Resting-state cerebral blood flow in amygdala is modulated by sex and serotonin transporter genotype

NeuroImage

Volumn 76, Issue , 2013, Pages 90-97

  El Hage, W ^a,b   Zelaya, F ^b   Radua, J ^b,c   Gohier, B ^d   Alsop, D C ^e   Phillips, M L ^f,g   Surguladze, S A ^b,h  

^a UNIVERSITÉ DE TOURS   (France)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

^d ANGERS UNIVERSITY HOSPITAL   (France)

^e HARVARD MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF PITTSBURGH   (United States)

^g CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^h ILIA STATE UNIVERSITY   (Georgia)

Author keywords

Affective disorders; Amygdala; Brain perfusion; Gender; Serotonin transporter

Indexed keywords

DNA; SEROTONIN TRANSPORTER;

ADULT; ALLELE; AMYGDALOID NUCLEUS; ARTICLE; BOLD SIGNAL; BRAIN BLOOD FLOW; CAUCASIAN; CONTROLLED STUDY; DNA EXTRACTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENOTYPE; GRAY MATTER; HOMOZYGOTE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SEX DIFFERENCE; SPIN LABELING;

ADULT; AMYGDALA; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; FEMALE; GENOTYPE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PERSONALITY; POLYMORPHISM, SINGLE NUCLEOTIDE; REST; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SEX CHARACTERISTICS; YOUNG ADULT;

EID: 84876309327     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.03.003     Document Type: Article

References (72)

