Prenatal serotonin reuptake inhibitor (SRI) antidepressant exposure and serotonin transporter promoter genotype (SLC6A4) influence executive functions at 6 years of age

Frontiers in Cellular Neuroscience

Volumn , Issue OCT, 2013, Pages

  Weikum, Whitney M ^a   Brain, Ursula ^a   Chau, Cecil M Y ^a   Grunau, Ruth E ^a   Boyce, W Thomas ^a   Diamond, Adele ^b   Oberlander, Tim F ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Childhood; Depression; Executive function; Prenatal exposure; Serotonin; SLC6A4 genotype; SRI

Indexed keywords

SEROTONIN TRANSPORTER; SEROTONIN UPTAKE INHIBITOR;

ADULT; ARTICLE; ATTENTION DISTURBANCE; CHILD; CHILD BEHAVIOR; CHILD DEVELOPMENT; CONTROLLED STUDY; COPING BEHAVIOR; DEVELOPMENTAL STAGE; DISEASE SEVERITY; EXECUTIVE FUNCTION; FEMALE; GENE FREQUENCY; GENETIC VARIABILITY; HUMAN; MALE; MOOD; ONSET AGE; PARENTAL ATTITUDE; PRENATAL DRUG EXPOSURE; PRESCHOOL CHILD; PROMOTER REGION; PUERPERAL DEPRESSION; SLC6A4 GENE; TASK PERFORMANCE; THIRD TRIMESTER PREGNANCY;

EID: 84886813311     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00180     Document Type: Article

References (124)

1. Ablow, J. C., Measelle, J. R., Kraemer, H. C., Harrington, R., Luby, J., Smider, N., et al. (1999). The macarthur three-city outcome study: evaluating multi-informant measures of young children's symptomatology. J. Am. Acad. Child Adolesc. Psychiatry 38, 1580-1590. doi: 10.1097/00004583-199912000-00020
2. American Psychiatric Association. (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR®. Washington, DC: American Psychiatric Pub.
3. Ansorge, M. S., Hen, R., and Gingrich, J. A. (2007). Neurodevelopmental origins of depressive disorders. Curr. Opin. Pharmacol. 7, 8-17. doi: 10.1016/j.coph.2006.11.006
4. Ansorge, M. S., Morelli, E., and Gingrich, J. A. (2008). Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice. J. Neurosci. 28, 199-207. doi: 10.1523/JNEUROSCI.3973-07.2008
5. Ansorge, M. S., Zhou, M., Lira, A., Hen, R., and Gingrich, J. A. (2004). Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science306, 879-881. doi: 10.1126/science.1101678
6. Bairy, K., Madhyastha, S., Ashok, K., Bairy, I., and Malini, S. (2006). Developmental and behavioral consequences of prenatal fluoxetine. Pharmacology 79, 1-11. doi: 10.1159/000096645
7. Barr, C. S., Newman, T. K., Lindell, S., et al. (2004). Interaction between serotonin transporter gene variation and rearingcondition in alcohol preference and consumption in female primates. Arch. Gen. Psychiatry 61, 1146-1152. doi: 10.1001/archpsyc.61.11.1146
8. Belsky, J., Bakermans-Kranenburg, M. J., and van Ijzendoorn, M. H. F. (2007). For better and for worse: differential susceptibility to environmental influences. Curr. Dir. Psychol. Sci. 16, 300-304. doi: 10.1111/j.1467-8721.2007.00525.x
9. Belsky, J., and Pluess, M. (2009). Beyond diathesis stress: differential susceptibility to environmental influences. Psychol. Bull. 135, 885-908. doi: 10.1037/a0017376
10. Bernier, A., Carlson, S. M., Deschênes, M., and Matte-Gagné, C. (2011). Social factors in the development of early executive functioning: a closer look at the caregiving environment. Dev. Sci. 15, 12-24. doi: 10.1111/j.1467-7687.2011.01093.x
11. Blair, C. (2002). School readiness: Integrating cognition and emotion in a neurobiological conceptualization of children's functioning at school entry. Am. Psychol. 57, 111. doi: 10.1037/0003-066X.57.2.111
12. Blair, C., Granger, D., and Peters Razza, R. (2005). Cortisol reactivity is positively related to executive function in preschool children attending Head Start. Child Dev. 76, 554-567. doi: 10.1111/j.1467-8624.2005.00863.x
13. Blair, C., and Razza, R. P. (2007). Relating effortful control, executive function, and false belief understanding to emerging math and literacy ability in kindergarten. Child Dev. 78, 647-663. doi: 10.1111/j.1467-8624.2007.01019.x
14. Blood-Siegfried, J., and Rende, E. K. (2010). The long-term effects of prenatal nicotine exposure on neurologic development. J. Midwifery Womens Health 55, 143-152. doi: 10.1016/j.jmwh.2009.05.006
15. Borg, J., Henningsson, S., Saijo, T., Inoue, M., Bah, J., Westberg, L., et al. (2009). Serotonin transporter genotype is associated with cognitive performance but not regional 5-HT1A receptor binding in humans. Int. J. Neuropsychopharmacol. 12, 783-792. doi: 10.1017/S1461145708009759
16. Boyce, W. T., Chesney, M., Alkon, A., Tschann, J. M., Adams, S., Chesterman, B., et al. (1995). Psychobiologic reactivity to stress and childhood respiratory illnesses: results of two prospective studies. Psychosom. Med. 57, 411-422.
