Cited by 156 · see citing works
Brain perfusion SPECT and MRI in foetal alcohol syndrome
Riikonen, R., Salonen, I., Partanen, K. P. L., & Verho, S. (1999) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162299001358 · Cited by 151 · see citing works
Denny, C. H., Acero, C. S., Naimi, T. S., et al. (2019) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6816a1 · Cited by 151 · see citing works
Waldorf, K. M. A., Nelson, B. R., Stencel-Baerenwald, J., Studholme, C., Kapur, R. P., Armistead, B., Walker, C. L., Merillat, S. A., Vornhagen, J., Tisoncik-Go, J., et al. (2018) · Nature Medicine · doi:10.1038/nm.4485 · Cited by 147 · see citing works
Self-citationPopova, S., Lange, S., Probst, C., Gmel, G. E., & Rehm, J. T. (2017) · Biochemistry and Cell Biology · doi:10.1139/bcb-2017-0077 · Cited by 135 · see citing works
Ma, X., Coles, C. D., Lynch, M. E., LaConte, S. M., Zurkiya, O., Wang, D., & Hu, X. P. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000171934.22755.6d · Cited by 131 · see citing works
Wozniak, J. R., Muetzel, R. L., Mueller, B. A., Petrenko, C. L. M., Freerks, M. A., Ward, E. E., Nelson, M. L., Chang, P., & Lim, K. O. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.01021.x · Cited by 130 · see citing works
Mapping cerebellar vermal morphology and cognitive correlates in prenatal alcohol exposure
O’Hare, E. D., Kan, E., Yoshii, J., Mattson, S. N., Riley, E. P., Thompson, P. M., Toga, A. W., & Sowell, E. R. (2005) · Neuroreport · doi:10.1097/01.wnr.0000176515.11723.a2 · Cited by 130 · see citing works
Carlson, V. C. C., Seabold, G. K., Helms, C. M., Garg, N., Odagiri, M., Rau, A. R., Daunais, J. B., Alvarez, V. A., Lovinger, D. M., & Grant, K. A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.140 · Cited by 126 · see citing works
Self-citationDiffusion tensor imaging in children with fetal alcohol spectrum disorders.
Wozniak, J., Mueller, B., Chang, P., Muetzel, R., Caros, L., & Lim, K. (2006) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2006.00213.x · Cited by 125 · see citing works
In utero alcohol exposure, epigenetic changes, and their consequences
Ungerer, M. (2013) · Alcohol research · doi:10.35946/arcr.v35.1.05 · Cited by 119 · see citing works
Scott, J. A., Habas, P. A., Kim, K., Rajagopalan, V., Hamzelou, K. S., Corbett‐Detig, J. M., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.04.001 · Cited by 119 · see citing works
Self-citationKhan, S., Vasung, L., Marami, B., Rollins, C. K., Afacan, O., Ortinau, C. M., Yang, E., Warfield, S. K., & Gholipour, A. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.08.030 · Cited by 115 · see citing works
Characterization of White Matter Microstructure in Fetal Alcohol Spectrum Disorders
Fryer, S. L., Schweinsburg, B. C., Bjorkquist, O. A., Frank, L. R., Mattson, S. N., Spadoni, A. D., & Riley, E. P. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00864.x · Cited by 108 · see citing works
Guo, W., Crossey, E. L., Zhang, L., Zucca, S., George, O. L., Valenzuela, C. F., & Zhao, X. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019351 · Cited by 99 · see citing works
White matter maturation of normal human fetal brain. An in vivo diffusion tensor tractography study
Zanin, É., Ranjeva, J., Sylviane Confort-gouny, A., Guye, M., Denis, D., Cozzone, P. J., & Girard, N. J. (2011) · Brain and Behavior · doi:10.1002/brb3.17 · Cited by 94 · see citing works
Studholme, C. (2011) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071910-124654 · Cited by 94 · see citing works
Self-citationHansen, M. F., Seshamani, S., Kroenke, C. D., Cheng, X. E., Chapman, T., Wilm, J., Rousseau, F., & Studholme, C. (2013) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2013.2284014 · Cited by 87 · see citing works
Self-citationIn Vivo Tractography of Fetal Association Fibers
Mitter, C., Prayer, D., Brugger, P. C., Weber, M., & Kasprian, G. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119536 · Cited by 78 · see citing works
Lo, J. O.-T., Schabel, M. C., Roberts, V. H. J., Wang, X., Lewandowski, K. S., Grant, K. A., Frias, A. E., & Kroenke, C. D. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.01.016 · Cited by 72 · see citing works
Self-citationFan, J., Jacobson, S. W., Taylor, P. A., Molteno, C. D., Dodge, N. C., Stanton, M. E., Jacobson, J. L., & Meintjes, E. M. (2016) · Human Brain Mapping · doi:10.1002/hbm.23218 · Cited by 67 · see citing works
Spottiswoode, B. S., Meintjes, E. M., Anderson, A. W., Molteno, C. D., Stanton, M. E., Dodge, N. C., Gore, J. C., Peterson, B. S., Jacobson, J. L., & Jacobson, S. W. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01566.x · Cited by 65 · see citing works
