Postnatal Zika virus infection is associated with persistent abnormalities in brain structure, function, and behavior in infant macaques

Science Translational Medicine

Volumn 10, Issue 435, 2018, Pages

  Mavigner, Maud ^a   Raper, Jessica ^b   Kovacs Balint, Zsofia ^b   Gumber, Sanjeev ^b   O'Neal, Justin T ^b   Bhaumik, Siddhartha K ^a   Zhang, Xiaodong ^b   Habib, Jakob ^a   Mattingly, Cameron ^a   McDonald, Circe E ^b   Avanzato, Victoria ^a   Burke, Mark W ^c   Magnani, Diogo M ^d   Bailey, Varian K ^d   Watkins, David I ^d   Vanderford, Thomas H ^b   Fair, Damien ^e   Earl, Eric ^e   Feczko, Eric ^e   Styner, Martin ^f   Jean, Sherrie M ^b   Cohen, Joyce K ^b   Silvestri, Guido ^a,b   Paul Johnson, R ^b   O'Connor, David H ^g   Wrammert, Jens ^a   Suthar, Mehul S ^a,b   Sanchez, Mar M ^a,b   Alvarado, Maria C ^a,b   Chahroudi, Ann ^a,b,h   more..

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c HOWARD UNIVERSITY   (United States)

^d UNIVERSITY OF MIAMI   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF WISCONSIN   (United States)

^h CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; BRAIN FUNCTION; BRAIN SIZE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; DYNAMICS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HISTOPATHOLOGY; HUMORAL IMMUNITY; INFANT; LONGITUDINAL STUDY; MALE; NEUROPATHOLOGY; NEWBORN INFECTION; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; RHESUS MONKEY; STRUCTURE ANALYSIS; TASK PERFORMANCE; VIRAL TROPISM; VISUAL MEMORY; ZIKA FEVER; ANIMAL; BRAIN; COMPLICATION; DIAGNOSTIC IMAGING; GENETICS; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY; VIROLOGY;

VIRUS RNA;

ANIMALS; ANIMALS, NEWBORN; BRAIN; FEMALE; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; PREGNANCY; RNA, VIRAL; ZIKA VIRUS INFECTION;

EID: 85045091218     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aao6975     Document Type: Article

References (103)

1. P. Brasil, J. P. Pereira Jr., M. E. Moreira, R. M. Ribeiro Nogueira, L. Damasceno, M. Wakimoto, R. S. Rabello, S. G. Valderramos, U.-A. Halai, T. S. Salles, A. A. Zin, D. Horovitz, P. Daltro, M. Boechat, C. Raja Gabaglia, P. Carvalho de Sequeira, J. H. Pilotto, R. Medialdea-Carrera, D. Cotrim da Cunha, L. M. Abreu de Carvalho, M. Pone, A. Machado Siqueira, G. A. Calvet, A. E. Rodrigues Baião, E. S. Neves, P. R. Nassar de Carvalho, R. H. Hasue, P. B. Marschik, C. Einspieler, C. Janzen, J. D. Cherry, A. M. Bispo de Filippis, K. Nielsen-Saines, Zika virus infection in pregnant women in Rio de Janeiro. N. Engl. J. Med. 375, 2321-2334 (2016).
2. J. Mlakar, M. Korva, N. Tul, M. Popovi?, M. Poljšak-Prijatelj, J. Mraz, M. Kolenc, K. Resman Rus, T. Vesnaver Vipotnik, V. Fabjan Vodušek, A. Vizjak, J. Pižem, M. Petrovec, T. Avši? Županc, Zika virus associated with microcephaly. N. Engl. J. Med. 374, 951-958 (2016).
3. C. A. Moore, J. E. Staples, W. B. Dobyns, A. Pessoa, C. V. Ventura, E. B. Fonseca, E. M. Ribeiro, L. O. Ventura, N. N. Neto, J. F. Arena, S. A. Rasmussen, Characterizing the pattern of anomalies in congenital Zika syndrome for pediatric clinicians. JAMA Pediatr. 171, 288-295 (2017).
4. G. W. A. Dick, S. F. Kitchen, A. J. Haddow, Zika virus. I. Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46, 509-520 (1952).
5. K. C. Smithburn, Neutralizing antibodies against certain recently isolated viruses in the sera of human beings residing in East Africa. J. Immunol. 69, 223-234 (1952).
6. M. P. Weinbren, M. C. Williams, Zika virus: Further isolations in the Zika area, and some studies on the strains isolated. Trans. R. Soc. Trop. Med. Hyg. 52, 263-268 (1958).