1. Abercrombie H.C., Schaefer S.M., Larson C.L., Oakes T.R., Lindgren K.A., Holden J.E., Perlman S.B., Turski P.A., Krahn D.D., Benca R.M., Davidson R.J. Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport 1998, 9:3301-3307.
2. Alexander N., Klucken T., Koppe G., Osinsky R., Walter B., Vaitl D., Sammer G., Stark R., Hennig J. Interaction of the serotonin transporter-linked polymorphic region and environmental adversity: increased amygdala-hypothalamus connectivity as a potential mechanism linking neural and endocrine hyperreactivity. Biol. Psychiatry 2012, 72:49-56.
3. Anand A., Shekhar A. Brain imaging studies in mood and anxiety disorders. Ann. N. Y. Acad. Sci. 2003, 985:370-388.
4. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
5. Beck A.T., Steer R.A., Brown G.K. Beck Depression Inventory - Second Edition Manual 1986, Psychological Corporation, Harcourt, Brace, San Antonio, TX.
6. Bertolino A., Arciero G., Rubino V., Latorre V., De Candia M., Mazzola V., Blasi G., Caforio G., Hariri A., Kolachana B., Nardini M., Weinberger D.R., Scarabino T. Variation of human amygdala response during threatening stimuli as a function of 5'HTTLPR genotype and personality style. Biol. Psychiatry 2005, 57:1517-1525.
7. Brockmann H., Zobel A., Schuhmacher A., Daamen M., Joe A., Biermann K., Schwab S.G., Biersack H.J., Maier W., Boecker H. Influence of 5-HTTLPR polymorphism on resting state perfusion in patients with major depression. J. Psychiatr. Res. 2011, 45:442-451.
8. Brummett B., Boyle S., Siegler I., Kuhn C., Ashley-Koch A., Jonassaint C., Züchner S., Collins A., Williams R. Effects of environmental stress and gender on associations among symptoms of depression and the serotonin transporter gene linked polymorphic region (5-HTTLPR). Behav. Genet. 2008, 38:34-43.
9. Burton L.A., Rabin L., Wyatt G., Frohlich J., Vardy S.B., Dimitri D. Priming effects for affective vs. neutral faces. Brain Cogn. 2005, 59:322-329.
10. Buxton R.B., Uludag K., Dubowitz D.J., Liu T.T. Modeling the hemodynamic response to brain activation. Neuroimage 2004, 23(Supplement 1):S220-S233.
11. Canli T., Omura K., Haas B.W., Fallgatter A., Constable R.T., Lesch K.P. 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. 2005, 102:12224-12229.
12. Canli T., Qiu M., Omura K., Congdon E., Haas B.W., Amin Z. Neural correlates of epigenesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16033-16038.
13. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClay J., Mill J., Martin J., Braithwaite A., Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
14. Cloninger C.R., Przybeck T.R., Svrakic D.M., Wetzel R.D. The temperament and character inventory (TCI). A guide to its development and use 1994, Center for Psychobiology and Personality, Washington University, St Louis, MO.
15. Collignon O., Girard S., Gosselin F., Saint-Amour D., Lepore F., Lassonde M. Women process multisensory emotion expressions more efficiently than men. Neuropsychologia 2010, 48:220-225.
16. Dai W., Garcia D., de Bazelaire C., Alsop D.C. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn. Reson. Med. 2008, 60:1488-1497.
17. Davidson R.J., Pizzagalli D., Nitschke J.B., Putnam K. Depression: perspectives from affective neuroscience. Annu. Rev. Psychol. 2002, 53:545-574.
18. Domes G., Schulze L., Böttger M., Grossmann A., Hauenstein K., Wirtz P.H., Heinrichs M., Herpertz S.C. The neural correlates of sex differences in emotional reactivity and emotion regulation. Hum. Brain Mapp. 2010, 31:758-769.
19. Drevets W.C. Neuroimaging abnormalities in the amygdala in mood disorders. Ann. N. Y. Acad. Sci. 2003, 985:420-444.
20. Drevets W.C., Videen T.O., Price J.L., Preskorn S.H., Carmichael S.T., Raichle M.E. A functional anatomical study of unipolar depression. J. Neurosci. 1992, 12:3628-3641.
21. El-Hage W., Powell J.F., Surguladze S.A. Vulnerability to depression: What is the role of stress genes in gene×environment interaction?. Psychol. Med. 2009, 39:1407-1411.
22. Eysenck H.J., Eysenck S.B.G. Manual of the Eysenck personality scales 1991, Hodder and Stoughton, London.
23. First M.B., Gibbon M., Spitzer R.L., Williams J.B.W. SCID DSM-IV-TR axis 1 disorders 2001, (New York). Biometrics Research (Ed.).
24. Folstein M.F., Folstein S.E., McHugh P.R. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12(3):189-198.
25. Freeman B., Smith N., Curtis C., Huckett L., Mill J., Craig I.W. DNA from buccal swabs recruited by mail: evaluation of storage effects on long-term stability and suitability for multiplex polymerase chain reaction genotyping. Behav. Genet. 2003, 33:67-72.
