Interaction of catechol O-methyltransferase and serotonin transporter genes modulates effective connectivity in a facial emotion-processing circuitry

Translational Psychiatry

Volumn 2, Issue , 2012, Pages

  Surguladze, S A ^a,b   Radua, J ^a,c   El Hage, W ^a,d   Gohier, B ^e   Sato, J R ^f   Kronhaus, D M ^g   Proitsi, P ^a   Powell, J ^a   Phillips, M L ^h,i  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Cygnet Health Care   (United Kingdom)

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

^d UNIVERSITÉ DE TOURS   (France)

^e ANGERS UNIVERSITY HOSPITAL   (France)

^f UNIVERSIDADE FEDERAL DO ABC   (Brazil)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

ⁱ CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

5 HTTLPR; COMT; effective connectivity; facial emotion processing

Indexed keywords

CATECHOL METHYLTRANSFERASE; OXYGEN; SEROTONIN TRANSPORTER; SLC6A4 PROTEIN, HUMAN;

ADULT; ALLELE; AMYGDALOID NUCLEUS; ARTICLE; BLOOD; COMPUTER ASSISTED DIAGNOSIS; DEPRESSION; EMOTION; FACIAL EXPRESSION; FEAR; FEMALE; FRONTAL LOBE; GENETIC EPISTASIS; GENETIC MARKER; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; HEMISPHERIC DOMINANCE; HUMAN; LIMBIC SYSTEM; MALE; MIDDLE AGED; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL LOBE; PATHOPHYSIOLOGY; PATTERN RECOGNITION; PHYSIOLOGY; PREFRONTAL CORTEX; RISK FACTOR; TEMPORAL LOBE; VASCULARIZATION;

ADULT; ALLELES; AMYGDALA; CATECHOL O-METHYLTRANSFERASE; DEPRESSIVE DISORDER; DOMINANCE, CEREBRAL; EMOTIONS; EPISTASIS, GENETIC; FACIAL EXPRESSION; FEAR; FEMALE; FRONTAL LOBE; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; OCCIPITAL LOBE; OXYGEN; PATTERN RECOGNITION, VISUAL; PREFRONTAL CORTEX; RISK FACTORS; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TEMPORAL LOBE; YOUNG ADULT;

EID: 84856256363     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2011.69     Document Type: Article

References (71)