Treit, S., Chen, Z., Zhou, D., Baugh, L., Rasmussen, C., Andrew, G., Pei, J. R., & Beaulieu, C. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.05.006 · Cited by 63 · see citing works
Taylor, P. A., Jacobson, S. W., van der Kouwe, A. J. W., Molteno, C. D., Chen, G., Wintermark, P., Alhamud, A. A., Jacobson, J. L., & Meintjes, E. M. (2014) · Human Brain Mapping · doi:10.1002/hbm.22620 · Cited by 61 · see citing works
Magnetic resonance microscopy‐based analyses of the brains of normal and ethanol‐exposed fetal mice
O’Leary‐Moore, S. K., Parnell, S. E., Godin, E. A., Dehart, D. B., Ament, J. J., Khan, A. A., Johnson, G. A., Styner, M. A., & Sulik, K. K. (2010) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20719 · Cited by 61 · see citing works
Wang, X., Studholme, C., Grigsby, P. L., Frias, A. E., Carlson, V. C. C., & Kroenke, C. D. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3157-16.2017 · Cited by 58 · see citing works
Self-citationDonald, K. A., Roos, A., Fouché, J., Koen, N., Howells, F. M., Woods, R. P., Zar, H. J., Narr, K. L., & Stein, D. J. (2015) · Acta Neuropsychiatrica · doi:10.1017/neu.2015.35 · Cited by 57 · see citing works
Goodlett, C. R., Hamre, K. M., & West, J. R. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90133-j · Cited by 50 · see citing works
Nguyen, V. T., Chong, S., Tieng, Q. M., Mardon, K., Galloway, G. J., & Kurniawan, N. D. (2017) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2017.06.012 · Cited by 50 · see citing works
Parnell, S. E., Holloway, H. T., O'Leary-Moore, S. K., Dehart, D. B., Paniaqua, B., Oguz, I., Budin, F., Styner, M., Johnson, G., & Sulik, K. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2013.07.009 · Cited by 47 · see citing works
Parnell, S. E., Holloway, H., Baker, L. K., Styner, M. A., & Sulik, K. K. (2014) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12464 · Cited by 47 · see citing works
Novel Detection of Placental Insufficiency by Magnetic Resonance Imaging in the Nonhuman Primate
Lo, J. O.-T., Roberts, V. H. J., Schabel, M. C., Wang, X., Morgan, T. K., Liu, Z., Studholme, C., Kroenke, C. D., & Frias, A. E. (2017) · Reproductive Sciences · doi:10.1177/1933719117699704 · Cited by 47 · see citing works
Self-citationFan, J., Meintjes, E. M., Molteno, C. D., Spottiswoode, B. S., Dodge, N. C., Alhamud, A. A., Stanton, M. E., Peterson, B. S., Jacobson, J. L., & Jacobson, S. W. (2015) · Human Brain Mapping · doi:10.1002/hbm.22785 · Cited by 43 · see citing works
Maternal circulating miRNAs that predict infant FASD outcomes influence placental maturation
Tseng, A. M., Mahnke, A. H., Wells, A., Salem, N. A., Allan, A. M., Roberts, V. H. J., Newman, N., Walter, N. A. R., Kroenke, C. D., Grant, K. A., et al. (2019) · Life Science Alliance · doi:10.26508/lsa.201800252 · Cited by 43 · see citing works
Self-citationRamadoss, J., Lunde, E. R., Chen, W. A., West, J. R., & Cudd, T. A. (2007) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00477.x · Cited by 41 · see citing works
Leigland, L. A., Ford, M. M., Lerch, J. P., & Kroenke, C. D. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12051 · Cited by 41 · see citing works
Self-citationLiu, Z., Neuringer, M. D., Erdman, J. W., Kuchan, M. J., Renner, L. M., Johnson, E. E., Wang, X., & Kroenke, C. D. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.09.015 · Cited by 40 · see citing works
Self-citationKim, K., Habas, P. A., Rajagopalan, V., et al. (2011) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2011.2143724 · Cited by 39 · see citing works
Ramadoss, J., Lunde, E. R., Piña, K. B., et al. (2007) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00422.x · Cited by 37 · see citing works
Paolozza, A., Treit, S., Beaulieu, C., et al. (2016) · Human Brain Mapping · doi:10.1002/hbm.23371 · Cited by 36 · see citing works
Liu, Z., Wang, X., Newman, N., Grant, K. A., Studholme, C., & Kroenke, C. D. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116310 · Cited by 36 · see citing works
Self-citationCarlson, V. C. C., Grant, K. A., & Lovinger, D. M. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.12.010 · Cited by 34 · see citing works
Self-citationDelatour, L. C., Yeh, P. W. L., & Yeh, H. H. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy094 · Cited by 34 · see citing works
Sawant, O. B., Lunde, E. R., Washburn, S. E., Chen, W. A., Goodlett, C. R., & Cudd, T. A. (2012) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.11.001 · Cited by 33 · see citing works