7. A. J. Haddow, M. C. Williams, J. P. Woodall, D. I. H. Simpson, L. K. H. Goma, Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda forest. Bull. World Health Organ. 31, 57-69 (1964).
8. G. W. A. Dick, Zika virus. II. Pathogenicity and physical properties. Trans. R. Soc. Trop. Med. Hyg. 46, 521-534 (1952).
9. A. Gulland, Zika virus is a global public health emergency, declares WHO. BMJ 352, i657 (2016).
10. F. R. Cugola, I. R. Fernandes, F. B. Russo, B. C. Freitas, J. L. M. Dias, K. P. Guimarães, C. Benazzato, N. Almeida, G. C. Pignatari, S. Romero, C. M. Polonio, I. Cunha, C. L. Freitas, W. N. Brandão, C. Rossato, D. G. Andrade, D. P. de Faria, A. T. Garcez, C. A. Buchpigel, C. T. Braconi, E. Mendes, A. A. Sall, P. M. A. de Zanotto, J. P. S. Peron, A. R. Muotri, P. C. B. Beltrão-Braga, The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534, 267-271 (2016).
11. G. V. A. França, L. Schuler-Faccini, W. K. Oliveira, C. M. P. Henriques, E. H. Carmo, V. D. Pedi, M. L. Nunes, M. C. Castro, S. Serruya, M. F. Silveira, F. C. Barros, C. G. Victora, Congenital Zika virus syndrome in Brazil: A case series of the first 1501 livebirths with complete investigation. Lancet 388, 891-897 (2016).
12. H. Malkki, CNS infections: Mouse studies confirm the link between Zika virus infection and microcephaly. Nat. Rev. Neurol. 12, 369 (2016).
13. S. A. Rasmussen, D. J. Jamieson, M. A. Honein, L. R. Petersen, Zika virus and birth defects-Reviewing the evidence for causality. N. Engl. J. Med. 374, 1981-1987 (2016).
14. L. A. Glantz, J. H. Gilmore, R. M. Hamer, J. A. Lieberman, L. F. Jarskog, Synaptophysin and postsynaptic density protein 95 in the human prefrontal cortex from mid-gestation into early adulthood. Neuroscience 149, 582-591 (2007).
15. P. R. Huttenlocher, A. S. Dabholkar, Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387, 167-178 (1997).
16. R. C. Knickmeyer, S. Gouttard, C. Kang, D. Evans, K. Wilber, J. K. Smith, R. M. Hamer, W. Lin, G. Gerig, J. H. Gilmore, A structural MRI study of human brain development from birth to 2 years. J. Neurosci. 28, 12176-12182 (2008).
17. D. J. Miller, T. Duka, C. D. Stimpson, S. J. Schapiro, W. B. Baze, M. J. McArthur, A. J. Fobbs, A. M. M. Sousa, N. Šestan, D. E. Wildman, L. Lipovich, C. W. Kuzawa, P. R. Hof, C. C. Sherwood, Prolonged myelination in human neocortical evolution. Proc. Natl. Acad. Sci. U.S.A. 109, 16480-16485 (2012).
18. P. Lavenex, P. Banta Lavenex, D. G. Amaral, Postnatal development of the primate hippocampal formation. Dev. Neurosci. 29, 179-192 (2007).
19. S. Bianchi, C. D. Stimpson, T. Duka, M. D. Larsen, W. G. M. Janssen, Z. Collins, A. L. Bauernfeind, S. J. Schapiro, W. B. Baze, M. J. McArthur, W. D. Hopkins, D. E. Wildman, L. Lipovich, C. W. Kuzawa, B. Jacobs, P. R. Hof, C. C. Sherwood, Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans. Proc. Natl. Acad. Sci. U.S.A. 110 (suppl. 2), 10395-10401 (2013).
20. E. R. Cooper, C. Hanson, C. Diaz, H. Mendez, R. Abboud, R. Nugent, J. Pitt, K. Rich, E. M. Rodriguez, V. Smeriglio; Women and Infants Transmission Study Group, Encephalopathy and progression of human immunodeficiency virus disease in a cohort of children with perinatally acquired human immunodeficiency virus infection. J. Pediatr. 132, 808-812 (1998).
21. L. G. Epstein, L. R. Sharer, J. Goudsmit, Neurological and neuropathological features of human immunodeficiency virus infection in children. Ann. Neurol. 23, S19-S23 (1988).
