Prenatal stress induces increased striatal dopamine transporter binding in adult nonhuman primates

Biological Psychiatry

Volumn 74, Issue 7, 2013, Pages 502-510

  Converse, Alexander K ^a   Moore, Colleen F ^c,d   Moirano, Jeffrey M ^b   Ahlers, Elizabeth O ^a   Larson, Julie A ^c   Engle, Jonathan W ^b   Barnhart, Todd E ^b   Murali, Dhanabalan ^b   Christian, Bradley T ^b   Dejesus, Onofre T ^b   Holden, James E ^b   Nickles, Robert J ^b   Schneider, Mary L ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d MONTANA STATE UNIVERSITY   (United States)

Author keywords

Brain dopamine transporter prenatal stress primate striatum tactile responsivity

Indexed keywords

DOPAMINE TRANSPORTER; FLUORINE 18; NORTROPANE DERIVATIVE;

ACOUSTIC STRESS; ALCOHOL CONSUMPTION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING KINETICS; CAUDATE NUCLEUS; CONTROLLED STUDY; CORPUS STRIATUM; ENVIRONMENTAL EXPOSURE; FEMALE; HABITUATION; LIGAND BINDING; MALE; MESENCEPHALON; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PREGNANCY; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PUTAMEN; RHESUS MONKEY; STRESS; TACTILE STIMULATION;

BRAIN; DOPAMINE TRANSPORTER; PRENATAL STRESS; PRIMATE; STRIATUM; TACTILE RESPONSIVITY;

ANIMALS; CORPUS STRIATUM; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; FEMALE; MACACA MULATTA; MALE; POSITRON-EMISSION TOMOGRAPHY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PHYSIOLOGICAL; TOUCH PERCEPTION;

EID: 84883797640     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.04.023     Document Type: Article

References (70)

