Interaction of the serotonin transporter-linked polymorphic region and environmental adversity: Increased amygdala-hypothalamus connectivity as a potential mechanism linking neural and endocrine hyperreactivity

Biological Psychiatry

Volumn 72, Issue 1, 2012, Pages 49-56

  Alexander, Nina ^a,b   Klucken, Tim ^b   Koppe, Georgia ^b,c   Osinsky, Roman ^d   Walter, Bertram ^b   Vaitl, Dieter ^b   Sammer, Gebhard ^b   Stark, Rudolf ^b   Hennig, Juergen ^b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

5 HTTLPR; Amygdala; functional connectivity; gene by environment interaction; stress reactivity; stressful life events

Indexed keywords

HYDROCORTISONE; SEROTONIN TRANSPORTER;

ADULT; ALLELE; AMYGDALOID NUCLEUS; ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; FEAR; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; HORMONE RELEASE; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS; LIFE EVENT; MALE; NERVE POTENTIAL; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SAMPLE; STIMULUS; STRESS;

ADULT; AMYGDALA; BRAIN MAPPING; FACIAL EXPRESSION; FEAR; GENE-ENVIRONMENT INTERACTION; HUMANS; HYDROCORTISONE; HYPOTHALAMUS; LIFE CHANGE EVENTS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; POLYMORPHISM, GENETIC; REFERENCE VALUES; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL;

EID: 84862007285     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.01.030     Document Type: Article

References (81)