22. K. Hamprecht, R. Goelz, Postnatal cytomegalovirus infection through human milk in preterm infants: Transmission, clinical presentation, and prevention. Clin. Perinatol. 44, 121-130 (2017).
23. A. B. Goodman, E. J. Dziuban, K. Powell, R. H. Bitsko, G. Langley, N. Lindsey, J. L. Franks, K. Russell, S. Dasgupta, W. D. Barfield, E. Odom, E. Kahn, S. Martin, M. Fischer, J. E. Staples, Characteristics of children aged <18 years with Zika virus disease acquired postnatally-U.S. States, January 2015-July 2016. MMWR Morb. Mortal. Wkly Rep. 65, 1082-1085 (2016).
24. J. Li, C. Y. Chong, N. W. H. Tan, C. F. Yung, N. W. S. Tee, K. C. Thoon, Characteristics of Zika virus disease in children: Clinical, hematological and virological findings from an outbreak in Singapore. Clin. Infect. Dis. 64, 1445-1448 (2017).
25. Centers for Disease Control and Prevention, Zika in infants and children, www.cdc.gov/zika/hc-providers/infants-children/zika-in-infants-children.html (accessed 01 August 2017).
26. K. M. Adams Waldorf, J. E. Stencel-Baerenwald, R. P. Kapur, C. Studholme, E. Boldenow, J. Vornhagen, A. Baldessari, M. K. Dighe, J. Thiel, S. Merillat, B. Armistead, J. Tisoncik-Go, R. R. Green, M. A. Davis, E. C. Dewey, M. R. Fairgrieve, J. C. Gatenby, T. Richards, G. A. Garden, M. S. Diamond, S. E. Juul, R. F. Grant, L. Kuller, D. W. W. Shaw, J. Ogle, G. M. Gough, W. Lee, C. English, R. F. Hevner, W. B. Dobyns, M. Gale Jr., L. Rajagopal, Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate. Nat. Med. 22, 1256-1259 (2016).
27. L. L. Coffey, P. A. Pesavento, R. I. Keesler, A. Singapuri, J. Watanabe, R. Watanabe, J. Yee, E. Bliss-Moreau, C. Cruzen, K. L. Christe, J. R. Reader, W. von Morgenland, A. M. Gibbons, A. M. Allen, J. Linnen, K. Gao, E. Delwart, G. Simmons, M. Stone, M. Lanteri, S. Bakkour, M. Busch, J. Morrison, K. K. A. Van Rompay, Zika virus tissue and blood compartmentalization in acute infection of rhesus macaques. PLOS ONE 12, e0171148 (2017).
28. D. M. Dudley, M. T. Aliota, E. L. Mohr, A. M. Weiler, G. Lehrer-Brey, K. L. Weisgrau, M. S. Mohns, M. E. Breitbach, M. N. Rasheed, C. M. Newman, D. D. Gellerup, L. H. Moncla, J. Post, N. Schultz-Darken, M. L. Schotzko, J. M. Hayes, J. A. Eudailey, M. A. Moody, S. R. Permar, S. L. O'Connor, E. G. Rakasz, H. A. Simmons, S. Capuano, T. G. Golos, J. E. Osorio, T. C. Friedrich, D. H. O'Connor, A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun. 7, 12204 (2016).
29. C. E. Osuna, S.-Y. Lim, C. Deleage, B. D. Griffin, D. Stein, L. T. Schroeder, R. Omange, K. Best, M. Luo, P. T. Hraber, H. Andersen-Elyard, E. F. C. Ojeda, S. Huang, D. L. Vanlandingham, S. Higgs, A. S. Perelson, J. D. Estes, D. Safronetz, M. G. Lewis, J. B. Whitney, Zika viral dynamics and shedding in rhesus and cynomolgus macaques. Nat. Med. 22, 1448-1455 (2016).
30. R. S. Lanciotti, A. J. Lambert, M. Holodniy, S. Saavedra, Leticia del Carmen Castillo Signor, Phylogeny of Zika virus in western hemisphere, 2015. Emerg. Infect. Dis. 22, 933-935 (2016).
31. L. Priyamvada, A. Cho, N. Onlamoon, N.-Y. Zheng, M. Huang, Y. Kovalenkov, K. Chokephaibulkit, N. Angkasekwinai, K. Pattanapanyasat, R. Ahmed, P. C. Wilson, J. Wrammert, B cell responses during secondary dengue virus infection are dominated by highly cross-reactive, memory-derived plasmablasts. J. Virol. 90, 5574-5585 (2016).