17. Boyce, W. T., and Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev. Psychopathol. 17, 271-301. doi: 10.1017/S0954579405050145
18. Boyce, W. T., Essex, M. J., Woodward, H. R., Measelle, J. R., Ablow, J. C., and Kupfer, D. J. (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood. I: exploring the "headwaters" of early life morbidities. J. Am. Acad. Child Adolesc. Psychiatry 41, 580-587. doi: 10.1097/00004583-200205000-00016
19. Boyle, M. H., Offord, D. R., Racine, Y., Fleming, J. E., Szatmari, P., and Sanford, M. (1993). Evaluation of the revised Ontario child health study scales. J. Child Psychol. Psychiatry 34, 189-213. doi: 10.1111/j.1469-7610.1993.tb00979.x
20. Braver, T. S., Cohen, J. D., and Barch, D. M. (2002). "The role of the prefrontal cortex in normal and disordered cognitive control: a cognitive neuroscience perspective, " inPrinciples of Frontal Lobe Function, eds D. T. Stuss and R. T. Knight (Oxford, England: Oxford University Press), 428-448.
21. Brigman, J. L., Mathur, P., Harvey-White, J., Izquierdo, A., Saksida, L. M., Bussey, T. J., et al. (2010). Pharmacological or genetic inactivation of the serotonin transporter improves reversal learning in mice. Cereb. Cortex 20, 1955-1963. doi: 10.1093/cercor/bhp266
22. Bull, R., and Scerif, G. (2001). Executive functioning as a predictor of children's mathematics ability: Inhibition, switching, and working memory. Dev. Neuropsychol. 19, 273-293. doi: 10.1207/S15326942DN1903_3
23. Buss, C., Davis, E., Hobel, C., and Sandman, C. (2011). Maternal pregnancy-specific anxiety is associated with child executive function at 6-9 years age. Stress 14, 665-676.