1. A. Caspi, K. Sugden, T.E. Moffitt, A. Taylor, I.W. Craig, H. Harrington Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene Science 301 2003 291 293
2. B.D. Greenberg, T.J. Tolliver, S.J. Huang, Q. Li, D. Bengel, D.L. Murphy Genetic variation in the serotonin transporter promoter region affects serotonin uptake in human blood platelets Am J Med Genet 88 1999 83 87
3. K.P. Lesch, D. Bengel, A. Heils, S.Z. Sabol, B.D. Greenberg, S. Petri Association of anxiety-related traits with a polymorphismus in the serotonin transporter gene regulatory region Science 274 1996 1527 1531
4. S.F. Stoltenberg, G.R. Twitchell, G.L. Hanna, E.H. Cook, H.E. Fitzgerald, R.A. Zucker, K.Y. Little Serotonin transporter promoter polymorphism, peripheral indexes of serotonin function, and personality measures in families with alcoholism Am J Med Genet 114 2002 230 234
5. R. Uher, P. McGuffin The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: Review and methodological analysis Mol Psychiatry 13 2008 131 146
6. R. Uher, P. McGuffin The moderation by the serotonin transporter gene of environmental adversity in the etiology of depression: 2009 update Mol Psychiatry 15 2010 18 22
7. N. Risch, R. Herrell, T. Lehner, K.Y. Liang, L. Eaves, J. Hoh Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: A meta-analysis JAMA 301 2009 2462 2471
8. A. Caspi, A.R. Hariri, A. Holmes, R. Uher, T.E. Moffitt Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits Am J Psychiatry 167 2010 509 527
9. K. Karg, M. Burmeister, K. Shedden, S. Sen The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: Evidence of genetic moderation Arch Gen Psychiatry 68 2010 444 454
10. G. Hasler, W.C. Drevets, H.K. Manji, D.S. Charney Discovering endophenotypes for major depression Neuropsychopharmacology 29 2004 1765 1781
11. A. Bertolino, G. Arciero, V. Rubino, V. Latorre, M. De Candia, V. Mazzola Variation of human amygdala response during threatening stimuli as a function of 5'HTTLPR genotype and personality style Biol Psychiatry 57 2005 1517 1525
12. A.R. Hariri, V.S. Mattay, A. Tessitore, B. Kolachana, F. Fera, D. Goldman Serotonin transporter genetic variation and the response of the human amygdala Science 297 2002 400 403
13. A.R. Hariri, E.M. Drabant, K.E. Munoz, B.S. Kolachana, V.S. Mattay, M.F. Egan, D.R. Weinberger A susceptibility gene for affective disorders and the response of the human amygdala Arch Gen Psychiatry 62 2005 146 152
14. J.Y. Lau, D. Goldman, B. Buzas, S.J. Fromm, A.E. Guyer, C. Hodgkinson Amygdala function and 5-HTT gene variants in adolescent anxiety and major depressive disorder Biol Psychiatry 65 2009 349 355
15. M.R. Munafo, S.M. Brown, A.R. Hariri Serotonin transporter (5-HTTLPR) genotype and amygdala activation: A meta-analysis Biol Psychiatry 63 2007 852 857
16. T. Canli, M. Qiu, K. Omura, E. Congdon, B.W. Haas, Z. Amin Neural correlates of epigenesis Proc Natl Acad Sci U S A 103 2006 16033 16038
17. L.M. Williams, J.M. Gatt, P.R. Schofield, G. Olivieri, A. Peduto, E. Gordon 'Negativity bias' in risk for depression and anxiety: Brain-body fear circuitry correlates, 5-HTTLPR and early life stress Neuroimage 47 2009 804 814
18. D. Armbruster, D. Moser, A. Strobel, T. Hensch, C. Kirschbaum, K.P. Lesch, B. Brocke Serotonin transporter gene variation and stressful life events impact processing of fear and anxiety Int J Neuropsychopharmacol 12 2009 393 401
19. C.S. Barr, T.K. Newman, M. Schwandt, C. Shannon, R.L. Dvoskin, S.G. Lindell Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques Proc Natl Acad Sci U S A 101 2004 12358 12363
20. K. McCormack, T.K. Newman, J.D. Higley, D. Maestripieri, M.M. Sanchez Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants Horm Behav 55 2009 538 547
21. N. Alexander, Y. Kuepper, A. Schmitz, R. Osinsky, E. Kozyra, J. Hennig Gene-environment interactions predict cortisol responses after acute stress: Implications for the etiology of depression Psychoneuroendocrinology 34 2009 1294 1303
22. A. Mueller, D. Armbruster, D.A. Moser, T. Canli, K.P. Lesch, B. Brocke, C. Kirschbaum Interaction of serotonin transporter gene-linked polymorphic region and stressful life events predicts cortisol stress response Neuropsychopharmacology 36 2011 1332 1339
23. J.P. Herman, M.M. Ostrander, N.K. Mueller, H. Figueiredo Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis Prog Neuropsychopharmacol Biol Psychiatry 29 2005 1201 1213
24. R. Jankord, J.P. Herman Limbic regulation of hypothalamo-pituitary- adrenocortical function during acute and chronic stress Ann N Y Acad Sci 1148 2008 64 73
25. T. Canli, K.P. Lesch Long story short: The serotonin transporter in emotion regulation and social cognition Nat Neurosci 10 2007 1103 1109
26. J. Margraf Mini-DIPS: Diagnostisches Kurz-Interview bei psychischen Störungen 1994 Springer-Verlag Berlin
27. M. Hautzinger, M. Bailer, H. Worall, F. Keller Beck Depression Inventory (BDI) 1994 Huber Bern Switzerland