32. C. Payne, C. J. Machado, N. G. Bliwise, J. Bachevalier, Maturation of the hippocampal formation and amygdala in Macaca mulatta: A volumetric magnetic resonance imaging study. Hippocampus 20, 922-935 (2010).
33. M. R. Hunsaker, J. A. Scott, M. D. Bauman, C. M. Schumann, D. G. Amaral, Postnatal development of the hippocampus in the rhesus macaque (Macaca mulatta): A longitudinal magnetic resonance imaging study. Hippocampus 24, 794-807 (2014).
34. J. W. Lewis, D. C. Van Essen, Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112-137 (2000).
35. N. T. Markov, M. M. Ercsey-Ravasz, A. R. Ribeiro Gomes, C. Lamy, L. Magrou, J. Vezoli, P. Misery, A. Falchier, R. Quilodran, M. A. Gariel, J. Sallet, R. Gamanut, C. Huissoud, S. Clavagnier, P. Giroud, D. Sappey-Marinier, P. Barone, C. Dehay, Z. Toroczkai, K. Knoblauch, D. C. Van Essen, H. Kennedy, A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex 24, 17-36 (2014).
36. Y. Shi, F. Budin, E. Yapuncich, A. Rumple, J. T. Young, C. Payne, X. Zhang, X. Hu, J. Godfrey, B. Howell, M. M. Sanchez, M. A. Styner, UNC-Emory infant atlases for macaque brain image analysis: Postnatal brain development through 12 months. Front. Neurosci. 10, 617 (2017).
37. K. Coleman, P. J. Pierre, Assessing anxiety in nonhuman primates. ILAR J. 55, 333-346 (2014).
38. N. H. Kalin, S. E. Shelton, Defensive behaviors in infant rhesus monkeys: Environmental cues and neurochemical regulation. Science 243, 1718-1721 (1989).
39. J. Raper, K. Wallen, M. M. Sanchez, S. B. Z. Stephens, A. Henry, T. Villareal, J. Bachevalier, Sex-dependent role of the amygdala in the development of emotional and neuroendocrine reactivity to threatening stimuli in infant and juvenile rhesus monkeys. Horm. Behav. 63, 646-658 (2013).
40. J. Raper, M. Wilson, M. Sanchez, C. J. Machado, J. Bachevalier, Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys. Psychoneuroendocrinology 38, 1021-1035 (2013).
41. J. Kagan, J. S. Reznick, N. Snidman, Biological bases of childhood shyness. Science 240, 167-171 (1988).
42. J. Raper, M. Wilson, M. Sanchez, C. Payne, J. Bachevalier, Increased anxiety-like behaviors, but blunted cortisol stress response after neonatal hippocampal lesions in monkeys. Psychoneuroendocrinology 76, 57-66 (2017).
43. A. Bechara, Disturbances of emotion regulation after focal brain lesions. Int. Rev. Neurobiol. 62, 159-193 (2004).
44. A. S. Heberlein, A. A. Padon, S. J. Gillihan, M. J. Farah, L. K. Fellows, Ventromedial frontal lobe plays a critical role in facial emotion recognition. J. Cogn. Neurosci. 20, 721-733 (2008).
45. T. W. Buchanan, S. Kern, J. S. Allen, D. Tranel, C. Kirschbaum, Circadian regulation of cortisol after hippocampal damage in humans. Biol. Psychiatry 56, 651-656 (2004).
46. M. C. Alvarado, K. L. Murphy, M. G. Baxter, Visual recognition memory is impaired in rhesus monkeys repeatedly exposed to sevoflurane in infancy. Br. J. Anaesth. 119, 517-523 (2017).
47. T. M. Burbacher, K. S. Grant, Measuring infant memory: Utility of the visual paired-comparison test paradigm for studies in developmental neurotoxicology. Neurotoxicol. Teratol. 34, 473-480 (2012).
48. J. F. Fagan III, Memory in the infant. J. Exp. Child Psychol. 9, 217-226 (1970).
49. R. L. Fantz, Visual experience in infants: Decreased attention to familiar patterns relative to novel ones. Science 146, 668-670 (1964).
50. F. B. Russo, P. Jungmann, P. C. B. Beltrão-Braga, Zika infection and the development of neurological defects. Cell. Microbiol. 19, e12744 (2017).
