Behavioral effects of prenatal ketamine exposure in rhesus macaques are dependent on MAOA genotype

Experimental and Clinical Psychopharmacology

Volumn 20, Issue 3, 2012, Pages 173-180

  Capitanio, John P ^a   Del Rosso, Laura A ^a   Calonder, Laura A ^a   Blozis, Shelley A ^b   Penedo, M Cecilia T ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anxiety; Ketamine; MAOA; Rhesus monkey; Temperament

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; KETAMINE; AMINE OXIDASE (FLAVIN CONTAINING);

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONCEPTION; CONTROLLED STUDY; EMOTIONALITY; FEMALE; FIRST TRIMESTER PREGNANCY; GENETIC TRAIT; GENOTYPE; MALE; MATERNAL DEPRIVATION; NONHUMAN; PREGNANCY; PRENATAL DRUG EXPOSURE; PRENATAL PERIOD; RECOGNITION; RHESUS MONKEY; SECOND TRIMESTER PREGNANCY; THIRD TRIMESTER PREGNANCY; ANIMAL; DRUG EFFECT; EMOTION; EXPLORATORY BEHAVIOR; GENETICS; PRENATAL EXPOSURE; PSYCHOLOGICAL ASPECT;

ANIMALS; EMOTIONS; EXPLORATORY BEHAVIOR; FEMALE; GENOTYPE; KETAMINE; MACACA MULATTA; MALE; MATERNAL DEPRIVATION; MONOAMINE OXIDASE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECOGNITION (PSYCHOLOGY);

EID: 84867907155     PISSN: 10641297     EISSN: 19362293     Source Type: Journal    
DOI: 10.1037/a0026773     Document Type: Article

References (44)

1. Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. London, United Kingdom: Sage.
2. Ansorge, M. S., Zhou, M., Lira, A., Hen, R., & Gingrich, J. A. (2004). Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science, 306, 879-881. doi:10.1126/science.1101678.
3. Bachevalier, J., Brickson, M., & Hagger, C. (1993). Limbic-dependent recognition memory in monkeys develops early in infancy. Neuroreport: An International Journal for the Rapid Communication of Research in Neuroscience, 4, 77-80. doi:10.1097/00001756-199301000-00020.
4. Bubeníková-Valešová, V., Horácek, J., Vrajová, M., & Höschl, C. (2008). Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neuroscience and Biobehavioral Reviews, 32, 1014-1023. doi:10.1016/j.neubiorev.2008.03.012.
5. Capitanio, J. P., Mason, W. A., Mendoza, S. P., Del Rosso, L. A., & Roberts, J. A. (2006). Nursery rearing and biobehavioral organization. In: G. P. Sackett, G. Ruppenthal, & K. Elias, (Eds.), Nursery rearing of nonhuman primates in the 21st century (pp. 191-214). New York, NY: Springer. doi:10.1007/978-0-387-25640-5_11.
6. Cases, O., Seif, I., Grimsby, J., Gaspar, P., Chen, K., Pournin, S., De Maeyer, E. (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science, 268, 1763-1766. doi:10.1126/science.7792602.
7. Chen, K., Holschneider, D. P., Wu, W., Rebrin, I., & Shih, J. C. (2004). A spontaneous point mutation produces monoamine oxidase A/B knockout mice with greatly elevated monoamines and anxiety-like behavior. The Journal of Biological Chemistry, 279, 39645-39652. doi:10.1074/jbc.M405550200.
8. Cheng, A., Scott, A. L., Ladenheim, B., Chen, K., Ouyang, X., Lathia, J.D., Shih, J. C. (2010). Monoamine oxidases regulate telence-phalic neural progenitors in late embryonic and early postnatal development. The Journal of Neuroscience, 30, 10752-62. doi: 10.1523/JNEUROSCI.2037-10.2010.
9. Deasy, C., & Babl, F. E. (2010). Intravenous vs. intramuscular ketamine for pediatric procedural sedation by emergency medicine specialists: A review. Paediatric Anaesthesia, 20, 787-796. doi:10.1111/j.1460-9592.2010.03338.x.
10. Dobbing, J., & Sands, J. (1979). The brain growth spurt in various mammalian species. Early Human Development, 3, 79-83. doi:10.1016/0378-3782(79)90022-7.
11. D'Souza, U. M., & Craig. I. W. (2006). Functional polymorphisms in dopamine and serotonin pathway genes. Human Mutation, 27, 1-13. doi:10.1002/humu.20278.
12. Ellingson, A., Haram, K., Sagen, N., & Solheim, E. (1977). Transplacental passage of ketamine after intravenous administration. Acta Anaesthesiologica Scandinavica, 21, 41-44. doi:10.1111/j.1399-6576.1977.tb01191.x Fredriksson, A., Archer, T., Alm, H., Gordh, T., & Eriksson, P. (2004). Neurofunctional deficits and potentiated apoptosis by neonatal NMDA antagonist administration. Behavioural Brain Research, 153, 367-376. doi:10.1016/j.bbr.2003.12.026.
13. Fredriksson, A., Archer, T., Alm, H., Gordh, T., & Eriksson, P. (2004). Neurofunctional deficits and potentiated apoptosis by neonatal NMDA antagonist administration. Behavioural Brain Research, 153, 367-376. doi:10.1016/j.bbr.2003.12.026.
14. Gaspar, P., Cases, O., & Maroteaux, L. (2003). The developmental role of serotonin: News from mouse molecular genetics. Nature Reviews Neuroscience, 4, 1002-1012. doi:10.1038/nrn1256.
15. Golub, M. S., Hogrefe, C. E., Widaman, K. F., & Capitanio, J. P. (2009). Iron deficiency anemia and affective response in rhesus monkey infants. Developmental Psychobiology, 51, 47-59. doi:10.1002/dev.20345.
16. Granger, B., Tekaia, F., Le Sourd, A. M., Rakic, P., & Bourgeois, J.-P. (1995). Tempo of neurogenesis and synaptogenesis in the primate cingulate mesocortex: Comparison with the neocortex. The Journal of Comparative Neurology, 360, 363-376. doi:10.1002/cne.903600212.
17. Gunderson, V. M., Grant-Webster, K. S., Burbacher, T. M., & Mottet, N. K. (1988). Visual recognition memory deficits in methylmercury-exposed Macaca fascicularis infants. Neurotoxicology and Teratology, 10, 373-379. doi:10.1016/0892-0362(88)90041-4.
18. Gunderson, V. M., Grant-Webster, K. S., & Fagan, J. F. (1987). Visual recognition memory in high-and low-risk infant pigtailed macaques (Macaca nemestrina). Developmental Psychology, 23, 671-675. doi: 10.1037/0012-1649.23.5.671.
19. Gunduz-Bruce, H. (2009). The acute effects of NMDA antagonism: From the rodent to the human brain. Brain Research Reviews, 60, 279-286. doi:10.1016/j.brainresrev.2008.07.006.
20. Herlenius, E., & Lagercrantz, H. (2004). Development of neurotransmitter systems during critical periods. Experimental Neurology, 190, Suppl. 1, 8-21. doi:10.1016/j.expneurol.2004.03.027.
21. Kapur, S., & Seeman, P. (2002). NMDA receptor antagonists ketamine and PCP have direct effects on the dopamine D(2) and serotonin 5-HT(2) receptors-implications for models of schizophrenia. Molecular Psychiatry, 7, 837-844. doi:10.1038/sj.mp.4001093.
22. Karere, G. M., Kinnally, E. L., Sanchez, J. N., Famula, T. R., Lyons, L. A., & Capitanio. J. P. (2009). What is an "adverse" environment? Interactions of rearing experiences and MAOA genotype in rhesus monkeys. Biological Psychiatry, 65, 770-777. doi:10.1016/j.biopsych.2008.11.004.