28. M. Nakamura, S. Ueno, A. Sano, H. Tanabe The human serotonin transporter gene linked polymorphism (5-HTTLPR) shows ten novel allelic variants Mol Psychiatry 5 2000 32 38
29. X. Hu, R.H. Lipsky, G. Zhu, L.A. Akhtar, J. Taubman, B.D. Greenberg Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder Am J Hum Genet 78 2006 815 826
30. L.R. Dougherty, D.N. Klein, E. Congdon, T. Canli, E.P. Hayden Interaction between 5-HTTLPR and BDNF Val66Met polymorphisms on HPA axis reactivity in preschoolers Biol Psychol 83 2010 93 100
31. I.H. Gotlib, J. Joormann, K.L. Minor, J. Hallmayer HPA axis reactivity: A mechanism underlying the associations among 5-HTTLPR, stress, and depression Biol Psychiatry 63 2008 847 851
32. A. Mueller, B. Brocke, E. Fries, K.P. Lesch, C. Kirschbaum The role of the serotonin transporter polymorphism for the endocrine stress response in newborns Psychoneuroendocrinology 35 2010 289 296
33. B.M. Way, S.E. Taylor The serotonin transporter promoter polymorphism is associated with cortisol response to psychosocial stress Biol Psychiatry 67 2010 487 492
34. M.J. Gray, B.T. Litz, J.L. Hsu, T.W. Lombardo Psychometric properties of the life events checklist Assessment 11 2004 330 341
35. D. Lundqvist, J.E. Litton The Karolinska Directed Faces 1998 Karolinska Institute Stockholm
36. T. Klucken, S. Kagerer, J. Schweckendiek, K. Tabbert, D. Vaitl, R. Stark Neural, electrodermal and behavioral response patterns in contingency aware and unaware subjects during a picture-picture conditioning paradigm Neuroscience 158 2009 721 731
37. T. Klucken, J. Schweckendiek, C.J. Merz, K. Tabbert, B. Walter, S. Kagerer Neural activations of the acquisition of conditioned sexual arousal: Effects of contingency awareness and sex J Sex Med 6 2009 3071 3085
38. T. Klucken, J. Schweckendiek, G. Koppe, C.J. Merz, S. Kagerer, B. Walter Neural correlates of disgust- and fear-conditioned responses Neuroscience 201 2012 209 218
39. C. Esslinger, H. Walter, P. Kirsch, S. Erk, K. Schnell, C. Arnold Neural mechanisms of a genome-wide supported psychosis variant Science 324 2009 605
40. M.R. Delgado, K.I. Nearing, J.E. Ledoux, E.A. Phelps Neural circuitry underlying the regulation of conditioned fear and its relation to extinction Neuron 59 2008 829 838
41. C. Lemogne, P. Gorwood, C. Boni, M. Pessiglione, S. Lehéricy, P. Fossati Cognitive appraisal and life stress moderate the effects of the 5-HTTLPR polymorphism on amygdala reactivity Hum Brain Mapp 32 2011 1856 1867
42. S.A. Surguladze, A. Elkin, C. Ecker, S. Kalidindi, A. Corsico, V. Giampietro Genetic variation in the serotonin transporter modulates neural system-wide response to fearful faces Genes Brain Behav 7 2008 543 551
43. K. Vytal, S. Hamann Neuroimaging support for discrete neural correlates of basic emotions: A voxel-based meta-analysis J Cogn Neurosci 22 2010 2864 2885
44. A. Ohman, K. Carlsson, D. Lundqvist, M. Ingvar On the unconscious subcortical origin of human fear Physiol Behav 92 2007 180 185
45. A.J. Pegna, A. Khateb, F. Lazeyras, M.L. Seghier Discriminating emotional faces without primary visual cortices involves the right amygdala Nat Neurosci 8 2005 24 25
46. T.B. Lonsdorf, A. Golkar, K.M. Lindstöm, P. Fransson, M. Schalling, A. Ohman, M. Ingvar 5-HTTLPR and COMTval158met genotype gate amygdala reactivity and habituation Biol Psychol 87 2011 106 112
47. H. Scherk, O. Gruber, P. Menzel, T. Schneider-Axmann, C. Kemmer, J. Usher 5-HTTLPR genotype influences amygdala volume Eur Arch Psychiatry Clin Neurosci 259 2009 212 217
48. J.C. Root, O. Tuescher, A. Cunningham-Bussel, H. Pan, J. Epstein, M. Altemus Frontolimbic function and cortisol reactivity in response to emotional stimuli Neuroreport 20 2009 429 434
49. A. Meyer-Lindenberg Neural connectivity as an intermediate phenotype: Brain networks under genetic control Hum Brain Mapp 30 2009 1938 1946
50. K. Amunts, O. Kedo, M. Kindler, P. Pieperhoff, H. Mohlberg, N.J. Shah Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps Anat Embryol (Berl) 210 2005 343 352
51. S.B. Eickhoff, K.E. Stephan, H. Mohlberg, C. Grefkes, G.R. Fink, K. Amunts, K. Zilles A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data Neuroimage 4 2005 1325 1335
52. S.B. Eickhoff, S. Heim, K. Zilles, K. Amunts Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps Neuroimage 32 2006 570 582
53. B. Walter, C. Blecker, P. Kirsch, G. Sammer, A. Schienle, R. Stark et al. MARINA: An easy to use tool for the creation of Masks for Region of Interest Analyses Presented at the 9th International Conference on Human Brain Mapping; June 19-22, 2003; New York, NY Neuroimage 19 2003 [serial on CD-ROM]
54. N. Tzourio-Mazoyer, B. Landeau, D. Papathanassiou, F. Crivello, O. Etard, N. Delcroix Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain Neuroimage 15 2002 273 289