51. M. F. V. V. Aragao, A. C. Holanda, A. M. Brainer-Lima, N. C. L. Petribu, M. Castillo, V. van der Linden, S. C. Serpa, A. G. Tenório, P. T. C. Travassos, M. T. Cordeiro, C. Sarteschi, M. M. Valenca, A. Costello, Nonmicrocephalic Infants with congenital Zika syndrome suspected only after neuroimaging evaluation compared with those with microcephaly at birth and postnatally: How large is the Zika virus “iceberg”? AJNR Am. J. Neuroradiol. 38, 1427-1434 (2017).
52. V. van der Linden, A. Pessoa, W. Dobyns, A. J. Barkovich, H. van der Linden Júnior, E. L. R. Filho, E. M. Ribeiro, M. de Carvalho Leal, P. P. de Araújo Coimbra, M. de Fátima Viana Vasco Aragão, I. Verçosa, C. Ventura, R. C. Ramos, D. D. C. S. Cruz, M. T. Cordeiro, V. M. R. Mota, M. Dott, C. Hillard, C. A. Moore, Description of 13 infants born during October 2015-January 2016 with congenital Zika virus infection without microcephaly at birth-Brazil. MMWR Morb. Mortal. Wkly Rep. 65, 1343-1348 (2016).
53. G. Paz-Bailey, E. S. Rosenberg, K. Doyle, J. Munoz-Jordan, G. A. Santiago, L. Klein, J. Perez-Padilla, F. A. Medina, S. H. Waterman, C. G. Gubern, L. I. Alvarado, T. M. Sharp, Persistence of Zika virus in body fluids-Preliminary report. N. Engl. J. Med. (2017).
54. T. M. Bell, E. J. Field, H. K. Narang, Zika virus infection of the central nervous system of mice. Arch. Gesamte Virusforsch. 35, 183-193 (1971).
55. E. Gabriel, A. Ramani, U. Karow, M. Gottardo, K. Natarajan, L. M. Gooi, G. Goranci-Buzhala, O. Krut, F. Peters, M. Nikolic, S. Kuivanen, E. Korhonen, T. Smura, O. Vapalahti, A. Papantonis, J. Schmidt-Chanasit, M. Riparbelli, G. Callaini, M. Krönke, O. Utermöhlen, J. Gopalakrishnan, Recent Zika virus isolates induce premature differentiation of neural progenitors in human brain organoids. Cell Stem Cell 20, 397-406.e5 (2017).
56. C. Li, D. Xu, Q. Ye, S. Hong, Y. Jiang, X. Liu, N. Zhang, L. Shi, C.-F. Qin, Z. Xu, Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19, 120-126 (2016).
57. L. de Noronha, C. Zanluca, M. L. V. Azevedo, K. G. Luz, C. N. D. dos Santos, Zika virus damages the human placental barrier and presents marked fetal neurotropism. Mem. Inst. Oswaldo Cruz 111, 287-293 (2016).
58. X. Qian, H. N. Nguyen, M. M. Song, C. Hadiono, S. C. Ogden, C. Hammack, B. Yao, G. R. Hamersky, F. Jacob, C. Zhong, K.-J. Yoon, W. Jeang, L. Lin, Y. Li, J. Thakor, D. A. Berg, C. Zhang, E. Kang, M. Chickering, D. Nauen, C.-Y. Ho, Z. Wen, K. M. Christian, P.-Y. Shi, B. J. Maher, H. Wu, P. Jin, H. Tang, H. Song, G.-L. Ming, Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165, 1238-1254 (2016).
59. H. Retallack, E. Di Lullo, C. Arias, K. A. Knopp, M. T. Laurie, C. Sandoval-Espinosa, W. R. Mancia Leon, R. Krencik, E. M. Ullian, J. Spatazza, A. A. Pollen, C. Mandel-Brehm, T. J. Nowakowski, A. R. Kriegstein, J. L. DeRisi, Zika virus cell tropism in the developing human brain and inhibition by azithromycin. Proc. Natl. Acad. Sci. U.S.A. 113, 14408-14413 (2016).
60. B. S. F. Souza, G. L. A. Sampaio, C. S. Pereira, G. S. Campos, S. I. Sardi, L. A. R. Freitas, C. P. Figueira, B. D. Paredes, C. K. V. Nonaka, C. M. Azevedo, V. P. C. Rocha, A. C. Bandeira, R. Mendez-Otero, R. R. dos Santos, M. B. P. Soares, Zika virus infection induces mitosis abnormalities and apoptotic cell death of human neural progenitor cells. Sci. Rep. 6, 39775 (2016).