26. Gillihan S.J., Rao H., Wang J., Detre J.A., Breland J., Sankoorikal G.M., Brodkin E.S., Farah M.J. Serotonin transporter genotype modulates amygdala activity during mood regulation. Soc. Cogn. Affect. Neurosci. 2010, 5:1-10.
27. Gillihan S.J., Rao H., Brennan L., Wang D.J.J., Detre J.A., Sankoorikal G.M., Brodkin E.S., Farah M.J. Serotonin transporter genotype modulates the association between depressive symptoms and amygdala activity among psychiatrically healthy adults. Psychiatry Res. 2011, 193:161-167.
28. Gohier B., Senior C., Brittain P.J., Lounes N., El-Hage W., Law V., Phillips M.L., Surguladze S.A. Gender differences in the sensitivity to negative stimuli: cross-modal affective priming study. Eur. Psychiatry 2013, 28(2):74-80.
29. Goldberg D.P., Hillier V.F. A scale version of the general health questionnaire. Psychol. Med. 1979, 9:139-145.
30. Goldstein J.M., Seidman L.J., Horton N.J., Makris N., Kennedy D.N., Caviness V.S., Faraone S.V., Tsuang M.T. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb. Cortex 2001, 11:490-497.
31. Gray N.S., Pickering A.D., Gray J.A. Psychoticism and dopamine D2 binding in the basal ganglia using single photon emission tomography. Pers. Individ. Differ. 1994, 17:431-434.
32. Gur R.C., Mozley L.H., Mozley P.D., Resnick S.M., Karp J.S., Alavi A., Arnold S.E., Gur R.E. Sex differences in regional cerebral glucose metabolism during a resting state. Science 1995, 267:528-531.
33. Haier R.J., Sokolski K., Katz M., Buchsbaum M.S. The study of personality with positron emission tomography. Personality Dimensions and Arousal 1987, 251-267. Plenum Press, New York. J. Strelau, H.J. Eysenck (Eds.).
34. Hamann S. Sex differences in the responses of the human amygdala. Neuroscientist 2005, 11:288-293.
35. Hariri A.R., Mattay V.S., Tessitore A., Kolachana B., Fera F., Goldman D., Egan M.F., Weinberger D.R. Serotonin transporter genetic variation and the response of the human amygdala. Science 2002, 297:400-403.
36. Hariri A.R., Drabant E.M., Munoz K.E., Kolachana B.S., Mattay V.S., Egan M.F., Weinberger D.R. A susceptibility gene for affective disorders and the response of the human amygdala. Arch. Gen. Psychiatry 2005, 62:146-152.
37. He Q., Xue G., Chen C., Lu Z., Dong Q., Lei X., Ding N., Li J., Li H., Chen C., Li J., Moyzis R.K., Bechara A. Serotonin transporter gene-linked polymorphic region (5-HTTLPR) influences decision making under ambiguity and risk in a large Chinese sample. Neuropharmacology 2010, 59:518-526.
38. Heils A., Teufel A., Petri S., Stober G., Riederer P., Bengel D. Allelic variation of human serotonin transporter gene expression. J. Neurochem. 1996, 66:2621-2624.
39. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:1201-1213.
40. Hu X.Z., Lipsky R.H., Zhu G., Akhtar L.A., Taubman J., Greenberg B.D., Xu K., Arnold P.D., Richter M.A., Kennedy J.L., Murphy D.L., Goldman D. Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. Am. J. Hum. Genet. 2006, 78:815-826.
41. Josephs R.A., Telch M.J., Hixon J.G., Evans J.J., Lee H., Knopik V.S., McGeary J.E., Hariri A.R., Beevers C.G. Genetic and hormonal sensitivity to threat: testing a serotonin transporter genotype×testosterone interaction. Psychoneuroendocrinology 2012, 37:752-761.
42. Jovanovic H., Lundberg J., Karlsson P., Cerin A., Saijo T., Varrone A., Halldin C., Nordström A.L. Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. Neuroimage 2008, 39:1408-1419.
43. Juruena M.F., Cleare A.J., Papadopoulos A.S., Poon L., Lightman S., Pariante C.M. Different responses to dexamethasone and prednisolone in the same depressed patients. Psychopharmacology 2006, 189:225-235.
44. Kendler K.S., Kuhn J.W., Vittum J., Prescott C.A., Riley B. The interaction of stressful life events and a serotonin transporter polymorphism in the prediction of episodes of major depression: a replication. Arch. Gen. Psychiatry 2005, 62:529-535.
45. Klein S., Smolka M.N., Wrase J., Gruesser S.M., Mann K., Braus D.F., Heinz A. The influence of gender and emotional valence of visual cues on fMRI activation in humans. Pharmacopsychiatry 2003, 36:191-194.
46. Lesch K.P., Bengel D., Heils A., Sabol S.Z., Greenberg B.D., Petri S., Benjamin J., Muller C.R., Hamer D.H., Murphy D.L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
47. Li Y., Qin W., Jiang T., Zhang Y., Yu C. Sex-dependent correlations between the personality dimension of harm avoidance and the resting-state functional connectivity of amygdala subregions. PLoS One 2012, 7:e35925.
48. Lu H., Yezhuvath U.S., Xiao G. Improving fMRI sensitivity by normalization of basal physiologic state. Hum. Brain Mapp. 2010, 31:80-87.
49. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
50. Munafo M.R., Brown S.M., Hariri A.R. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol. Psychiatry 2008, 63:852-857.