24. Canli, T., Omura, K., Haas, B. W., Fallgatter, A., Constable, R. T., and Lesch, K. P. (2005). Beyond affect: a role for genetic variation of the serotonin transporter in neural activation during a cognitive attention task. Proc. Natl. Acad. Sci. U.S.A. 102, 12224-12229. doi: 10.1073/pnas.0503880102
25. Carlson, S. M. (2003). Executive function in context: development, measurement, theory, and experience. Monogr. Soc. Res. Child Dev. 68, 138-151. doi: 10.1111/j.1540-5834.2003.06803012.x
26. Caspi, A., and Moffitt, T. E. (2006). Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat. Rev. Neurosci. 7, 583-590. doi: 10.1038/nrn1925
27. Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389. doi: 10.1126/science.1083968
28. Champod, A. S., and Petrides, M. (2007). Dissociable roles of the posterior parietal and the prefrontal cortex in manipulation and monitoring processes. Proc. Natl. Acad. Sci. U.S.A. 104, 14837-14842. doi: 10.1073/pnas.0607101104
29. Clarke, H., Walker, S., Dalley, J., Robbins, T., and Roberts, A. (2007). Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. Cereb. Cortex 17, 18-27. doi: 10.1093/cercor/bhj120
30. Cooper, W. O., Willy, M. E., Pont, S. J., and Ray, W. A. (2007). Increasing use of antidepressants in pregnancy. Am. J. Obstet. Gynecol. 196, 544. e1-544. e5. doi: 10.1016/j.ajog.2007.01.033
31. Davidson, M. C., Amso, D., Anderson, L. C., and Diamond, A. (2006). Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia 44, 2037. doi: 10.1016/j.neuropsychologia.2006.02.006
32. Davis, E. P., Buss, C., Muftuler, L. T., Head, K., Hasso, A., Wing, D. A., et al. (2011). Children's brain development benefits from longer gestation. Front. Psychol. 2, 1-7. doi: 10.3389/fpsyg.2011.00001
33. Diamond, A. (2011). Biological and social influences on cognitive control processes dependent on prefrontal cortex. Prog. Brain Res. 189, 319-339. doi: 10.1016/B978-0-444-53884-0.00032-4
34. Diamond, A. (2013). Executive Functions. Annu. Rev. Psychol. 64, 135-168. doi: 10.1146/annurev-psych-113011-143750
35. Diamond, A., Barnett, W. S., Thomas, J., and Munro, S. (2007). Preschool program improves cognitive control. Science 318, 1387-1388. doi: 10.1126/science.1151148
36. DiPietro, J. A., Novak, M. F. S. X., Costigan, K. A., Atella, L. D., and Reusing, S. P. (2006). Maternal psychological distress during pregnancy in relation to child development at age two. Child Dev. 77, 573-587. doi: 10.1111/j.1467-8624.2006.00891.x
37. Elgar, F. J., McGrath, P. J., Waschbusch, D. A., Stewart, S. H., and Curtis, L. J. (2004). Mutual influences on maternal depression and child adjustment problems. Clin. Psychol. Rev. 24, 441-459. doi: 10.1016/j.cpr.2004.02.002
38. Ellis, B. J., Boyce, W. T., Belsky, J., and Bakermans-Kranenburg, M. J. (2011). Differential susceptibility to the environment: an evolutionary-neurodevelopmental theory. Dev. Psychopathol. 23, 7. doi: 10.1017/S0954579410000611
39. Enge, S., Fleischhauer, M., Lesch, K. P., Reif, A., and Strobel, A. (2011). Serotonergic modulation in executive functioning: linking genetic variations to working memory performance. Neuropsychologia 49, 3776-3785. doi: 10.1016/j.neuropsychologia.2011.09.038
40. Espy, K. A., Kaufmann, P. M., and Glisky, M. L. (1999). Neuropsychologic function in toddlers exposed to cocaine in utero: a preliminary study. Dev. Neuropsychol. 15, 447-460. doi: 10.1080/87565649909540761
41. Essex, M. J., Boyce, W. T., Goldstein, L. H., Armstrong, J. M., Kraemer, H. C., and Kupfer, D. J. (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood. II: developing the macarthur health and behavior questionnaire. J. Am. Acad. Child Adolesc. Psychiatry 41, 588-603. doi: 10.1097/00004583-200205000-00017