61. H. Tang, C. Hammack, S. C. Ogden, Z. Wen, X. Qian, Y. Li, B. Yao, J. Shin, F. Zhang, E. M. Lee, K. M. Christian, R. A. Didier, P. Jin, H. Song, G.-L. Ming, Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18, 587-590 (2016).
62. M. S. Vermillion, J. Lei, Y. Shabi, V. K. Baxter, N. P. Crilly, M. McLane, D. E. Griffin, A. Pekosz, S. L. Klein, I. Burd, Intrauterine Zika virus infection of pregnant immunocompetent mice models transplacental transmission and adverse perinatal outcomes. Nat. Commun. 8, 14575 (2017).
63. R. W. Driggers, C.-Y. Ho, E. M. Korhonen, S. Kuivanen, A. J. Jääskeläinen, T. Smura, A. Rosenberg, D. A. Hill, R. L. DeBiasi, G. Vezina, J. Timofeev, F. J. Rodriguez, L. Levanov, J. Razak, P. Iyengar, A. Hennenfent, R. Kennedy, R. Lanciotti, A. du Plessis, O. Vapalahti, Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N. Engl. J. Med. 374, 2142-2151 (2016).
64. K. M. A. Waldorf, B. R. Nelson, J. E. Stencel-Baerenwald, C. Studholme, R. P. Kapur, B. Armistead, C. L. Walker, S. Merillat, J. Vornhagen, J. Tisoncik-Go, A. Baldessari, M. Coleman, M. K. Dighe, D. W. W. Shaw, J. A. Roby, V. Santana-Ufret, E. Boldenow, J. Li, X. Gao, M. A. Davis, J. A. Swanstrom, K. Jensen, D. G. Widman, R. S. Baric, J. T. Medwid, K. A. Hanley, J. Ogle, G. M. Gough, W. Lee, C. English, W. M. Durning, J. Thiel, C. Gatenby, E. C. Dewey, M. R. Fairgrieve, R. D. Hodge, R. F. Grant, L. Kuller, W. B. Dobyns, R. F. Hevner, M. Gale Jr., L. Rajagopal, Congenital Zika virus infection as a silent pathology with loss of neurogenic output in the fetal brain. Nat. Med. 24, 368-374 (2018).
65. M. Aid, P. Abbink, R. A. Larocca, M. Boyd, R. Nityanandam, O. Nanayakkara, A. J. Martinot, E. T. Moseley, E. Blass, E. N. Borducchi, A. Chandrashekar, A. L. Brinkman, K. Molloy, D. Jetton, L. J. Tartaglia, J. Liu, K. Best, A. S. Perelson, R. A. De La Barrera, M. G. Lewis, D. H. Barouch, Zika virus persistence in the central nervous system and lymph nodes of rhesus monkeys. Cell 169, 610-620.e14 (2017).
66. A. J. Hirsch, J. L. Smith, N. N. Haese, R. M. Broeckel, C. J. Parkins, C. Kreklywich, V. R. DeFilippis, M. Denton, P. P. Smith, W. B. Messer, L. M. A. Colgin, R. M. Ducore, P. L. Grigsby, J. D. Hennebold, T. Swanson, A. W. Legasse, M. K. Axthelm, R. MacAllister, C. A. Wiley, J. A. Nelson, D. N. Streblow, Zika virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLOS Pathog. 13, e1006219 (2017).
67. M. Besnard, D. Eyrolle-Guignot, P. Guillemette-Artur, S. Lastère, F. Bost-Bezeaud, L. Marcelis, V. Abadie, C. Garel, M.-L. Moutard, J.-M. Jouannic, F. Rozenberg, I. Leparc-Goffart, H.-P. Mallet, Congenital cerebral malformations and dysfunction in fetuses and newborns following the 2013 to 2014 Zika virus epidemic in French Polynesia. Euro. Surveill. 21, 30181 (2016).
68. A. N. Hazin, A. Poretti, D. Di Cavalcanti Souza Cruz, M. Tenorio, A. van der Linden, L. J. Pena, C. Brito, L. H. Gil, D. de Barros Miranda-Filho, E. T. Marques, C. M. Turchi Martelli, J. G. Alves, T. A. Huisman; Microcephaly Epidemic Research Group, Computed tomographic findings in microcephaly associated with Zika virus. N. Engl. J. Med. 374, 2193-2195 (2016).
69. D. H. Gottlieb, J. P. Capitanio, Latent variables affecting behavioral response to the human intruder test in infant rhesus macaques (Macaca mulatta). Am. J. Primatol. 75, 314-323 (2013).
