Long-term alterations in brain and behavior after postnatal Zika virus infection in infant macaques
Open accessPublished version of a preprint
Abstract
Zika virus (ZIKV) infection has a profound impact on the fetal nervous system. The postnatal period is also a time of rapid brain growth, and it is important to understand the potential neurobehavioral consequences of ZIKV infection during infancy. Here we show that postnatal ZIKV infection in a rhesus macaque model resulted in long-term behavioral, motor, and cognitive changes, including increased emotional reactivity, decreased social contact, loss of balance, and deficits in visual recognition memory at one year of age. Structural and functional MRI showed that ZIKV-infected infant rhesus macaques had persistent enlargement of lateral ventricles, smaller volumes and altered functional connectivity between brain areas important for socioemotional behavior, cognitive, and motor function (e.g. amygdala, hippocampus, cerebellum). Neuropathological changes corresponded with neuroimaging results and were consistent with the behavioral and memory deficits. Overall, this study demonstrates that postnatal ZIKV infection in this model may have long-lasting neurodevelopmental consequences.
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?
Even a postnatal viral infection can lead to postnatal meningitis and neurodevelopmental problems due to structural and functional damage of frontal areas.
“Even a postnatal viral infection can lead to postnatal meningitis and neurodevelopmental problems due to structural and functional damage of frontal areas [344].”
From Development of prefrontal cortex (2022) · cites this paper as [344]
The Discussion reports long-term neurodevelopmental, behavioral and cognitive changes after postnatal Zika infection in infant macaques. The Results describe altered functional connectivity involving prefrontal areas, but the reported structural changes chiefly involve other regions. Our copy does not report postnatal meningitis or establish that damage to frontal areas caused the developmental problems (pages unavailable). (LLM, conf=0.88)
Experimental — accuracy not yet measured
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
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.018 · Cited by 7,429 · see citing works
Methods to detect, characterize, and remove motion artifact in resting state fMRI
Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.08.048 · Cited by 3,748 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
Andersson, J. L. R., Skare, S., & Ashburner, J. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00336-7 · Cited by 3,469 · see citing works
Zika Virus Associated with Microcephaly
Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1600651 · Cited by 2,884 · see citing works
Zika Virus (I). Isolations and serological specificity
Dick, G. W. A., Kitchen, S. F., & Haddow, A. J. (1952) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(52)90042-4 · Cited by 2,698 · see citing works
The brain basis of emotion: a meta-analytic review
Lindquist, K. A., Wager, T. D., Kober, H., Bliss-Moreau, E., & Barrett, L. F. (2012) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11000446 · Cited by 2,320 · see citing works
Zika Virus Infection in Pregnant Women in Rio de Janeiro
Brasil, P., Pereira, J. P., Moreira, M. E. L., Nogueira, R. M. R., Damasceno, L. S., Wakimoto, M. D., Rabello, R. S., Gaw, S. L., Halai, U., Salles, T. R. S., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1602412 · Cited by 2,190 · see citing works
Nipype: A Flexible, Lightweight and Extensible Neuroimaging Data Processing Framework in Python
Gorgolewski, K. J., Burns, C. D., Madison, C. M., Clark, D., Halchenko, Y. O., Waskom, M., & Ghosh, S. (2011) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2011.00013 · Cited by 2,162 · see citing works