42. Essex, M. J., Kraemer, H. C., Armstrong, J. M., Boyce, W. T., Goldsmith, H. H., Klein, M. H., et al. (2006). Exploring risk factors for the emergence of children's mental health problems. Arch. Gen. Psychiatry 63, 1246-1256. doi: 10.1001/archpsyc.63.11.1246
43. Evers, E., Van der Veen, F., Jolles, J., Deutz, N., and Schmitt, J. (2006). Acute tryptophan depletion improves performance and modulates the BOLD response during a Stroop task in healthy females. Neuroimage 32, 248-255. doi: 10.1016/j.neuroimage.2006.03.026
44. Fox, S. E., Levitt, P., and Nelson, C. A. (2010). How the timing and quality of early experiences influence the development of brain architecture. Child Dev. 81, 28-40. doi: 10.1111/j.1467-8624.2009.01380.x
45. Gaspar, P., Cases, O., and Maroteaux, L. (2003). The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 4, 1002-1012. doi: 10.1038/nrn1256
46. Gathercole, S. E., Tiffany, C., Briscoe, J., and Thorn, A. (2005). Developmental consequences of poor phonological short-term memory function in childhood: a longitudinal study. J. Child Psychol. Psychiatry 46, 598-611. doi: 10.1111/j.1469-7610.2004.00379.x
47. Gelfand, D. M., and Teti, D. M. (1990). The effects of maternal depression on children. Clin. Psychol. Rev. 10, 329-353. doi: 10.1016/0272-7358(90)90065-I
48. Gizer, I. R., Ficks, C., and Waldman, I. D. (2009). Candidate gene studies of ADHD: a meta-analytic review. Hum. Genet. 126, 51-90. doi: 10.1007/s00439-009-0694-x
49. Goldman, D., Oroszi, G., and Ducci, F. (2005). The genetics of addictions: uncovering the genes. Nat. Rev. Genet. 6, 521-532. doi: 10.1038/nrg1635
50. Goodman, S. H., and Gotlib, I. H. (1999). Risk for psychopathology in the children of depressed mothers: a developmental model for understanding mechanisms of transmission. Psychol. Rev. 106, 458. doi: 10.1037/0033-295X.106.3.458
51. Gross, H. E., Shaw, D. S., Moilanen, K. L., Dishion, T. J., and Wilson, M. N. (2008). Reciprocal models of child behavior and depressive symptoms in mothers and fathers in a sample of children at risk for early conduct problems. J. Fam. 22, 742. doi: 10.1037/a0013514
52. Hamilton, M. (1960). A rating scale for depression. J. Neurol. Neurosurg. Psychiatr. 23, 56-62. doi: 10.1136/jnnp.23.1.56
53. Hanley, G. E., and Oberlander, T. F. (2012). Neurodevelopmental outcomes following prenatal exposure to serotonin reuptake inhibitor antidepressants: a "social teratogen" or moderator of developmental risk? Birth Defects Res. A 94, 651-659. doi: 10.1002/bdra.23032
54. Harmer, C. J., Bhagwagar, Z., Cowen, P. J., and Goodwin, G. M. (2002). Acute administration of citalopram facilitates memory consolidation in healthy volunteers. Psychopharmacology 163, 106-110. doi: 10.1007/s00213-002-1151-x
55. Heils, A., Teufel, A., Petri, S., Stöber, G., Riederer, P., Bengel, D., et al. (1996). Allelic variation of human serotonin transporter gene expression. J. Neurochem. 66, 2621-2624. doi: 10.1046/j.1471-4159.1996.66062621.x
56. Hensler, J. G. (2006). Serotonergic modulation of the limbic system. Neurosci. Biobehav. Rev. 30, 203-214. doi: 10.1016/j.neubiorev.2005.06.007
57. Homberg, J. R., and Lesch, K. P. (2011). Looking on the bright side of serotonin transporter gene variation. Biol. Psychiatry 69, 513-519. doi: 10.1016/j.biopsych.2010.09.024
58. Homberg, J., Olivier, J., Smits, B., Mul, J., Mudde, J., Verheul, M., et al. (2007a). Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 146, 1662-1676. doi: 10.1016/j.neuroscience.2007.03.030
59. Homberg, J. R., Pattij, T., Janssen, M. C., Ronken, E., De Boer, S. F., Schoffelmeer, A. N., et al. (2007b). Serotonin transporter deficiency in rats improves inhibitory control but not behavioural flexibility. Eur. J. Neurosci. 26, 2066-2073. doi: 10.1111/j.1460-9568.2007.05839.x