1. B.R.H. Van den Bergh, and A. Marcoen High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8-and 9-year-olds Child Dev 75 2004 1085 1097
2. V. Glover Prenatal stress and the origins of psychopathology: An evolutionary perspective J Child Psychol Psychiatry 52 2011 356 367
3. P.D. Wadhwa, and I.S. Federenko Prenatal stress influences human fetal development and birth outcomes: Implications for development origins of health and disease D.M. Hodgson, C.L. Coe, Perinatal Programming: Early Life Determinants of Adult Health and Disease 2006 Taylor and Francis Group London 29 46
4. D.K. Kinney, K.M. Munir, D.J. Crowley, and A.M. Miller Prenatal stress and risk for autism Neurosci Biobehav Rev 32 2008 1519 1532
5. M.L. Schneider, C.F. Moore, O.T. Dejesus, and A.K. Converse Prenatal stress influences on neurobehavior, stress reactivity, and dopaminergic function in rhesus macaques T. Burbacher, G.P. Sackett, K.S. Grant, Primate Models of Children's Health and Developmental Disabilities 2008 Elsevier New York 231 258
6. M.A. Bozarth The mesolimbic dopamine system as a model reward system P. Willner, J. Scheel-Kruger, The Mesolimbic Dopamine System: From Motivation to Action 1991 Wiley Chichester, England 302 330
7. M.J. Bannon The dopamine transporter: Role in neurotoxicity and human disease Toxicol Appl Pharmacol 204 2005 355 360
8. M.M. Goodman, C.D. Kilts, R. Keil, B. Shi, L. Martarello, and D.X. Xing 18F-labeled FECNT: A selective radioligand for PET imaging of brain dopamine transporters Nucl Med Biol 27 2000 1 12
9. G. Masilamoni, J. Votaw, L. Howell, R.M. Villalba, M. Goodman, and R.J. Voll 18F-FECNT: Validation as PET dopamine transporter ligand in parkinsonism Exp Neurol 226 2010 265 273
10. R.R. Ahn, L.J. Miller, S. Milberger, and D.N. McIntosh Prevalence of parents' perceptions of sensory processing disorders among kindergarten children Am J Occup Ther 58 2004 287 293
11. G.T. Baranek Efficacy of sensory and motor interventions for children with autism J Autism Dev Disord 32 2002 397 422
12. B.J. Casey Disruption of inhibitory control in developmental disorders: A mechanistic model of implicated fronto-striatal circuitry J.L. McClelland, R.S. Siegler, Mechanisms of Cognitive Development: Behavioral and Neural Perspectives 2001 Erlbaum Mahwah, NJ 327 349
13. A.D. Roberts, C.F. Moore, O.T. Dejesus, T.E. Barnhart, J.A. Larson, and J. Mukherjee Prenatal stress, moderate fetal alcohol exposure, and dopamine system function in rhesus monkeys Neurotoxicol Teratol 26 2004 169 178
14. M.L. Schneider, C.F. Moore, L.L. Gajewski, J.A. Larson, A.D. Roberts, A.K. Converse, and O.T. DeJesus Sensory processing disorder in a primate model: Evidence from a longitudinal study of prenatal alcohol and prenatal stress effects Child Dev 79 2008 100 113
15. E.A. Bolan, B. Kivell, V. Jaligam, M. Oz, L.D. Jayanthi, and Y. Han D2 receptors regulate dopamine transporter function via an extracellular signal-regulated kinases 1 and 2-dependent and phosphoinositide 3 kinase-independent mechanism Mol Pharmacol 71 2007 1222 1232
16. J. Zhu, and M.E. Reith Role of the dopamine transporter in the action of psychostimulants, nicotine, and other drugs of abuse CNS Neurol Disord Drug Targets 7 2008 393 409
17. A.-J. Rodrigues, P. Leao, M. Carvalho, O.F.X. Almeida, and N. Sousa Potential programming of dopaminergic circuits by early life stress Psychopharmacology 214 2011 107 120
18. G.H. Son, S. Chung, D. Geum, S.S. Kang, W.S. Choi, K. Kim, and S. Choi Hyperactivity and alteration of the midbrain dopaminergic system in maternally stressed male mice offspring Biochem Biophys Res Commun 352 2007 823 829
19. M.L. Schneider, C.F. Moore, and M.M. Adkins The effects of prenatal alcohol exposure on behavior: Rodent and primate studies Neuropsychol Rev 21 2011 186 203
20. M.L. Schneider, and C.F. Moore Effects of prenatal stress on development: A nonhuman primate model C. Nelson, Minnesota Symposium on Child Psychology 2000 Lawrence Erlbaum Hillsdale, NJ 201 244
21. M.L. Schneider, E.C. Roughton, and G.R. Lubach Moderate alcohol consumption and psychological stress during pregnancy induce attention and neuromotor impairments in primate infants Child Dev 68 1997 747 759
22. M.L. Schneider, C.F. Moore, and G.W. Kraemer Moderate level alcohol during pregnancy, prenatal stress, or both and limbic-hypothalamic-pituitary- adrenocortical axis response to stress in rhesus monkeys Child Dev 75 2004 96 109
23. M.L. Schneider, C.F. Moore, and G.W. Kraemer Moderate alcohol during pregnancy: Learning and behavior in adolescent rhesus monkeys Alcohol Clin Exp Res 25 2001 1383 1392