1. Meyer-Lindenberg A, Weinberger DR. Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev Neurosci 2006; 7: 818-827. (Pubitemid 44435264)
2. Scharinger C, Rabl U, Sitte HH, Pezawas L. Imaging genetics of mood disorders. Neuroimage 2010; 53: 810-821.
3. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D et al. Serotonin transporter genetic variation and the response of the human amygdala. Science 2002; 297: 400-403. (Pubitemid 34790769)
4. Smolka MN, Schumann G, Wrase J, Grüsser SM, Flor H, Mann K et al. Catechol-Omethyltransferase val158met genotype affects processing of emotional stimuli in the amygdala and prefrontal cortex. J Neurosci 2005; 25: 836-842. (Pubitemid 40170998)
5. Drabant EM, Hariri AR, Meyer-Lindenberg A, Munoz KE, Mattay VS, Kolachana BS et al. Catechol O-methyltransferase val158met genotype and neural mechanisms related to affective arousal and regulation. Arch Gen Psychiatry 2006; 63: 1396-1406. (Pubitemid 44878523)
6. Williams LM, Gatt JM, Grieve SM, Dobson-Stone C, Paul RH, Gordon E et al. COMT Val108/158Met polymorphism effects on emotional brain function and negativity bias. Neuroimage 2010; 53: 918-925.
7. Papaleo F, Crawley JN, Song J, Lipska BK, Pickel J, Weinberger DR et al. Genetic dissection of the role of catechol-O-methyltransferase in cognition and stress reactivity in mice. J Neurosci 2008; 28: 8709-8723.
8. Lopez-Leon S, Janssens ACJW, Gonzalez-Zuloeta Ladd AM, Del-Favero J, Claes SJ, Oostra BA et al. Meta-analyses of genetic studies on major depressive disorder. Mol Psychiatry 2007; 13: 772-785.
9. Grigorenko EL. Epistasis and the genetics of complex traits. In: Plomin R, DeFries J, Craig IW, McGuffin P (eds). Behavioral Genetics in the Postgenomic Era. American Psychological Association: Washington, DC, USA, 2003, pp 247-266.
10. Opmeer EM, Kortekaas R, Aleman A. Depression and the role of genes involved in dopamine metabolism and signalling. Prog Neurobiol 2010; 92: 112-133.
11. Mandelli L, Serretti A, Marino E, Pirovano A, Calati R, Colombo C. Interaction between serotonin transporter gene, catechol-O-methyltransferase gene and stressful life events in mood disorders. Int J Neuropsychopharmacol 2007; 10: 437-447. (Pubitemid 46985252)
12. Smolka MN, Buhler M, Schumann G, Klein S, Hu XZ, Moayer M et al. Gene-gene effects on central processing of aversive stimuli. Mol Psychiatry 2007; 12: 307-317. (Pubitemid 46328512)
13. Meyer-Lindenberg A. Neural connectivity as an intermediate phenotype: brain networks under genetic control. Hum Brain Mapp 2009; 30: 1938-1946.
14. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 2005; 8: 828-834. (Pubitemid 43085851)
15. Jacques P, Dolcos F, Cabeza R. Effects of aging on functional connectivity of the amygdala during negative evaluation: A network analysis of fMRI data. Neurobiol Aging 2010; 31: 315-327.
16. Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L et al. Activity and connectivity of brain mood regulating circuit in depression: A functional magnetic resonance study. Biol Psychiatry 2005; 57: 1079-1088. (Pubitemid 40615768)
17. Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ. Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci 2007; 27: 8877-8884. (Pubitemid 47292771)
18. Chen CH, Suckling J, Ooi C, Fu CH, Williams SC, Walsh ND et al. Functional coupling of the amygdala in depressed patients treated with antidepressant medication. Neuropsychopharmacology 2008; 33: 1909-1918. (Pubitemid 351832606)
19. Heller AS, Johnstone T, Shackman AJ, Light SN, Peterson MJ, Kolden GG et al. Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proc Natl Acad Sci USA 2011; 106: 22445-22450.
20. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biol Psychiatry 2003; 54: 515-528. (Pubitemid 37289438)
21. Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, Hermann D et al. Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 2005; 8: 20-21. (Pubitemid 41236725)
22. Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, de Quervain DJ et al. Aversive stimuli lead to differential amygdala activation and connectivity patterns depending on catechol-O-methyltransferase Val158Met genotype. Neuroimage 2010; 52: 1712-1719.
23. Krugel LK, Biele G, Mohr PN, Li SC, Heekeren HR. Genetic variation in dopaminergic neuromodulation influences the ability to rapidly and flexibly adapt decisions. Proc Natl Acad Sci USA 2009; 106: 17951-17956.
24. Granger CWJ. Investigating causal relations by econometric models and crossspectral methods. Econometrica 1969; 37: 424-438.
25. Goebel R, Roebroeck A, Kim DS, Formisano E. Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping. Magn Reson Imaging 2003; 21: 1251-1261. (Pubitemid 38199731)
26. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997; 6: 218-229. (Pubitemid 27488453)
27. McIntosh AR. Understanding neural interactions in learning and memory using functional neuroimaging. Ann NY Acad Sci 1998; 8: 556-571. (Pubitemid 29110037)
28. Friston K, Harrison L, PennyW. Dynamic causal modelling. Neuroimage 2003; 19: 1273-1302.
29. Almeida JR, Versace A, Mechelli A, Hassel S, Quevedo K, Kupfer DJ et al. Abnormal amygdala-prefrontal effective connectivity to happy faces differentiates bipolar from major depression. Biol Psychiatry 2009; 66: 451-459.
30. Sato JR, Fujita A, Cardoso EF, Thomaz CE, Brammer MJ, Amaro Jr E. Analyzing the connectivity between regions of interest: an approach based on cluster Granger causality for fMRI data analysis. Neuroimage 2010; 52: 1444-1455.
31. LaBar KS, Crupain MJ, Voyvodic JT, McCarthy G. Dynamic perception of facial affect and identity in the human brain. Cereb Cortex 2003; 13: 1023-1033. (Pubitemid 37168076)
32. First MB, Gibbon M, Spitzer RL, Williams JBW. SCID-1. Structured Clinical Interview for DSM-IV-TR Axis 1 Disorders. Biometrics Research: New York, NY, 2001.
33. Puls I, Mohr J, Wrase J, Vollstädt-Klein S, Leménager T, Vollmert C et al. A model comparison of COMT effects on central processing of affective stimuli. Neuroimage 2009; 46: 683-691.
34. Meyer-Lindenberg A, Nichols T, Callicott JH, Ding J, Kolachana B, Buckholtz J et al. Impact of complex genetic variation in COMT on human brain function. Mol Psychiatry 2006; 11: 867-877. (Pubitemid 44299108)
35. Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, Makarov SS et al. Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science (New York, NY) 2006; 314: 1930-1933. (Pubitemid 46026115)
36. 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. (Pubitemid 26159101)
37. Hu XZ, Lipsky RH, Zhu G, Akhtar LA, Taubman J, Greenberg BD et al. Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. Am J Hum Genet 2006; 78: 815-826.
38. Parsey RV, Hastings RS, Oquendo MA, Hu X, Goldman D, Huang YY et al. 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. (Pubitemid 43050102)
39. Zhao JH, Lissarrague S, Essioux L, Sham PC. Genecounting: haplotype analysis with missing genotypes. Bioinformatics 2002; 18: 1694-1695. (Pubitemid 36097739)
40. Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus DM, Cardoner N et al. A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry 2011; doi: 10.1016/j.eurpsy.2011.04.001 (in press).
41. Brammer MJ, Bullmore ET, Simmons A, Williams SC, Grasby PM, Howard RJ et al. Generic brain activation mapping in functional magnetic resonance imaging: A nonparametric approach. Magn Reson Imaging 1997; 15: 763-770. (Pubitemid 27398247)
42. Hamilton JP, Chen G, Thomason ME, Schwartz ME, Gotlib IH. Investigating neural primacy in major depressive disorder: multivariate Granger causality analysis of resting-state fMRI time-series data. Mol Psychiatry 2011; 16: 763-772.
43. Bassett DS, Bullmore ET. Human brain networks in health and disease. Curr Opin Neurol 2009; 22: 340-347.
44. Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends Cogn Sci 2000; 4: 223-233. (Pubitemid 30332148)
45. Said CP, Moore CD, Engell AD, Todorov A, Haxby JV. Distributed representations of dynamic facial expressions in the superior temporal sulcus. J Vis 2010; 10: 1-12.
46. Surguladze SA, Elkin A, Ecker C, Kalidindi S, Corsico A, Giampietro V et al. Genetic variation in the serotonin transporter modulates neural system-wide response to fearful faces. Genes Brain Behav 2008; 7: 543-551. (Pubitemid 351991489)
47. Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, Marchante AN et al. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 2011; 223: 403-410.
48. Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B et al. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry 2005; 62: 273-281. (Pubitemid 40990972)
49. Klumpp H, Angstadt M, Phan KL. Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder. Biol Psychol 2012; 89: 273-276.
50. Ghashghaei HT, Barbas H. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 2002; 115: 1261-1279. (Pubitemid 35351714)
51. Quirk GJ, Garcia R, Gonzblez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 2006; 60: 337-343. (Pubitemid 44215848)
52. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Mattay VS et al. A validated network of effective amygdala connectivity. Neuroimage 2007; 36: 736-745. (Pubitemid 46915503)
53. Rajkowska G, Miguel-Hidalgo JJ. Gliogenesis and glial pathology in depression. CNS Neurol Disord Drug Targets 2007; 6: 219-233. (Pubitemid 46916253)
54. Sheline YI. 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity. Biol Psychiatry 2000; 48: 791-800.
55. Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999; 156: 675-682. (Pubitemid 29220063)
56. Aggleton JP, Burton MJ, Passingham RE. Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 1980; 190: 347-368. (Pubitemid 10085062)
57. Amaral DG, Price JL. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 1984; 230: 465-496. (Pubitemid 15183874)
58. Ghashghaei HT, Hilgetag CC, Barbas H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 2007; 34: 905-923. (Pubitemid 46394469)
59. Thompson RH, Swanson LW. Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc Natl Acad Sci USA 2010; 107: 15235-15239.
60. Liao W, Qiu C, Gentili C, Walter M, Pan Z, Ding J et al. Altered effective connectivity network of the amygdala in social anxiety disorder: a resting-state FMRI study. PLoS ONE 2010; 5: e15238.
61. Deshpande G, Santhanam P, Hu X. Instantaneous and causal connectivity in resting state brain networks derived from functional MRI data. Neuroimage 2011; 54: 1043-1052.
62. Ge T, Feng J, Grabenhorst F, Rolls ET. Componential Granger causality, and its application to identifying the source and mechanisms of the topGÇôdown biased activation that controls attention to affective vs sensory processing. Neuroimage 2012; 59: 1846-1858.
63. Whalen PJ. Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Curr Dir Psychol Sci 1998; 7: 177-187.
64. Williams LM, Das P, Liddell B, Olivieri G, Peduto A, Brammer MJ et al. BOLD, sweat and fears: fMRI and skin conductance distinguish facial fear signals. Neuroreport 2005; 16: 49-52. (Pubitemid 40194559)
65. Del-Ben CM, Ferreira CA, Alves-Neto WC, Graeff FG. Serotonergic modulation offaceemotion recognition. Braz J Med Biol Res 2008; 41: 263-269.
66. Szekely E, Herba CM, Arp PP, Uitterlinden AG, Jaddoe VW, Hofman A et al. Recognition of scared faces and the serotonin transporter gene in young children: the Generation R Study. J Child Psychol Psychiatry 2011; 52: 1279-1286.
67. Lonsdorf TB, Weike AI, Nikamo P, Schalling M, Hamm AO, Ohman A. Genetic gating of human fear learning and extinction: possible implications for gene-environment interaction in anxiety disorder. Psychol Sci 2009; 20: 198-206.
68. Munafo MR, Brown SM, Hariri AR. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol Psychiatry 2008; 63: 852-857. (Pubitemid 351458448)
69. Canli T, Omura K, Haas BW, Fallgatter A, Constable RT, Lesch KP. Beyond affect: A role for genetic variation of the serotonin transporter in neural activation during a cognitive attention task. PNAS 2005; 102: 12224-12229. (Pubitemid 41291156)
70. Heinz A, Smolka MN, Braus DF, Wrase J, Beck A, Flor H et al. Serotonin transporter genotype (5-HTTLPR): effects of neutral and undefined conditions on amygdala activation. Biol Psychiatry 2007; 61: 1011-1014. (Pubitemid 46482463)
71. von dem Hagen EA, Passamonti L, Nutland S, Sambrook J, Calder AJ. The serotonin transporter gene polymorphism and the effect of baseline on amygdala response to emotional faces. Neuropsychologia 2011; 49: 674-680.