60. Homberg, J. R., Schubert, D., and Gaspar, P. (2010). New perspectives on the neurodevelopmental effects of SSRIs. Trends Pharmacol. Sci. 31, 60-65. doi: 10.1016/j.tips.2009.11.003
61. Hughes, C., Roman, G., Hart, M. J., and Ensor, R. (2013). Does maternal depression predict young children's executive function?-a 4-year longitudinal study. J. Child Psychol. Psychiatry 54, 169-177. doi: 10.1111/jcpp.12014
62. Hughes, C. H., and Ensor, R. A. (2009). How do families help or hinder the emergence of early executive function? New Dir. Child Adolesc. Dev. 2009, 35-50. doi: 10.1002/cd.234
63. Jedema, H. P., Gianaros, P. J., Greer, P. J., Kerr, D. D., Liu, S., Higley, J. D., et al. (2009). Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Mol. Psychiatry 15, 512-522. doi: 10.1038/mp.2009.90
64. Kail, R., and Salthouse, T. A. (1994). Processing speed as a mental capacity. Acta Psychol. 86, 199-225. doi: 10.1016/0001-6918(94)90003-5
65. Kalueff, A., Olivier, J., Nonkes, L., and Homberg, J. (2010). Conserved role for the serotonin transporter gene in rat and mouse neurobehavioral endophenotypes. Neurosci. Biobehav. Rev. 34, 373-386. doi: 10.1016/j.neubiorev.2009.08.003
66. Kendler, K. S., Kuhn, J. W., Vittum, J., Prescott, C. A., and Riley, B. (2005). The interaction of stressful life events and a serotonin transporter polymorphism in the prediction of episodes of major depression: a replication. Arch. Gen. Psychiatry 62, 529-535. doi: 10.1001/archpsyc.62.5.529
67. Kim, J., Riggs, K. W., Misri, S., Kent, N., Oberlander, T. F., Grunau, R. E., et al. (2006). Stereoselective disposition of fluoxetine and norfluoxetine during pregnancy and breast-feeding. Br. J. Clin. Pharmacol. 61, 155-163. doi: 10.1111/j.1365-2125.2005.02538.x
68. King, M. V., Marsden, C. A., and Fone, K. C. (2008). A role for the 5-HT1A, 5-HT 4 and 5-HT6 receptors in learning and memory. Trends Pharmacol. Sci. 29, 482-492. doi: 10.1016/j.tips.2008.07.001
69. Kolb, B., Gibb, R., and Robinson, T. E. (2003). Brain plasticity and behavior. Curr. Dir. Psychol. 12, 1-5. doi: 10.1111/1467-8721.01210
70. Laine, K., Heikkinen, T., Ekblad, U., and Kero, P. (2003). Effects of exposure to selective serotonin reuptake inhibitors during pregnancy on serotonergic symptoms in newborns and cord blood monoamine and prolactin concentrations. Arch. Gen. Psychiatry 60, 720-726. doi: 10.1001/archpsyc.60.7.720
71. Lee, L., and Lee, L. J. (2012). Neonatal fluoxetine exposure alters motor performances of adolescent rats. Dev. Neurobiol. 72, 1122-1132. doi: 10.1002/dneu.20942
72. Lemery-Chalfant, K., Schreiber, J. E., Schmidt, N. L., Van Hulle, C. A., Essex, M. J., and Goldsmith, H. (2007). Assessing internalizing, externalizing, and attention problems in young children: validation of the MacArthur HBQ. J. Am. Acad. Child Adolesc. Psychiatry 46, 1315-1323. doi: 10.1097/chi.0b013e3180f616c6
73. Lesch, K. (2007). Linking emotion to the social brain. EMBO Rep. 8, S24-S29. doi: 10.1038/sj.embor.7401008
74. Lesch, K., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531. doi: 10.1126/science.274.5292.1527
75. Lesch, K., Wolozin, B., Estler, H., Murphy, D., and Riederer, P. (1993). Isolation of a cDNA encoding the human brain serotonin transporter. J. Neural Transm. 91, 67-72. doi: 10.1007/BF01244919
76. Liao, C., and Lee, L. (2011). Neonatal fluoxetine exposure affects the action potential properties and dendritic development in cortical subplate neurons of rats. Toxicol. Lett. 207, 314-321. doi: 10.1016/j.toxlet.2011.09.028
77. Lira, A., Zhou, M., Castanon, N., Ansorge, M. S., Gordon, J. A., Francis, J. H., et al. (2003). Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol. Psychiatry 54, 960-971. doi: 10.1016/S0006-3223(03)00696-6