Zika Virus and Birth Defects — Reviewing the Evidence for Causality
Rasmussen, S. A., Jamieson, D. J., Honein, M. A., & Petersen, L. R. (2016) · New England Journal of Medicine · doi:10.1056/nejmsr1604338 · Cited by 1,988 · see citing works
Intrinsic functional architecture in the anaesthetized monkey brain
Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., Zempel, J. M., Snyder, L. H., Corbetta, M., & Raichle, M. E. (2007) · Nature · doi:10.1038/nature05758 · Cited by 1,786 · see citing works
Functional brain networks develop from a local to distributed organization
Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U. F., Church, J. A., Miezin, F. M., Schlaggar, B. L., & Petersen, S. E. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000381 · Cited by 1,530 · see citing works
Self-citationThe Brazilian Zika virus strain causes birth defects in experimental models
Cugola, F. R., Fernandes, I. R., Russo, F. B., Freitas, B. C., Dias, J. L. M., Guimarães, K. P., Benazzato, C., Almeida, N., Pignatari, G. C., Romero, S., et al. (2016) · Nature · doi:10.1038/nature18296 · Cited by 1,326 · see citing works
Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth
Tang, H., Hammack, C., Ogden, S. C., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E. M., et al. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.02.016 · Cited by 1,292 · see citing works
Development of distinct control networks through segregation and integration
Fair, D. A., Dosenbach, N. U. F., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., Barch, D. M., Raichle, M. E., Petersen, S. E., & Schlaggar, B. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705843104 · Cited by 1,244 · see citing works
Self-citationLateral prefrontal cortex: architectonic and functional organization
Petrides, M. (2005) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2005.1631 · Cited by 1,212 · see citing works
A Structural MRI Study of Human Brain Development from Birth to 2 Years
Knickmeyer, R. C., Gouttard, S., Kang, C., Evans, D., Wilber, K., Smith, J. K., Hamer, R. M., Lin, W., Gerig, G., & Gilmore, J. H. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3479-08.2008 · Cited by 1,151 · see citing works
Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · see citing works
Characterizing the Pattern of Anomalies in Congenital Zika Syndrome for Pediatric Clinicians
Moore, C. A., Staples, J. E., Dobyns, W. B., Pessoa, A. L. S., Ventura, C. V. O. C., da Fonseca, E. B., Ribeiro, E. M., Ventura, L. O., Neto, N. N., Arena, J. F., et al. (2016) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2016.3982 · Cited by 953 · see citing works
Visual Experience in Infants: Decreased Attention to Familiar Patterns Relative to Novel Ones
Fantz, R. L. (1964) · Science · doi:10.1126/science.146.3644.668 · Cited by 901 · see citing works
A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex
Markov, N. T., Ercsey-Ravasz, M. M., Ribeiro Gomes, A. R., Lamy, C., Magrou, L., Vezoli, J., Misery, P., Falchier, A., Quilodran, R., Gariel, M. A., et al. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhs270 · Cited by 857 · see citing works
Hutchison, R. M., Womelsdorf, T., Gati, J. S., Everling, S., & Menon, R. S. (2012) · Human Brain Mapping · doi:10.1002/hbm.22058 · Cited by 715 · see citing works
Zika virus (II). Pathogenicity and physical properties
Dick, G. W. A. (1952) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(52)90043-6 · Cited by 690 · see citing works
de França, G. V. A., Schüler‐Faccini, L., de Oliveira, W. K., Henriques, C. M. P., Carmo, E. H., Pedí, V. D., Nunes, M. L., Castro, M. C., Serruya, S. J., da Silveira, M. F., et al. (2016) · The Lancet · doi:10.1016/s0140-6736(16)30902-3 · Cited by 601 · see citing works
Perspectives on Cognitive Neuroscience
Churchland, P. S., & B, T. J. S. A. (1988) · Science · doi:10.1126/science.3055294 · Cited by 505 · see citing works