24. G.T. Baranek, and G. Berkson Tactile defensiveness in children with developmental disabilities: Responsiveness and habituation J Autism Dev Disord 24 1994 457 471
25. L.J. Miller, D.N. McIntosh, J. McGrath, V. Shyu, M. Lampe, and A.K. Taylor Electrodermal responses to sensory stimuli in individuals with fragile X syndrome: A preliminary report Am J Med Genet 83 1999 268 279
26. D. Murali, T.E. Barnhart, N.T. Vandehey, B.T. Christian, R.J. Nickles, and A.K. Converse An efficient synthesis of dopamine transporter tracer [(18)F]FECNT Appl Radiat Isot 72 2013 128 132
27. Y.C. Tai, A. Chatziioannou, S. Siegel, J. Young, D. Newport, and R.N. Goble Performance evaluation of the microPET P4: A PET system dedicated to animal imaging Phys Med Biol 46 2001 1845 1862
28. G. Paxinos, X.-F. Huang, M. Petrides, and A.W. Toga The Rhesus Monkey Brain in Stereotaxic Coordinates 2nd ed 2009 Academic Press, San Diego 416
29. D.G. McLaren, K.J. Kosmatka, T.R. Oakes, C.D. Kroenke, S.G. Kohama, and J.A. Matochik A population-average MRI-based atlas collection of the rhesus macaque Neuroimage 45 2009 52 59
30. J. Logan, J.S. Fowler, N.D. Volkow, G.J. Wang, Y.S. Ding, and D.L. Alexoff Distribution volume ratios without blood sampling from graphical analysis of PET data J Cereb Blood Flow Metab 16 1996 834 840
31. R.B. Innis, V.J. Cunningham, J. Delforge, M. Fujita, A. Giedde, and R.N. Gunn Consensus nomenclature for in vivo imaging of reversibly binding radioligands J Cereb Blood Flow Metab 27 2007 1533 1539
32. S.E. Best, P.M. Sarrel, R.T. Malison, M. Laruelle, S.S. Zoghbi, and R.M. Baldwin Striatal dopamine transporter availability with [123I]beta-CIT SPECT is unrelated to gender or menstrual cycle Psychopharmacology 183 2005 181 189
33. C.H. Van Dyck, J.P. Seibyl, R.T. Malison, M. Laruelle, E. Wallace, and S.S. Zoghbi Age-related decline in striatal dopamine transporter binding with iodine-123-beta-CITSPECT J Nucl Med 36 1995 1175 1181
34. J. Lavalaye, J. Booij, L. Reneman, J.B. Habraken, and E.A. Van Royen Effect of age and gender on dopamine transporter imaging with [123I]FP-CIT SPET in healthy volunteers Eur J Nucl Med 27 2000 867 869
35. A. Eusebio, J.-P. Azulay, M. Ceccaldi, N. Girard, O. Mundler, and E. Guedj Voxel-based analysis of whole-brain effects of age and gender on dopamine transporter SPECT imaging in healthy subjects Eur J Nucl Med Mol Imaging 39 2012 1778 1783
36. L.H. Mozley, R.C. Gur, P.D. Mozley, and R.E. Gur Striatal dopamine transporters and cognitive functioning in healthy men and women Am J Psychiatry 158 2001 1492 1499
37. J.K. Staley, S. Krishnan-Sarin, S. Zoghbi, G. Tamagnan, M. Fujita, and J.P. Seibyl Sex differences in [123I]beta-CIT SPECT measures of dopamine and serotonin transporter availability in healthy smokers and nonsmokers Synapse 41 2001 275 284
38. K.K. Wong, MLTM Müller, H. Kuwabara, S.A. Studenski, and N.I. Bohnen Gender differences in nigrostriatal dopaminergic innervation are present at young-to-middle but not at older age in normal adults J Clin Neurosci 19 2012 183 184
39. A. Varrone, and C. Halldin Molecular imaging of the dopamine transporter J Nucl Med 51 2010 1331 1334
40. C.A. Sandman, E.P. Davis, C. Buss, and L.M. Glynn Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus Neuroendocrinology 95 2011 8 21
41. K.P. Bhatia, and C.D. Marsden The behavioural and motor consequences of focal lesions of the basal ganglia in man Brain 117 1994 859 876
42. T.J. Spencer, J. Biederman, B.K. Madras, D.D. Dougherty, A.A. Bonab, and E. Livni Further evidence of dopamine transporter dysregulation in ADHD: A controlled PET imaging study using altropane Biol Psychiatry 62 2007 1059 1061
43. N.D. Volkow, G.-J. Wang, S.H. Kollins, T.L. Wigal, J.H. Newcorn, and F. Telang Evaluating dopamine reward pathway in ADHD: Clinical implications JAMA 302 2009 1084 1091
44. S.J. Alonso, E. Navarro, C. Santana, and M. Rodriguez Motor lateralization, behavioral despair and dopaminergic brain asymmetry after prenatal stress Pharmacol Biochem Behav 58 1997 443 448
45. K.H.C. Choy, Y.P. De Visser, and M. Van den Buuse The effect of "two hit" neonatal and young-adult stress on dopaminergic modulation of prepulse inhibition and dopamine receptor density Br J Pharmacol 156 2009 388 396
46. E. Fride, and M. Weinstock Alterations in behavioral and striatal dopamine asymmetries induced by prenatal stress Pharmacol Biochem Behav 32 1989 425 430