Cardenas, V. A., Price, M., Infante, M. A., et al. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.01.002 · Cited by 32 · see citing works
Gestational alcohol exposure disrupts cognitive function and striatal circuits in adult offspring
Carlson, V. C. C., Gremel, C. M., & Lovinger, D. M. (2020) · Nature Communications · doi:10.1038/s41467-020-16385-4 · Cited by 26 · see citing works
Gestational Age at Birth and Brain White Matter Development in Term-Born Infants and Children
Ou, X., Glasier, C. M., Ramakrishnaiah, R. H., Kanfi, A., Rowell, A. C., Pivik, R. T., Andres, A., Cleves, M. A., & Badger, T. M. (2017) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5408 · Cited by 23 · see citing works
In-utero Three Dimension High Resolution Fetal Brain Diffusion Tensor Imaging
Jiang, S., Xue, H., Counsell, S. J., Anjari, M., Allsop, J. M., Rutherford, M., Rueckert, D., & Hajnal, J. V. (2007) · Springer eBooks · doi:10.1007/978-3-540-75757-3_3 · Cited by 21 · see citing works
Enhancement of developmental toxicity effects of chemicals by gestational stress. A review
Hougaard, K. S., & Hansen, Å. M. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2007.02.003 · Cited by 21 · see citing works
Jimenez, V. A., Wang, X., Newman, N., Walter, N. A. R., Gonzales, S. W., Lo, J. O.-T., Ford, M. M., Carlson, V. C. C., Grant, K. A., & Kroenke, C. D. (2018) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13938 · Cited by 11 · see citing works
Self-citationYazdani-Brojeni, P., Motz, M., & Koren, G. (2009) · PubMed · Cited by 10 · see citing works
Moore, T. E., & Gagnier, K. R. (2010) · The Corsini Encyclopedia of Psychology · doi:10.1002/9780470479216.corpsy0354 · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [6]CDC , Behavioral Risk Factor Surveillance System User’s Guide (US Centers for Disease Control and Prevention, Atlanta, GA, 2019). [[Google Scholar](https://scholar.google.com/scholar_lookup?title=Behavioral%20Risk%20Factor%20Surveillance%20System%20User%E2%80%99s%20Guide&publication_year=2019&)]
- [78]Fogtmann M., Seshamani S., Kim K., Chapman T., Studholme C., “A unified approach for motion estimation and super resolution reconstruction from structural Magnetic Resonance imaging on moving subjects” in MICCAI Workshop on Perinatal and Paediatric Imaging (Nice, 2012). [[Google Scholar](https://scholar.google.com/scholar_lookup?title=MICCAI%20Workshop%20on%20Perinatal%20and%20Paediatric%20Imaging&author=M.%20Fogtmann&author=S.%20Seshamani&author=K.%20Kim&author=T.%20Chapman&author=C.%20Studholme&publication_year=2012&)]
Cited by
Sorted by citations
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“MRI studies showed reductions in brainstem as well as cerebellum volume in a primate FAS model and a sex-dependent change in functional connectivity and metabolism in prefrontal areas in a rat FAS model [317, 318].”
Background
- Authors
- Wang, X., Cuzon Carlson, V. C., Studholme, C., Newman, N., Ford, M. M., Grant, K. A., & Kroenke, C. D.
- Affiliations
- Oregon National Primate Research Center (US)
- Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006;
- University of Washington (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2020-04-20
- Volume
- 117
- Issue
- 18
- Pages
- 10035-10044
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC7211988
- OpenAlex
- W3016443736
- Cited by
- 31
- References
- 91
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 2 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 1 · 2019: 1
- FWCI
- 4.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute on Alcohol Abuse and Alcoholism (AA021981, AA019431)
- HHS | NIH | NIH Office of the Director (OD011092)
- HHS | NIH | National Institute of Neurological Disorders and Stroke (NS055064)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- fetal alcohol spectrum disorders, prenatal alcohol exposure, fetal brain development, rhesus macaque model, fetal MRI, diffusion MRI, white matter anisotropy, brainstem volume, spontaneous excitatory postsynaptic currents, primary somatosensory cortex, putamen, motor control, early pregnancy
- MeSH terms
- Alcohol Drinking, Ethanol, Animals, Brain, Disease Models, Animal, Female, Fetus, Humans, Macaca mulatta, Pregnancy, Prenatal Exposure Delayed Effects, Retrospective Studies, Diffusion Magnetic Resonance Imaging, Fetal Development, Fetal Alcohol Spectrum Disorders
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 ›
Are you an author, or do you see a problem with this page? Request a review