Fair, D. A., Nigg, J. T., Iyer, S., Bathula, D., Mills, K. L., Dosenbach, N. U. F., Schlaggar, B. L., Mennes, M., Gutman, D., Bangaru, S., et al. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00080 · Cited by 463 · see citing works
Self-citationA Combined MRI and Histology Atlas of the Rhesus Monkey Brain: In Stereotaxic Coordinates
Saleem, K. S., & Logothetis, N. K. (2012) · Max Planck Digital Library · Cited by 446 · see citing works
van der Linden, V., Pessoa, A. L. S., Dobyns, W. B., et al. (2016) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6547e2 · Cited by 446 · see citing works
Postnatal Development of Vision in Human and Nonhuman Primates
Boothe, R. G., Dobson, V., & Teller, D. Y. (1985) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.08.030185.002431 · Cited by 383 · see citing works
Aragão, M. D. F. V. V., van der Linden, V., Brainer-Lima, A. M., Ramos, R. C. F., Rocha, M. Â. W., da Silva, P. F. S., Carvalho, M. D. C. G., van der Linden, A., Cesario, A., & Valênça, M. M. (2016) · BMJ · doi:10.1136/bmj.i1901 · Cited by 376 · see citing works
Phylogeny of Zika Virus in Western Hemisphere, 2015
Lanciotti, R. S., Lambert, A. J., Holodniy, M., Saavedra, S., & Signor, L. D. C. C. (2016) · Emerging infectious diseases · doi:10.3201/eid2205.160065 · Cited by 349 · see citing works
The behaviour of socially living rhesus monkeys in their first two and a half years
Hinde, R. A., & Spencer‐Booth, Y. (1967) · Animal Behaviour · doi:10.1016/s0003-3472(67)80029-0 · Cited by 331 · see citing works
Zika virus is a global public health emergency, declares WHO
Gulland, A. (2016) · BMJ · doi:10.1136/bmj.i657 · Cited by 306 · see citing works
Haddow, A. J., Williams, M., Woodall, J. P., Simpson, D. I. H., & Goma, L. K. H. (1964) · Europe PMC (PubMed Central) · Cited by 300 · see citing works
Bauman, M. D., Iosif, A.-M., Smith, S. E. P., Bregere, C., Amaral, D. G., & Patterson, P. H. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.025 · Cited by 294 · see citing works
Nielsen‐Saines, K., Brasil, P., Kerin, T., de Vasconcelos, Z. F. M., Gabaglia, C. R., Damasceno, L. S., Pone, M. V. D. S., de Carvalho, L. M. A., Pone, S. M., Zin, A., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0496-1 · Cited by 270 · see citing works
Smithburn, K. C. (1952) · The Journal of Immunology · doi:10.4049/jimmunol.69.2.223 · Cited by 263 · see citing works
Zika Virus infection of rhesus macaques leads to viral persistence in multiple tissues
Hirsch, A. J., Smith, J. L., Haese, N. N., Broeckel, R. M., Parkins, C. J., Kreklywich, C. N., DeFilippis, V. R., Denton, M. C., Smith, P. P., Messer, W. B., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006219 · Cited by 257 · see citing works
Computed Tomographic Findings in Microcephaly Associated with Zika Virus
Hazin, A. N., Poretti, A., Cruz, D. D. C. S., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmc1603617 · Cited by 255 · see citing works
Hinde, K., Skibiel, A. L., Foster, A. B., Rosso, L. A. D., Mendoza, S. P., & Capitanio, J. P. (2014) · Behavioral Ecology · doi:10.1093/beheco/aru186 · Cited by 254 · see citing works
A population-average MRI-based atlas collection of the rhesus macaque
McLaren, D. G., Kosmatka, K. J., Oakes, T. R., Kroenke, C. D., Kohama, S. G., Matochik, J. A., Ingram, D. K., & Johnson, S. C. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.058 · Cited by 241 · see citing works
The phenotypic spectrum of congenital Zika syndrome
Campo, M. D., Feitosa, I. M. L., Ribeiro, E. M., Horovitz, D. D. G., Pessoa, A. L. S., de França, G. V. A., Garcı́a-Alix, A., Doriqui, M. J. R., Wanderley, H. Y. C., Sanseverino, M. T. V., et al. (2017) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.38170 · Cited by 215 · see citing works
Besnard, M., Eyrolle‐Guignot, D., Guillemette-Artur, P., et al. (2016) · Eurosurveillance · doi:10.2807/1560-7917.es.2016.21.13.30181 · Cited by 212 · see citing works