51. Nelson H.E. The National Adult Reading Test Manual 1982, NFER-Nelson, Windsor, UK.
52. O'Gorman R.L., Kumari V., Williams S.C., Zelaya F.O., Connor S.E., Alsop D.C., Gray J.A. Personality factors correlate with regional cerebral perfusion. Neuroimage 2006, 31:489-495.
53. Olsson A., Phelps E.A. Social learning of fear. Nat. Neurosci. 2007, 10:1095-1102.
54. Parkes L.M., Rashid W., Chard D.T., Tofts P.S. Normal cerebral perfusion measurements using arterial spin labeling: reproducibility, stability, and age and gender effects. Magn. Reson. Med. 2004, 51:736-743.
55. Parsey R.V., Hastings R.S., Oquendo M.A., Hu X., Goldman D., Huang Y.Y., Simpson N., Arcement J., Huang Y., Ogden R.T., Van Heertum R.L., Arango V., Mann J.J. Effect of a triallelic functional polymorphism of the serotonin-transporter-linked promoter region on expression of serotonin transporter in the human brain. Am. J. Psychiatry 2006, 163:48-51.
56. Perthen J.E., Lansing A.E., Liau J., Liu T.T., Buxton R.B. Caffeine-induced uncoupling of cerebral blood flow and oxygen metabolism: a calibrated BOLD fMRI study. Neuroimage 2008, 40:237-247.
57. Phan K.L., Wager T.D., Taylor S.F., Liberzon I. Functional neuroimaging studies of human emotions. CNS Spectr. 2004, 9:258-266.
58. Quidé Y., Witteveen A.B., El-Hage W., Veltman D.J., Olff M. Differences between effects of psychological versus pharmacological treatments on functional and morphological brain alterations in anxiety disorders and major depressive disorder: a systematic review. Neurosci. Biobehav. Rev. 2012, 36:626-644.
59. Rao H., Gillihan S.J., Wang J., Korczykowski M., Sankoorikal G.M., Kaercher K.A., Brodkin E.S., Detre J.A., Farah M.J. Genetic variation in serotonin transporter alters resting brain function in healthy individuals. Biol. Psychiatry 2007, 62:600-606.
60. Scharinger C., Rabl U., Sitte H.H., Pezawas L. Imaging genetics of mood disorders. Neuroimage 2010, 53:810-821.
61. Spielberger C.D., Gorsuch R.L., Lushene R.E. Manual for the State-trait Anxiety Inventory (Self-evaluation Questionnaire) 1970, Consultant Psychologists Press, Palo Alto, CA.
62. Surguladze S.A., Elkin A., Ecker C., Kalidindi S., Corsico A., Giampietro V., Lawrence N., Deeley Q., Murphy D.G.M., Kucharska-Pietura K., Russell T.A., McGuffin P., Murray R., Phillips M.L. Genetic variation in the serotonin transporter modulates neural system-wide response to fearful faces. Genes Brain Behav. 2008, 7:543-551.
63. Surguladze S.A., Marshall N., Schulze K., Hall M.H., Walshe M., Bramon E., Phillips M.L., Murray R.M., McDonald C. Exaggerated neural response to emotional faces in patients with bipolar disorder and their first-degree relatives. Neuroimage 2010, 53:58-64.
64. Surguladze S.A., Radua J., El-Hage W., Gohier B., Sato J.R., Kronhaus D.M., Proitsi P., Powell J., Phillips M.L. Interaction of catechol O-methyltransferase and serotonin transporter genes modulates effective connectivity in a facial emotion-processing circuitry. Transl. Psychiatry. 2012, 2:e70.
65. Tottenham N., Tanaka J.W., Leon A.C., McCarry T., Nurse M., Hare T.A., Marcus D.J., Westerlund A., Casey B.J., Nelson C. The NimStim set of facial expressions: judgments from untrained research participants 2009, 168:242-249. (ed).
66. Van de Velde S., Bracke P., Levecque K. Gender differences in depression in 23 european countries. Cross-national variation in the gender gap in depression. Soc. Sci. Med. 2010, 71:305-313.
67. Viviani R., Sim E.J., Lo H., Beschoner P., Osterfeld N., Maier C., Seeringer A., Godoy A.L., Rosa A., Comas D., Kirchheiner J. Baseline brain perfusion and the serotonin transporter promoter polymorphism. Biol. Psychiatry 2010, 67:317-322.
68. von dem Hagen E.A.H., Passamonti L., Nutland S., Sambrook J., Calder A.J. The serotonin transporter gene polymorphism and the effect of baseline on amygdala response to emotional faces. Neuropsychologia 2011, 49:674-680.
69. Wankerl M., Zyriax B.C., Bondy B., Hinkelmann K., Windler E., Otte C. Serotonin transporter gene-linked polymorphic region (5-HTTLPR) and diurnal cortisol: a sex by genotype interaction. Biol. Psychol. 2010, 85:344-346.
70. Weidenfeld J., Newman M.E., Itzik A., Gur E., Feldman S. The amygdala regulates the pituitary-adrenocortical response and release of hypothalamic serotonin following electrical stimulation of the dorsal raphe nucleus in the rat. Neuroendocrinology 2002, 76:63-69.
71. Whalen P.J. Fear, vigilance, and ambiguity. Curr. Dir. Psychol. Sci. 1998, 7:177-188.
72. Wrase J., Klein S., Gruesser S.M., Hermann D., Flor H., Mann K., Braus D.F., Heinz A. Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study. Neurosci. Lett. 2003, 348:41-45.