23. Kari, H. P., Davidson, P. P., Kohl, H. H., & Kochhar, M. M. (1978). Effects of ketamine on brain monoamine levels in rats. Research Communications in Chemical Pathology and Pharmacology, 20, 475-488.
24. Krystal, J. H., Mathew, S. J., D'Souza, D. C., Garakani, A., Gunduz-Bruce, H., & Charney, D. S. (2010). Potential psychiatric applications of metabotropic glutamate receptor agonists and antagonists. CNS Drugs, 24, 669-693. doi:10.2165/11533230-000000000-00000.
25. Levitt, P., & Rakic, P. (1982). The time of genesis, embryonic origin and differentiation of the brainstem monoaminergic neurons in the rhesus monkey. Developmental Brain Research, 4, 35-57. doi:10.1016/0165-3806(82)90095-5.
26. Machado-Vieira, R., Salvadore, G., Diazgranados, N., & Zarate, C. A., Jr. (2009). Ketamine and the next generation of antidepressants with a rapid onset of action. Pharmacology & Therapeutics, 123, 143-150. doi: 10.1016/j.pharmthera.2009.02.010.
27. Medeiros, L. F., Rozisky, J. R., De Souza, A., Hidalgo, M. P., Netto, C. A., Caumo, Torres, I. L. S. (2011). Lifetime behavioural changes after exposure to anaesthetics in infant rats. Behavioural Brain Research, 218, 51-56. doi:10.1016/j.bbr.2010.10.028.
28. Mickley, G. A., Kenmuir, C. L., McMullen, C. A., Snyder, A., Yocom, A. M., Likins-Fowler, D., Biada, J. M. (2004). Long-term age-dependent behavioral changes following a single episode of fetal N-methyl-D-Aspartate (NMDA) receptor blockade. BMC Pharmacology, 4, 28. doi:10.1186/1471-2210-4-28.
29. Mickley, G. A., Remmers-Roeber, D. R., Crouse, C., & Peluso, R. (2000). Ketamine blocks a taste recognition memory in fetal rats. Pharmacology, Biochemistry and Behavior, 67, 575-581. doi:10.1016/S0091-3057(00)00391-9.
30. Mickley, G. A., Schaldach, M. A., Snyder, K. J., Balogh, S. A., Len, T., Neimanis, K., Yamamoto, B. K. (1998). Ketamine blocks a conditioned taste aversion (CTA) in neonatal rats. Physiology & Behavior, 64, 381-390. doi:10.1016/S0031-9384(98)00097-3.
31. Moghaddam, B., Adams, B., Verma, A., & Daly, D. (1997). Activation of glutamatergic neurotransmission by ketamine: A novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. The Journal of Neuroscience, 17, 2921-2927.
32. Muir, W. W. (2010). NMDA receptor antagonists and pain: Ketamine. The Veterinary Clinics of North America Equine Practice, 26, 565-578. doi:10.1016/j.cveq.2010.07.009.
33. Newman, T. K., Syagailo, Y. V., Barr, C. S., Wendland, J. R., Champoux, M., Graessle, M., Lesch, K. P. (2005). Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biological Psychiatry, 57, 167-172. doi:10.1016/j.biopsych.2004.10.012.
34. Nguyen, L., Rigo, J-M., Rocher, V., Belachew, S., Malgrange, B., Rogister, B., Moonen, G. (2001). Neurotransmitters as early signals for central nervous system development. Cell and Tissue Research, 305, 187-202. doi:10.1007/s004410000343.
35. Noldus L. P. J. J. (1991). The Observer: A software system for collection and analysis of observational data. Behavior Research Methods, Instruments & Computers, 23, 415-429.
36. Paule, M. G., Li, M., Allen, R. R., Liu, F., Zou, X., Hotchkiss, C., Wang, C. (2011). Ketamine anesthesia during the first week of life can cause long-lasting cognitive deficits in rhesus monkeys. Neurotoxicology and Teratology, 33, 220-230. doi:10.1016/j.ntt.2011.01.001 Reynaud-Maurupt, C., Bello, P. Y., Akoka, S., & Toufik, A. (2007). Characteristics and behaviors of ketamine users in France in 2003. Journal of Psychoactive Drugs, 39, 1-11. doi:10.1080/02791072.2007.10399859.
37. Rudin, M., Ben-Abraham, R., Gazit, V., Tendler, Y., Tashlykov, V., & Katz, Y. (2005). Single-dose ketamine administration induces apoptosis in neonatal mouse brain. Journal of Basic and Clinical Physiology and Pharmacology, 16, 231-243.
38. Sabol, S. Z., Hu, S., & Hamer, D. (1998). A functional polymorphism in the monoamine oxidase A gene promoter. Human Genetics, 103, 273-279. doi:10.1007/s004390050816.
39. Sancristobal-Gaudy, M., Renand, G., Amigues, Y., Boscher, M-Y., Levéziel, H., & Bibé, B. (2000). Traçabilité individuelle des viands bovines l'aide de marqueurs génétiques. INRA Productions Animales, 13, 269-276.
40. Scheetz, A. J., & Constantine-Paton, M. (1994). Modulation of NMDA receptor function: Implications for vertebrate neural development. The FASEB Journal, 8, 745-752.
41. Seeman, P., Ko, F., & Tallerico, T. (2005). Dopamine receptor contribution to the action of PCP, LSD and ketamine psychotomimetics. Molecular Psychiatry, 9,877-883. doi:10.1038/sj.mp.4001682.
42. Slikker, W. Jr., Zou, X., Hotchkiss, C. E., Divine, R. L., Sadovova, N., Twaddle, N. C., Wang, C. (2007). Ketamine-induced neuronal cell death in the perinatal rhesus monkey. Toxicological Sciences, 98, 145-158. doi:10.1093/toxsci/kfm084.
43. Wakschlag, L. S., Kistner, E. O., Pine, D. S., Biesecker, G., Pickett, K. E., Skol, A. D., Cook Jr., E. H. (2010). Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Molecular Psychiatry, 15, 928-937. doi:10.1038/mp.2009.22.
44. Ylitalo, P., Saarnivaara, L., & Ahtee, L. (1976). Effect of ketamine anaesthesia on the content of monoamines and their metabolites in the rat brain. Acta Anaesthesiologica Scandinavica, 20, 216-220.