Zika Virus Persistence in the Central Nervous System and Lymph Nodes of Rhesus Monkeys
Aïd, M., Abbink, P., Larocca, R. A., Boyd, M. B., Nityanandam, R., Nanayakkara, O., Martinot, A. J., Moseley, E. T., Blass, E., Borducchi, E. N., et al. (2017) · Cell · doi:10.1016/j.cell.2017.04.008 · Cited by 201 · see citing works
Bick, J., Zhu, T., Stamoulis, C., Fox, N. A., Zeanah, C., & Nelson, C. A. (2015) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2014.3212 · Cited by 199 · see citing works
Rice, M. E., Galang, R. R., Roth, N. M., Ellington, S., Moore, C. A., Valencia‐Prado, M., Ellis, E. M., Tufa, A. J., Taulung, L. A., Alfred, J. M., et al. (2018) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6731e1 · Cited by 192 · see citing works
How does Zika virus cause microcephaly?Preprint
Wen, Z., Song, H., & Ming, G. (2017) · Genes & Development · doi:10.1101/gad.298216.117 · Cited by 182 · see citing works
Local and Widespread Slow Waves in Stable NREM Sleep: Evidence for Distinct Regulation Mechanisms
Bernardi, G., Siclari, F., Handjaras, G., Riedner, B. A., & Tononi, G. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00248 · Cited by 167 · see citing works
Satterfield‐Nash, A., Kotzky, K., Allen, J. E., Bertolli, J., Moore, C. A., Pereira, I. O., Pessoa, A. L. S., de Melo, F. G., Santelli, A. C. F. E. S., Boyle, C. A., et al. (2017) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6649a2 · Cited by 164 · see citing works
Zika virus: Further isolations in the zika area, and some studies on the strains isolated
Weinbren, M. P., & Williams, M. (1958) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(58)90085-3 · Cited by 154 · see citing works
The Development of Social Behavior Following Neonatal Amygdala Lesions in Rhesus Monkeys
Bauman, M., Lavenex, P., Mason, W., Capitanio, J., & Amaral, D. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304741 · Cited by 148 · see citing works
Bachevalier, J., & Nemanic, S. (2007) · Hippocampus · doi:10.1002/hipo.20369 · Cited by 147 · see citing works
Aragao, M. F. V. V., Holanda, A. C., Brainer-Lima, A. M., Petribu, N. C. L., Castillo, M., van der Linden, V., Serpa, S. C., Tenório, A. G., Travassos, P. T. C., Cordeiro, M. T., et al. (2017) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5216 · Cited by 147 · see citing works
Long-term circulation of Zika virus in Thailand: an observational study
Ruchusatsawat, K., Wongjaroen, P., Posanacharoen, A., Rodríguez-Barraquer, I., Sangkitporn, S., Cummings, D. A. T., & Salje, H. (2019) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(18)30718-7 · Cited by 134 · see citing works
Miranda-Dominguez, O., Mills, B. D., Grayson, D., Woodall, A., Grant, K. A., Kroenke, C. D., & Fair, D. A. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4229-13.2014 · Cited by 130 · see citing works
Self-citationPayne, C., Machado, C. J., Bliwise, N. G., & Bachevalier, J. (2010) · Hippocampus · doi:10.1002/hipo.20688 · Cited by 129 · see citing works
Chen, Q., Sjölander, A., Långström, N., Rodriguez, A., Serlachius, E., D'Onofrio, B., Lichtenstein, P., & Larsson, H. (2014) · International Journal of Epidemiology · doi:10.1093/ije/dyt152 · Cited by 127 · see citing works
The Risk of Offspring Psychiatric Disorders in the Setting of Maternal Obesity and Diabetes
Kong, L., Norstedt, G., Schalling, M., Gissler, M., & Lavebratt, C. (2018) · PEDIATRICS · doi:10.1542/peds.2018-0776 · Cited by 127 · see citing works
The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys
Bauman, M., Lavenex, P., Mason, W., Capitanio, J., & Amaral, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3263-03.2004 · Cited by 122 · see citing works
Acute and chronic neurological consequences of early-life Zika virus infection in mice