70. G. M. Karere, E. L. Kinnally, J. N. Sanchez, T. R. Famula, L. A. Lyons, J. P. Capitanio, What is an “adverse” environment? Interactions of rearing experiences and MAOA genotype in rhesus monkeys. Biol. Psychiatry 65, 770-777 (2009).
71. E. A. Murray, S. P. Wise, Interactions between orbital prefrontal cortex and amygdala: Advanced cognition, learned responses and instinctive behaviors. Curr. Opin. Neurobiol. 20, 212-220 (2010).
72. E. Bliss-Moreau, G. Moadab, A. Santistevan, D. G. Amaral, The effects of neonatal amygdala or hippocampus lesions on adult social behavior. Behav. Brain Res. 322, 123-137 (2017).
73. G. Moadab, E. Bliss-Moreau, D. G. Amaral, Adult social behavior with familiar partners following neonatal amygdala or hippocampus damage. Behav. Neurosci. 129, 339-350 (2015).
74. G. Moadab, E. Bliss-Moreau, M. D. Bauman, D. G. Amaral, Early amygdala or hippocampus damage influences adolescent female social behavior during group formation. Behav. Neurosci. 131, 68-82 (2017).
75. M. W. Brown, J. P. Aggleton, Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat. Rev. Neurosci. 2, 51-61 (2001).
76. A. Zeamer, E. Heuer, J. Bachevalier, Developmental trajectory of object recognition memory in infant rhesus macaques with and without neonatal hippocampal lesions. J. Neurosci. 30, 9157-9165 (2010).
77. J. Raper, M. C. Alvarado, K. L. Murphy, M. G. Baxter, Multiple anesthetic exposure in infant monkeys alters emotional reactivity to an acute stressor. Anesthesiology 123, 1084-1092 (2015).
78. S. M. Nguyen, K. M. Antony, D. M. Dudley, S. Kohn, H. A. Simmons, B. Wolfe, M. S. Salamat, L. B. C. Teixeira, G. J. Wiepz, T. H. Thoong, M. T. Aliota, A. M. Weiler, G. L. Barry, K. L. Weisgrau, L. J. Vosler, M. S. Mohns, M. E. Breitbach, L. M. Stewart, M. N. Rasheed, C. M. Newman, M. E. Graham, O. E. Wieben, P. A. Turski, K. M. Johnson, J. Post, J. M. Hayes, N. Schultz-Darken, M. L. Schotzko, J. A. Eudailey, S. R. Permar, E. G. Rakasz, E. L. Mohr, S. Capuano III, A. F. Tarantal, J. E. Osorio, S. L. O'Connor, T. C. Friedrich, D. H. O'Connor, T. G. Golos, Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLOS Pathog. 13, e1006378 (2017).
79. M. Zare Mehrjardi, A. Poretti, T. A. G. M. Huisman, H. Werner, E. Keshavarz, E. Araujo Júnior, Neuroimaging findings of congenital Zika virus infection: A pictorial essay. Jpn. J. Radiol. 35, 89-94 (2017).
80. M. Zare Mehrjardi, G. Carteaux, A. Poretti, M. Sanei Taheri, S. Bermudez, H. Werner, L. C. Hygino da Cruz Jr., Neuroimaging findings of postnatally acquired Zika virus infection: A pictorial essay. Jpn. J. Radiol. 35, 341-349 (2017).
81. National Institutes of Health, Study to examine effects of Zika infection in Guatemalan infants and children (2017); https://www.nih.gov/news-events/news-releases/study-examine-effects-zika-infection-guatemalan-infants-children.
82. R. M. Hutchison, T. Womelsdorf, J. S. Gati, S. Everling, R. S. Menon, Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum. Brain Mapp. 34, 2154-2177 (2013).
83. C.-X. Li, S. Patel, E. J. Auerbach, X. Zhang, Dose-dependent effect of isoflurane on regional cerebral blood flow in anesthetized macaque monkeys. Neurosci. Lett. 541, 58-62 (2013).
84. C. Y. Tang, R. Ramani, fMRI and anesthesia. Int. Anesthesiol. Clin. 54, 129-142 (2016).
85. J. L. Vincent, G. H. Patel, M. D. Fox, A. Z. Snyder, J. T. Baker, D. C. Van Essen, J. M. Zempel, L. H. Snyder, M. Corbetta, M. E. Raichle, Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447, 83-86 (2007).
86. M. Beauregard, J. Bachevalier, Neonatal insult to the hippocampal region and schizophrenia: A review and a putative animal model. Can. J. Psychiatry 41, 446-456 (1996).