55. T. Canli, K. Omura, B.W. Haas, A. Fallgatter, R.T. Constable, K.P. Lesch 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 2005 12224 12229
56. E.A. von dem Hagen, L. Passamonti, S. Nutland, J. Sambrook, A.J. Calder The serotonin transporter gene polymorphism and the effect of baseline on amygdala response to emotional faces Neuropsychologia 49 2011 674 680
57. N.H. Kalin, S.E. Shelton, A.S. Fox, J. Rogers, T.R. Oakes, R.J. Davidson The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor Mol Psychiatry 13 2008 1021 1027
58. H. Rao, S.J. Gillihan, J. Wang, M. Korczykowski, G.M. Sankoorikal, K.A. Kaercher Genetic variation in serotonin transporter alters resting brain function in healthy individuals Biol Psychiatry 62 2007 600 606
59. H. Brockmann, A. Zobel, A. Schuhmacher, M. Daamen, A. Joe, K. Biermann Influence of 5-HTTLPR polymorphism on resting state perfusion in patients with major depression J Psychiatr Res 45 2011 442 451
60. R. Viviani, E.J. Sim, H. Lo, P. Beschoner, N. Osterfeld, C. Maier Baseline brain perfusion and the serotonin transporter promoter polymorphism Biol Psychiatry 67 2010 317 322
61. S.J. Gilbert, J.S. Simons, C.D. Frith, P.W. Burgess Performance-related activity in medial rostral prefrontal cortex (area 10) during low-demand tasks J Exp Psychol Hum Percept Perform 32 2006 45 48
62. M.E. Raichle, A.M. MacLeod, A.Z. Snyder, W.J. Powers, D.A. Gusnard, G.L. Shulman A default mode of brain function Proc Natl Acad Sci U S A 98 2001 676 682
63. M. Davis, P.J. Whalen The amygdala: Vigilance and emotion Mol Psychiatry 6 2001 13 34
64. I.I. Gottesman, T.D. Gould The endophenotype concept in psychiatry: Etymology and strategic intentions Am J Psychiatry 160 2003 636 645
65. T. Johnstone, L.H. Somerville, A.L. Alexander, T.R. Oakes, R.J. Davidson, N.H. Kalin, P.J. Whalen Stability of amygdala BOLD response to fearful faces over multiple scan sessions Neuroimage 25 2005 1112 1123
66. S.B. Manuck, S.M. Brown, E.E. Forbes, A.R. Hariri Temporal stability of individual differences in amygdala reactivity Am J Psychiatry 146 2007 1613 1634
67. A. Anand, Y. Li, Y. Wang, J. Wu, S. Gao, L. Bukhari Activity and connectivity of brain mood regulating circuit in depression: A functional magnetic resonance study Biol Psychiatry 57 2005 1079 1788
68. C.H. Fu, S.C. Williams, A.J. Cleare, M.J. Brammer, N.D. Walsh, J. Kim Attenuation of the neural response to sad faces in major depression by antidepressant treatment: A prospective, event-related functional magnetic resonance imaging study Arch Gen Psychiatry 61 2004 877 889
69. Y.I. Sheline, D.M. Barch, J.M. Donnelly, J.M. Ollinger, A.Z. Snyder, M.A. Mintun Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: An fMRI study Biol Psychiatry 50 2001 651 658
70. C.S. Monk, R.G. Klein, E.H. Telzer, E.A. Schroth, S. Mannuzza, J.L. Moulton 3rd Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression Am J Psychiatry 165 2008 90 98
71. F.M. van der Veen, E.A.T. Evers, N.E.P. Deutz, J.A.J. Schmitt Effects of acute tryptophan depletion on mood and facial emotion perception related brain activation and performance in healthy women with and without a family history of depression Neuropsychopharmacology 32 2007 216 224
72. S.W. Chan, R. Norbury, G.M. Goodwin, C.J. Harmer Risk for depression and neural responses to fearful facial expressions of emotion Br J Psychiatry 194 2009 139 145
73. R. Admon, G. Lubin, O. Stern, K. Rosenberg, L. Sela, H. Ben-Ami, T. Hendler Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity Proc Natl Acad Sci U S A 106 2009 14120 14125
74. F. Lederbogen, P. Kirsch, L. Haddad, F. Streit, H. Tost, P. Schuch City living and urban upbringing affect neural social stress processing in humans Nature 474 2011 498 501
75. J.C. Pruessner, K. Dedovic, N. Khalili-Mahani, V. Engert, M. Pruessner, C. Buss Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies Biol Psychiatry 63 2008 234 240
76. E.S. Redgate, E.E. Fahringer A comparison of the pituitary adrenal activity elicited by electrical stimulation of preoptic, amygdaloid and hypothalamic sites in the rat brain Neuroendocrinology 12 1973 334 343
77. J.W. Mason Plasma 17-hydroxycorticosteroid levels during electrical stimulation of the amygdaloid complex in conscious monkeys Am J Physiol 196 1959 44 48
78. B.B. Gallagher, H.F. Flanigin, D.W. King, W.H. Littleton The effect of electrical stimulation of medial temporal lobe structures in epileptic patients upon ACTH, prolactin, and growth hormone Neurology 37 1987 299 303
79. N.I. Eisenberger, S.E. Taylor, S.L. Gable, C.J. Hilmert, M.D. Lieberman Neural pathways link social support to attenuated neuroendocrine stress responses Neuroimage 35 2007 1601 1612
80. E.S. Brown, D.J. Woolston, A.B. Frol Amygdala volume in patients receiving chronic corticosteroid therapy Biol Psychiatry 63 2008 705 709
81. E. Goeleven, R. De Raedt, L. Leyman, B. Verschuere The Karolinska Directed Emotional Faces: A validation study Cogn Emot 22 2008 1094 1118