Souza, I. N. D. O., Frost, P. S., França, J. V., Nascimento-Viana, J. B., Neris, R. L. S., Oliveira, L. F., Pinheiro, D. J. L. L., Nogueira, C. O., Neves, G. A., Chimelli, L. M. C., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aar2749 · Cited by 119 · see citing works
Multi-atlas segmentation of subcortical brain structures via the AutoSeg software pipeline
Wang, J., Vachet, C., Rumple, A., Gouttard, S., Ouziel, C., Perrot, E., Du, G., Huang, X., Gerig, G., & Styner, M. A. (2014) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2014.00007 · Cited by 117 · see citing works
Self-citationKnickmeyer, R. C., Styner, M. A., Short, S. J., Lubach, G. R., Kang, C., Hamer, R. M., Coe, C. L., & Gilmore, J. H. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp166 · Cited by 113 · see citing works
Self-citationWellman, L. L., Forcelli, P. A., Aguilar, B. L., & Málková, L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0333-16.2016 · Cited by 108 · see citing works
Howell, B., McCormack, K. M., Grand, A. P., Sawyer, N. T., Zhang, X., Maestripieri, D., Hu, X. P., & Sánchez, M. M. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-21 · Cited by 107 · see citing works
Evidence for Mother-to-Child Transmission of Zika Virus Through Breast Milk
Blohm, G. M., Lednicky, J. A., Márquez, M., et al. (2017) · Clinical Infectious Diseases · doi:10.1093/cid/cix968 · Cited by 106 · see citing works
Zika infection and the development of neurological defects
Russo, F. B., Jungmann, P., & Beltrão-Braga, P. C. B. (2017) · Cellular Microbiology · doi:10.1111/cmi.12744 · Cited by 96 · see citing works
The Complex Nature of Hippocampal-Striatal Interactions in Spatial Navigation
Goodroe, S. C., Starnes, J., & Brown, T. I. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00250 · Cited by 93 · see citing works
Dose-dependent effect of isoflurane on regional cerebral blood flow in anesthetized macaque monkeys
Li, C.-X., Patel, S., Auerbach, E. J., & Zhang, X. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.02.007 · Cited by 88 · see citing works
Mavigner, M., Raper, J., Kovacs-Balint, Z., Gumber, S., O’Neal, J. T., Bhaumik, S. K., Zhang, X., Habib, J. G., Mattingly, C., McDonald, C. E., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aao6975 · Cited by 87 · see citing works
Self-citationCooperative interactions between hippocampal and striatal systems support flexible navigation
Brown, T. I., Ross, R. S., Tobyne, S. M., & Stern, C. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.046 · Cited by 86 · see citing works
Visual development in primates: Neural mechanisms and critical periods
Kiorpes, L. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22276 · Cited by 85 · see citing works
Rhesus macaque brain morphometry: A methodological comparison of voxel-wise approaches
McLaren, D. G., Kosmatka, K. J., Kastman, E. K., Bendlin, B. B., & Johnson, S. C. (2009) · Methods · doi:10.1016/j.ymeth.2009.10.003 · Cited by 85 · see citing works
Revisiting the Maturation of Medial Temporal Lobe Memory Functions in PrimatesPreprint
Alvarado, M. C., & Bachevalier, J. (2000) · Learning & Memory · doi:10.1101/lm.35100 · Cited by 73 · see citing works
Self-citationContributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience
Ferbinteanu, J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0840-16.2016 · Cited by 73 · see citing works
Postnatal development of the amygdala: A stereological study in macaque monkeys
Chareyron, L. J., Lavenex, P. B., Amaral, D. G., & Lavenex, P. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.23023 · Cited by 72 · see citing works
Zeamer, A., Heuer, E., & Bachevalier, J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0022-10.2010 · Cited by 69 · see citing works
de Carvalho, A. L., Brites, C. R., Mochida, G. H., et al. (2019) · Brain and Development · doi:10.1016/j.braindev.2019.03.005 · Cited by 69 · see citing works