87. J. Wang, C. Vachet, A. Rumple, S. Gouttard, C. Ouziel, E. Perrot, G. Du, X. Huang, G. Gerig, M. Styner, Multi-atlas segmentation of subcortical brain structures via the AutoSeg software pipeline. Front. Neuroinform. 8, 7 (2014).
88. R. C. Knickmeyer, M. Styner, S. J. Short, G. R. Lubach, C. Kang, R. Hamer, C. L. Coe, J. H. Gilmore, Maturational trajectories of cortical brain development through the pubertal transition: Unique species and sex differences in the monkey revealed through structural magnetic resonance imaging. Cereb. Cortex 20, 1053-1063 (2010).
89. J. L. R. Andersson, S. Skare, J. Ashburner, How to correct susceptibility distortions in spin-echo echo-planar images: Application to diffusion tensor imaging. Neuroimage 20, 870-888 (2003).
90. K. Gorgolewski, C. D. Burns, C. Madison, D. Clark, Y. O. Halchenko, M. L. Waskom, S. S. Ghosh, Nipype: A flexible, lightweight and extensible neuroimaging data processing framework in python. Front. Neuroinform. 5, 13 (2011).
91. D. A. Fair, A. L. Cohen, J. D. Power, N. U. F. Dosenbach, J. A. Church, F. M. Miezin, B. L. Schlaggar, S. E. Petersen, Functional brain networks develop from a “local to distributed” organization. PLOS Comput. Biol. 5, e1000381 (2009).
92. D. A. Fair, N. U. F. Dosenbach, J. A. Church, A. L. Cohen, S. Brahmbhatt, F. M. Miezin, D. M. Barch, M. E. Raichle, S. E. Petersen, B. L. Schlaggar, Development of distinct control networks through segregation and integration. Proc. Natl. Acad. Sci. U.S.A. 104, 13507-13512 (2007).
93. D. A. Fair, J. T. Nigg, S. Iyer, D. Bathula, K. L. Mills, N. U. F. Dosenbach, B. L. Schlaggar, M. Mennes, D. Gutman, S. Bangaru, J. K. Buitelaar, D. P. Dickstein, A. Di Martino, D. N. Kennedy, C. Kelly, B. Luna, J. B. Schweitzer, K. Velanova, Y.-F. Wang, S. Mostofsky, F. X. Castellanos, M. P. Milham, Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Front. Syst. Neurosci. 6, 80 (2013).
94. S. P. Iyer, I. Shafran, D. Grayson, K. Gates, J. T. Nigg, D. A. Fair, Inferring functional connectivity in MRI using Bayesian network structure learning with a modified PC algorithm. Neuroimage 75, 165-175 (2013).
95. O. Miranda-Dominguez, B. D. Mills, D. Grayson, A. Woodall, K. A. Grant, C. D. Kroenke, D. A. Fair, Bridging the gap between the human and macaque connectome: A quantitative comparison of global interspecies structure-function relationships and network topology. J. Neurosci. 34, 5552-5563 (2014).
96. D. G. McLaren, K. J. Kosmatka, E. K. Kastman, B. B. Bendlin, S. C. Johnson, Rhesus macaque brain morphometry: A methodological comparison of voxel-wise approaches. Methods 50, 157-165 (2010).
97. D. G. McLaren, K. J. Kosmatka, T. R. Oakes, C. D. Kroenke, S. G. Kohama, J. A. Matochik, D. K. Ingram, S. C. Johnson, A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage 45, 52-59 (2009).
98. J. D. Power, K. A. Barnes, A. Z. Snyder, B. L. Schlaggar, S. E. Petersen, Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154 (2012).
99. J. D. Power, A. Mitra, T. O. Laumann, A. Z. Snyder, B. L. Schlaggar, S. E. Petersen, Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320-341 (2014).
100. M. Styner, R. Knickmeyer, S. Joshi, C. Coe, S. J. Short, J. Gilmore, Automatic brain segmentation in rhesus monkeys. Proc. SPIE 6512, 65122L (2007).
101. G. Paxinos, X. Huang, A. W. Toga, The Rhesus Monkey Brain in Stereotaxic Coordinates (Academic Press, 1999).
102. K. S. Saleem, N. K. Logothetis, A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates (Academic Press, ed. 2, 2012).
103. C. Payne, J. Bachevalier, Crossmodal integration of conspecific vocalizations in rhesus macaques. PLOS ONE 8, e81825 (2013).