78. Luby, J. L., Heffelfinger, A., Measelle, J. R., Ablow, J. C., Essex, M. J., Dierker, L., et al. (2002). Differential performance of the MacArthur HBQ and DISC-IV in identifying DSM-IV internalizing psychopathology in young children. J. Am. Acad. Child Adolesc. Psychiatry 41, 458-466. doi: 10.1097/00004583-200204000-00019
79. Mannie, Z., Barnes, J., Bristow, G., Harmer, C., and Cowen, P. (2009). Memory impairment in young women at increased risk of depression: influence of cortisol and 5-HTT genotype. Psychol. Med. 39, 757-762. doi: 10.1017/S0033291708004248
80. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167-202. doi: 10.1146/annurev.neuro.24.1.167
81. Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., and Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex "frontal lobe" tasks: a latent variable analysis. Cognit. Psychol. 41, 49-100. doi: 10.1006/cogp.1999.0734
82. Moffitt, T. E., Arseneault, L., Belsky, D., Dickson, N., Hancox, R. J., Harrington, H., et al. (2011). A gradient of childhood self-control predicts health, wealth, and public safety. Proc. Natl. Acad. Sci. U.S.A. 108, 2693-2698. doi: 10.1073/pnas.1010076108
83. Moffitt, T. E., Caspi, A., and Rutter, M. (2005). Strategy for investigating interactions between measured genes and measured environments. Arch. Gen. Psychiatry 62, 473-481. doi: 10.1001/archpsyc.62.5.473
84. Moses-Kolko, E. L., Bogen, D., Perel, J., Bregar, A., Uhl, K., Levin, B., et al. (2005). Neonatal signs after late in utero exposure to serotonin reuptake inhibitors. J. Am. Med. Assoc. 293, 2372-2383. doi: 10.1001/jama.293.19.2372
85. Mulder, E. J., Ververs, F. F., de Heus, R., and Visser, G. H. (2011). Selective serotonin reuptake inhibitors affect neurobehavioral development in the human fetus. Neuropsychopharmacology 36, 1961-1971. doi: 10.1038/npp.2011.67
86. Munafò, M. R., Durrant, C., Lewis, G., and Flint, J. (2009). Gene× environment interactions at the serotonin transporter locus. Biol. Psychiatry 65, 211-219. doi: 10.1016/j.biopsych.2008.06.009
87. Nonkes, L. J., Tomson, K., and Mærtin, A. Dederen, J., Roald Maes, J., Homberg, J. (2010). Orbitofrontal cortex and amygdalar over-activity is associated with an inability to use the value of expected outcomes to guide behaviour in serotonin transporter knockout rats. Neurobiol. Learn. Mem. 94, 65-72. doi: 10.1016/j.nlm.2010.04.002
88. Nonkes, L. J., van de Vondervoort, I. I., de Leeuw, M. J., Wijlaars, L. P., Maes, J. H., and Homberg, J. R. (2012). Serotonin transporter knockout rats show improved strategy set-shifting and reduced latent inhibition. Learn. Mem. 19, 190-193. doi: 10.1101/lm.025908.112
89. Nulman, I., Rovet, J., Stewart, D. E., Wolpin, J., Pace-Asciak, P., Shuhaiber, S., et al. (2002). Child development following exposure to tricyclic antidepressants or fluoxetine throughout fetal life: a prospective, controlled study. Am. J. Psychiatry159, 1889-1895. doi: 10.1176/appi.ajp.159.11.1889
90. Oberlander, T., Gingrich, J., and Ansorge, M. (2009). Sustained neurobehavioral effects of exposure to SSRI antidepressants during development: molecular to clinical evidence. Clin. Pharmacol. Ther. 86, 672-677. doi: 10.1038/clpt.2009.201
91. Oberlander, T. F., Grunau, R. E., Fitzgerald, C., Ellwood, A. L., Misri, S., Rurak, D., et al. (2002). Prolonged prenatal psychotropic medication exposure alters neonatal acute pain response. Pediatr. Res. 51, 443-453. doi: 10.1203/00006450-200204000-00008
92. Oberlander, T. F., Grunau, R. E., Fitzgerald, C., Papsdorf, M., Rurak, D., and Riggs, W. (2005). Pain reactivity in 2-month-old infants after prenatal and postnatal selective serotonin reuptake inhibitor medication exposure. Pediatrics 115, 411-425. doi: 10.1542/peds.2004-0420