Mavigner, M., Habib, J. G., Deléage, C., Rosen, E. P., Mattingly, C., Bricker, K. M., Kashuba, A. D. M., Amblard, F., Schinazi, R. F., Lawson, B., et al. (2018) · Journal of Virology · doi:10.1128/jvi.00562-18 · Cited by 68 · see citing works
Self-citationUnravelling the development of the visual cortex: implications for plasticity and repair
Bourne, J. A. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01275.x · Cited by 65 · see citing works
Sequential Neuroimaging of the Fetus and Newborn With In Utero Zika Virus Exposure
Mulkey, S. B., Bulas, D., Vézina, G., Fourzali, Y., Morales, A., Arroyave‐Wessel, M., Swisher, C. B., Cristante, C., Russo, S. M., Encinales, L., et al. (2018) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2018.4138 · Cited by 65 · see citing works
White Matter Abnormalities in Children with HIV Infection and Exposure
Jankiewicz, M., Holmes, M., Taylor, P. A., Cotton, M. F., Laughton, B., van der Kouwe, A. J. W., & Meintjes, E. M. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00088 · Cited by 57 · see citing works
Uban, K. A., Herting, M. M., Williams, P. L., Ajmera, T., Gautam, P., Huo, Y., Malee, K., Yogev, R., Csernansky, J. G., Wang, L., et al. (2015) · AIDS · doi:10.1097/qad.0000000000000648 · Cited by 56 · see citing works
Prenatal Development of Layer-Specific Local Circuits in Primary Visual Cortex of the Macaque Monkey
Callaway, E. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01505.1998 · Cited by 54 · see citing works
Goodman, A. B., Dziuban, E. J., Powell, K. M., et al. (2016) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6539e2 · Cited by 49 · see citing works
Automatic brain segmentation in rhesus monkeys
Styner, M. A., Knickmeyer, R. C., Joshi, S. C., Coe, C. L., Short, S. J., & Gilmore, J. H. (2007) · Proceedings of SPIE, the International Society for Optical Engineering/Proceedings of SPIE · doi:10.1117/12.710027 · Cited by 42 · see citing works
Self-citationIyer, S., Izhak Shafran, J., Grayson, D. S., Gates, K. M., Nigg, J. T., & Fair, D. A. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.02.054 · Cited by 40 · see citing works
Self-citationZika Virus Seropositivity in 1–4-Year-Old Children, Indonesia, 2014
Sasmono, R. T., Dhenni, R., Yohan, B., et al. (2018) · Emerging infectious diseases · doi:10.3201/eid2409.180582 · Cited by 37 · see citing works
Long-term effects of neonatal medial temporal ablations on socioemotional behavior in monkeys
Malkova, L., Mishkin, M., Suomi, S., & Bachevalier, J. (2010) · Behavioral Neuroscience · doi:10.1037/a0021622 · Cited by 36 · see citing works
Shi, Y., Budin, F., Yapuncich, E., Rumple, A., Young, J. T., Payne, C. D., Zhang, X., Hu, X. P., Godfrey, J., Howell, B., et al. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00617 · Cited by 36 · see citing works
Self-citationThe effects of neonatal amygdala or hippocampus lesions on adult social behavior
Bliss‐Moreau, E., Moadab, G., Santistevan, A. C., & Amaral, D. G. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.11.052 · Cited by 35 · see citing works
Raper, J., Stephens, S. B. Z., Sánchez, M. M., Bachevalier, J., & Wallen, K. (2014) · Developmental Psychobiology · doi:10.1002/dev.21234 · Cited by 33 · see citing works
Self-citationBlue, S. N., Kazama, A. M., & Bachevalier, J. (2013) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617713000799 · Cited by 30 · see citing works
Zika Virus Disease in Children in Colombia, August 2015 to May 2016
Tolosa, N., Tinker, S. C., Pacheco, Ó., Valencia, D., Botero, D. S., Tong, V. T., Mercado, M., Gilboa, S. M., González, M., Nelson, C. A., et al. (2017) · Paediatric and Perinatal Epidemiology · doi:10.1111/ppe.12391 · Cited by 30 · see citing works
Hunsaker, M. R., Scott, J. A., Bauman, M. D., Schumann, C. M., & Amaral, D. G. (2014) · Hippocampus · doi:10.1002/hipo.22271 · Cited by 27 · see citing works