47. C. Henry, G. Guegant, M. Cador, E. Arnauld, J. Arsaut, M. Le Moal, and J. Demotes-Mainard Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine-receptors in the nucleus-accumbens Brain Res 685 1995 179 186
48. W.O. McClure, A. Ishtoyan, and M. Lyon Very mild stress of pregnant rats reduces volume and cell number in nucleus accumbens of adult offspring: some parallels to schizophrenia Brain Res Dev Brain Res 149 2004 21 28
49. G.M. Miller, S.M. Yatin, R. De La Garza, M. Goulet, and B.K. Madras Cloning of dopamine, norepinephrine and serotonin transporters from monkey brain: relevance to cocaine sensitivity Brain Res Mol Brain Res 87 2001 124 143
50. N.H. Chen, and M.E.A. Reith Structure and function of the dopamine transporter Eur J Pharmacol 405 2000 329 339
51. P.-O. Fernagut, S. Chalon, E. Diguet, D. Guilloteau, F. Tison, and M. Jaber Motor behaviour deficits and their histopathological and functional correlates in the nigrostriatal system of dopamine transporter knockout mice Neuroscience 116 2003 1123 1130
52. P. Joti, S. Kulashekhar, M. Behari, and A. Murthy Impaired inhibitory oculomotor control in patients with Parkinson's disease Exp Brain Res 177 2007 447 457
53. D. Gaffan Memory, action and the corpus striatum: Current developments in the memory-habit distinction Semin Neurosci 8 1996 33 38
54. S. Jackson, and G. Houghton Sensorimotor selection and the basal ganglia: A neruonal network model J.C. Houk, J.L. Davis, D.G. Beiser, Models of Information Processing in the Basal Ganglia 1995 MIT Press Cambridge, MA 337 369
55. J.M.A. Teixeira, N.M. Fisk, and V. Glover Association between maternal anxiety in pregnancy and increased uterine artery resistance index: Cohort based study BMJ 318 1999 153 157
56. L.K. Takahashi, J.G. Turner, and N.H. Kalin Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: Implications for prenatal stress studies Psychoneuroendocrinology 23 1998 571 581
57. R. Gitau, A. Cameron, N.M. Fisk, and V. Glover Fetal exposure to maternal cortisol Lancet 352 1998 707 708
58. A. Barbazanges, P.V. Piazza, M. Le Moal, and S. Maccari Maternal glucocorticoid secretion mediates long-term effects of prenatal stress J Neurosci 16 1996 3943 3949
59. R. Benediktsson, A.A. Calder, C.R.W. Edwards, and J.R. Seckl Placental 11 beta-hydroxysteroid dehydrogenase: A key regulator of fetal glucocorticoid exposure Clin Endocrinol (Oxf) 46 1997 161 166
60. M. Shams, M.D. Kilby, D.A. Somerset, A.J. Howie, A. Gupta, and P.J. Wood 11Beta-hydroxysteroid dehydrogenase type 2 in human pregnancy and reduced expression in intrauterine growth restriction Hum Reprod 13 1998 799 804
61. L.A.M. Welberg, K.V. Thrivikraman, and P.M. Plotsky Chronic maternal stress inhibits the capacity to up-regulate placental 11beta-hydroxysteroid dehydrogenase type 2 activity J Endocrinol 186 2005 R7 R12
62. P.J. Lucassen, O.J. Bosch, E. Jousma, S.A. Kroemer, R. Andrew, J.R. Seckl, and I.D. Neumann Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: Possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2 Eur J Neurosci 29 2009 97 103
63. E. Isovich, M.J. Mijnster, G. Flugge, and E. Fuchs Chronic psychosocial stress reduces the density of dopamine transporters Eur J Neurosci 12 2000 1071 1078
64. M. Cyr, M. Morissette, N. Barden, S. Beaulieu, J. Rochford, and T. Di Paolo Dopaminergic activity in transgenic mice underexpressing glucocorticoid receptors: Effect of antidepressants Neuroscience 102 2001 151 158
65. V. Sossi, K. Dinelle, S. Jivan, K. Fischer, J.E. Holden, and D. Doudet In vivo dopamine transporter imaging in a unilateral 6-hydroxydopamine rat model of Parkinson disease using 11C-methylphenidate PET J Nucl Med 53 2012 813 822
66. G.M. Raab Selecting confounders from covariates J R Stat Soc Ser A Stat Soc 157 1994 271
67. S.S. Zoghbi, H.U. Shetty, M. Ichise, M. Fujita, M. Imaizumi, and J.-S. Liow PET imaging of the dopamine transporter with 18F-FECNT: A polar radiometabolite confounds brain radioligand measurements J Nucl Med 47 2006 520 527
68. J.C. Price, B.J. Lopresti, C.C. Meltzer, G.S. Smith, N.S. Mason, and Y. Huang Analyses of [(18)F]altanserin bolus injection PET data. II: Consideration of radiolabeled metabolites in humans Synapse 41 2001 11 21
69. M. Ichise, H. Toyama, R.B. Innis, and R.E. Carson Strategies to improve neuroreceptor parameter estimation by linear regression analysis J Cereb Blood Flow Metab 22 2002 1271 1281
70. J. Votaw, M. Byas-Smith, J. Hua, R. Voll, L. Martarello, and A.I. Levey Interaction of isoflurane with the dopamine transporter Anesthesiology 98 2003 404 411