93. Oberlander, T. F., Papsdorf, M., Brain, U. M., Misri, S., Ross, C., and Grunau, R. E. (2010). Prenatal effects of selective serotonin reuptake inhibitor antidepressants, serotonin transporter promoter genotype (SLC6A4), and maternal mood on child behavior at 3 years of age. Arch. Pediatr. Adolesc. Med. 164, 444-451. doi: 10.1001/archpediatrics.2010.51
94. Olivier, J., Blom, T., Arentsen, T., and Homberg, J. (2011). The age-dependent effects of selective serotonin reuptake inhibitors in humans and rodents: a review. Prog. Neuro. Psychopharmacol. Biol. Psychiatry 35, 1400-1408. doi: 10.1016/j.pnpbp.2010.09.013
95. Owens, M., Goodyer, I. M., Wilkinson, P., Bhardwaj, A., Abbott, R., Croudace, T., et al. (2012). 5-HTTLPR and early childhood adversities moderate cognitive and emotional processing in adolescence. PLoS ONE 7:e48482. doi: 10.1371/journal.pone.0048482
96. Petrides, M. (2005). Lateral prefrontal cortex: architectonic and functional organization. Philos. Trans. R. Soc. B Biol. Sci. 360, 781-795. doi: 10.1098/rstb.2005.1631
97. Popa, D., Léna, C., Alexandre, C., and Adrien, J. (2008). Lasting syndrome of depression produced by reduction in serotonin uptake during postnatal development: evidence from sleep, stress, and behavior. J. Neurosci. 28, 3546. doi: 10.1523/JNEUROSCI.4006-07.2008
98. Preece, M., Dalley, J., Theobald, D., Robbins, T., and Reynolds, G. (2004). Region specific changes in forebrain 5-hydroxytryptamine 1a and 5-hydroxytryptamine 2a receptors in isolation-reared rats: an in vitro autoradiography study. Neuroscience123, 725-732. doi: 10.1016/j.neuroscience.2003.10.008
99. Reuter, M., Ott, U., Vaitl, D., and Hennig, J. (2007). Impaired executive control is associated with a variation in the promoter region of the tryptophan hydroxylase 2 gene. J. Cogn. Neurosci. 19, 401-408. doi: 10.1162/jocn.2007.19.3.401
100. Riedel, W. J., Eikmans, K., Heldens, A., and Schmitt, J. A. J. (2005). Specific serotonergic reuptake inhibition impairs vigilance performance acutely and after subchronic treatment. J. Psychopharmacology 19, 12-20. doi: 10.1177/0269881105048887
101. Riggs, N. R., Blair, C. B., and Greenberg, M. T. (2004). Concurrent and 2-year longitudinal relations between executive function and the behavior of 1st and 2nd grade children. Child Neuropsychol. 9, 267-276. doi: 10.1076/chin.9.4.267.23513
102. Risch, N., Herrell, R., Lehner, T., Liang, K., Eaves, L., Hoh, J., et al. (2009). Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression. J. Am. Med. Assoc. 301, 2462-2471. doi: 10.1001/jama.2009.878
103. Roiser, J. (2011). Bridging the gap between genes and behaviour: the case for neuroimaging genetics. J. Neurol. Neurosurg. Psychiatry 82, e2. doi: 10.1136/jnnp-2011-300504.24
104. Roiser, J. P., Blackwell, A. D., Cools, R., Clark, L., Rubinsztein, D. C., Robbins, T. W., et al. (2006). Serotonin transporter polymorphism mediates vulnerability to loss of incentive motivation following acute tryptophan depletion. Neuropsychopharmacology 31, 2264-2272. doi: 10.1038/sj.npp.1301084
105. Roiser, J. P., Müller, U., Clark, L., and Sahakian, B. J. (2007). The effects of acute tryptophan depletion and serotonin transporter polymorphism on emotional processing in memory and attention. Int. J. Neuropsychopharmacol. 10, 449. doi: 10.1017/S146114570600705X
106. Salisbury, A. L., Ponder, K. L., Padbury, J. F., and Lester, B. M. (2009). Fetal effects of psychoactive drugs. Clin. Perinatol. 36, 595. doi: 10.1016/j.clp.2009.06.002
107. Sasaki-Adams, D. M., and Kelley, A. E. (2001). Serotonin-dopamine interactions in the control of conditioned reinforcement and motor behavior. Neuropsychopharmacology 25, 440-452. doi: 10.1016/S0893-133X(01)00240-8