Besnard, M., Dub, T., & Gérardin, P. (2017) · Emerging infectious diseases · doi:10.3201/eid2308.170198 · Cited by 27 · see citing works
Li, J., Chong, C. Y., Tan, N. W., et al. (2017) · Clinical Infectious Diseases · doi:10.1093/cid/cix137 · Cited by 25 · see citing works
Snyder‐Keller, A., Kramer, L. D., Zink, S. D., & Bolivar, V. J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2666-18.2019 · Cited by 25 · see citing works
Moadab, G., Bliss-Moreau, E., Bauman, M., & Amaral, D. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000181 · Cited by 22 · see citing works
Raper, J., Wilson, M., Sánchez, M. M., Payne, C. D., & Bachevalier, J. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.11.018 · Cited by 21 · see citing works
Self-citationTang, C. Y., & Ramani, R. (2015) · International Anesthesiology Clinics · doi:10.1097/aia.0000000000000081 · Cited by 20 · see citing works
Amygdala growth from youth to adulthood in the macaque monkey
Schumann, C. M., Scott, J. A., Lee, A., Bauman, M. D., & Amaral, D. G. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24728 · Cited by 18 · see citing works
King, D. R., de Chastelaine, M., Elward, R. L., Wang, T. H., & Rugg, M. D. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.07.031 · Cited by 15 · see citing works
Mouse studies confirm the link between Zika virus infection and microcephaly
Malkki, H. A. I. (2016) · Nature Reviews Neurology · doi:10.1038/nrneurol.2016.78 · Cited by 11 · see citing works
Carryl, H., Rompay, K. K. A. V., Paris, K. D., & Burke, M. (2017) · Brain Sciences · doi:10.3390/brainsci7040040 · Cited by 11 · see citing works
Self-citationUncovering the Spectrum of Postnatal Zika Infection in Children
Asturias, E. J. (2018) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2018.0921 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The landscape of cognitive function in recovered COVID-19 patients
Zhou, H., Lu, S., Chen, J., Wei, N., Wang, D., Lyu, H., Shi, C., & Hu, S. (2020) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2020.06.022 · Cited by 440 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“Even a postnatal viral infection can lead to postnatal meningitis and neurodevelopmental problems due to structural and functional damage of frontal areas [344].”
- Authors
- Raper, J., Kovacs-Balint, Z., Mavigner, M., Gumber, S., Burke, M. W., Habib, J., Mattingly, C., Fair, D., Earl, E., Feczko, E., Styner, M., Jean, S. M., Cohen, J. K., Suthar, M. S., Sanchez, M. M., Alvarado, M. C., & Chahroudi, A.
- Affiliations
- Emory University (US)
- Howard University (US)
- Oregon Health & Science University (US)
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Chahroudi, Ann
- ORCID
- Venue
- Nature Communications
- Published
- 2020-05-21
- Volume
- 11
- Issue
- 1
- Pages
- 2534-2534
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7242369
- OpenAlex
- W3026333016
- Cited by
- 67
- References
- 106
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 12 · 2023: 14 · 2022: 11 · 2021: 13 · 2020: 4 · 2018: 1
- FWCI
- 7.86
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UNC Libraries
- Funders
- U.S. Department of Health & Human Services | NIH | NIH Office of the Director (P51 OD011132)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
- Health Sciences › Medicine › Infectious Diseases › Infectious Encephalopathies and Encephalitis
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Keywords
- Zika virus, postnatal infection, rhesus monkeys, neurodevelopmental outcomes, emotional reactivity, social contact, motor impairment, visual recognition memory, lateral ventricle enlargement, amygdala, hippocampus, cerebellum, functional connectivity, neuropathology, infant brain
- MeSH terms
- Zika Virus Infection, Zika Virus, Animals, Brain, Cognition, Disease Models, Animal, Female, Macaca mulatta, Memory, Nerve Net, Social Behavior, Neuroimaging
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