108. Schmitt, J. A., Kruizinga, M. J., and Riedel, W. J. (2001). Non-serotonergic pharmacological profiles and associated cognitive effects of serotonin reuptake inhibitors. J. Psychopharmacol. 15, 173-179. doi: 10.1177/026988110101500304
109. Schmitt, J. A. J., Jorissen, B. L., Sobczak, S., van Boxtel, M. P. J., Hogervorst, E., Deutz, N. E. P., et al. (2000). Tryptophan depletion impairs memory consolidation but improves focussed attention in healthy young volunteers. J. Psychopharmacol. 14, 21-29. doi: 10.1177/026988110001400102
110. Schmitt, J. A. J., Wingen, M., Ramaekers, J. G., Evers, E. A. T., and Riedel, W. J. (2006). Serotonin and human cognitive performance. Curr. Pharm. Des. 12, 2473-2486. doi: 10.2174/138161206777698909
111. Schonfeld, A. M., Paley, B., Frankel, F., and O'Connor, M. J. (2006). Executive functioning predicts social skills following prenatal alcohol exposure. Child Neuropsychol. 12, 439-452. doi: 10.1080/09297040600611338
112. 2-induced fear by 5-HTTLPR genotype. J. Psychopharmacol. 25, 37-42. doi: 10.1177/0269881110372543
113. Shirtcliff, E. A., and Essex, M. J. (2008). Concurrent and longitudinal associations of basal and diurnal cortisol with mental health symptoms in early adolescence. Dev. Psychobiol. 50, 690-703. doi: 10.1002/dev.20336
114. Siepmann, M., Grossmann, J., Mück-Weymann, M., and Kirch, W. (2003). Effects of sertraline on autonomic and cognitive functions in healthy volunteers. Psychopharmacology (Berl.) 168, 293-298. doi: 10.1007/s00213-003-1448-4
115. Simpson, K. L., Weaver, K. J., de Villers-Sidani, E., Lu, J. Y., Cai, Z., Pang, Y., et al. (2011). Perinatal antidepressant exposure alters cortical network function in rodents. Proc. Natl. Acad. Sci. U.S.A. 108, 18465-18470. doi: 10.1073/pnas.1109353108
116. Strobel, A., Dreisbach, G., Müller, J., Goschke, T., Brocke, B., and Lesch, K. P. (2007). Genetic variation of serotonin function and cognitive control. J. Cogn. Neurosci. 19, 1923-1931. doi: 10.1162/jocn.2007.19.12.1923
117. Taghavi, M. R., Neshat-Doost, H. T., Moradi, A. R., Yule, W., and Dalgleish, T. (1999). Biases in visual attention in children and adolescents with clinical anxiety and mixed anxiety-depression. J. Abnorm. Child Psychol. 27, 215-223. doi: 10.1023/A:1021952407074
118. Taylor, S. E., Way, B. M., Welch, W. T., Hilmert, C. J., Lehman, B. J., and Eisenberger, N. I. (2006). Early family environment, current adversity, the serotonin transporter promoter polymorphism, and depressive symptomatology. Biol. Psychiatry 60, 671-676. doi: 10.1016/j.biopsych.2006.04.019
119. Valluzzi, J. A., and Chan, K. H. (2007). Effects of fluoxetine on hippocampal-dependent and hippocampal-independent learning tasks. Behav. Pharmacol. 18, 507-513. doi: 10.1097/FBP.0b013e3282ee2a91
120. van Ijzendoorn, M. H., Belsky, J., and Bakermans-Kranenburg, M. J. (2012). Serotonin transporter genotype 5HTTLPR as a marker of differential susceptibility? A meta-analysis of child and adolescent gene-by-environment studies. Transl. Psychiatry2:e147. doi: 10.1038/tp.2012.73
121. Varnäs, K., Halldin, C., and Hall, H. (2004). Autoradiographic distribution of serotonin transporters and receptor subtypes in human brain. Hum. Brain Mapp. 22, 246-260. doi: 10.1002/hbm.20035
122. Weikum, W. M., Oberlander, T. F., Hensch, T. K., and Werker, J. F. (2012). Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception. Proc. Natl. Acad. Sci. U.S.A. 109, 17221-17227. doi: 10.1073/pnas.1121263109
123. Zanto, T. P., Rubens, M. T., Thangavel, A., and Gazzaley, A. (2011). Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat. Neurosci. 14, 656-661. doi: 10.1038/nn.2773
124. Zheng, J., Xu, D., Li, K., Wang, H., Shen, P., Lin, M., et al. (2011). Neonatal exposure to fluoxetine and fluvoxamine alteres spine density in mouse hippocampal CA1 pyramidal neurons. Int. J. Clin. Exp. Pathol. 4, 162