5-HTTLPR and anxiety modulate brain-heart covariation

Psychophysiology

Volumn 50, Issue 5, 2013, Pages 441-453

  Mueller, Erik M ^a,b   Stemmler, Gerhard ^a   Hennig, Jürgen ^b   Wacker, Jan ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Anxiety; Cardiovascular; Feedback; Heart rate; Neurovisceral; Serotonin

Indexed keywords

EID: 84875646695     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/psyp.12016     Document Type: Article

References (76)

1. Arinami, T., Ohtsuki, T., Yamakawa-Kobayashi, K., Amemiya, H., Fujiwara, H., Kawata, K., ... Hamaguchi, H. (1999). A synergistic effect of serotonin transporter gene polymorphism and smoking in association with CHD. Journal of Thrombosis and Haemostasis, 81, 853-856.
2. Bell, A. J., & Sejnowski, T. J. (1995). An information-maximization approach to blind separation and blind deconvolution. Neural Computation, 7, 1129-1159. doi: 10.1162/neco.1995.7.6.1129.
3. Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., & Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746-754. doi: 10.1038/mp.2009.44.
4. Benarroch, E. E. (1997). Central autonomic network: Functional organization and clinical correlations. Armonk, NY: Futura Publishing Co.
5. Berntson, G. G., Bigger, J. T., Jr., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., ... van der Molen, M. W. (1997). Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology, 34, 623-648. doi: 10.1111/j.1469-8986.1997.tb02140.x
6. Berntson, G. G., Sarter, M., & Cacioppo, J. T. (1998). Anxiety and cardiovascular reactivity: The basal forebrain cholinergic link. Behavioral Brain Research, 94, 225-248. doi: 10.1016/S0166-4328(98)00041-2
7. Brummett, B. H., Siegler, I. C., Ashley-Koch, A., & Williams, R. B. (2011). Effects of 5HTTLPR on cardiovascular response to an emotional stressor. Psychosomatic Medicine, 73, 318-322. doi: 10.1097/PSY.0b013e3182118c16
8. Canli, T., & Lesch, K. P. (2007). Long story short: The serotonin transporter in emotion regulation and social cognition. Nature Neuroscience, 10, 1103-1109. doi: 10.1038/nn1964
9. Carver, C. S., & White, T. L. (1994). Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology, 67, 319-333. doi: 10.1037/0022-3514.67.2.319
10. Cools, R., Roberts, A. C., & Robbins, T. W. (2008). Serotoninergic regulation of emotional and behavioural control processes. Trends in Cognitive Sciences, 12, 31-40. doi: 10.1016/j.tics.2007.10.011
11. Costa, P. T., & McCrae, R. R. (1992). The Revised NEO Personality Inventory. Odessa, FL: Psychological Assessment Resources.
12. Coto, E., Reguero, J. R., Alvarez, V., Morales, B., Batalla, A., Gonzalez, P., ... Cortina, A. (2003). 5-Hydroxytryptamine 5-HT2A receptor and 5-hydroxytryptamine transporter polymorphisms in acute myocardial infarction. Clinical Science (London), 104, 241-245. doi: 10.1042/CS20020246
13. Critchley, H. D., Mathias, C. J., Josephs, O., O'Doherty, J., Zanini, S., Dewar, B. K., ... Dolan, R. J. (2003). Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence. Brain, 126, 2139-2152. doi: 10.1093/brain/awg216
14. Crone, E. A., van der Veen, F. M., van der Molen, M. W., Somsen, R. J., van Beek, B., & Jennings, J. R. (2003). Cardiac concomitants of feedback processing. Biological Psychology, 64, 143-156. doi: 10.1016/S0301-0511(03)00106-6
15. David, S. P., Murthy, N. V., Rabiner, E. A., Munafo, M. R., Johnstone, E. C., Jacob, R., ... Grasby, P. M. (2005). A functional genetic variation of the serotonin (5-HT) transporter affects 5-HT1A receptor binding in humans. Journal of Neuroscience, 25, 2586-2590. doi: 10.1523/JNEUROSCI.3769-04.2005
16. Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134, 9-21. doi: 10.1016/j.jneumeth.2003.10.009
17. Donchin, E., Heffley, E., Hillyard, S. A., Loveless, N., Maltzman, I., Ohman, A., ... Siddle, D. (1984). Cognition and event-related potentials. II. The orienting reflex and P300. Annals of the New York Academy of Sciences, 425, 39-57. doi: 10.1111/j.1749-6632.1984.tb23522.x
18. Ellis, A. J., Beevers, C. G., Hixon, J. G., & McGeary, J. E. (2011). Serotonin transporter promoter region (5-HTTLPR) polymorphism predicts resting respiratory sinus arrhythmia. Psychophysiology, 48, 923-926. doi: 10.1111/j.1469-8986.2010.01154.x
19. Friedman, B. H. (2007). An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology, 74, 185-199. doi: 10.1016/j.biopsycho.2005.08.009
20. Fumeron, F., Betoulle, D., Nicaud, V., Evans, A., Kee, F., Ruidavets, J. B., ... Cambien, F. (2002). Serotonin transporter gene polymorphism and myocardial infarction: Etude Cas-Temoins de l'Infarctus du Myocarde (ECTIM). Circulation, 105, 2943-2945. doi: 10.1161/01.CIR.0000022603.92986.99
21. Gatchel, R. J., & Lang, P. J. (1973). Accuracy of psychophysical judgments and physiological response amplitude. Journal of Experimental Psychology, 98, 175-183. doi: 10.1037/h0034312
22. Gianaros, P. J., Van Der Veen, F. M., & Jennings, J. R. (2004). Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology, 41, 521-530. doi: 10.1111/1469-8986.2004.00179.x
23. Graeff, F. G. (1994). Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals. Brazilian Journal of Medical and Biological Research, 27, 811-829.
24. Gray, J. A., & McNaughton, N. (2000). The neuropsychology of anxiety: An enquiry into the functions of the septohippocampal system (2nd ed.). Oxford, UK: Oxford University Press.
25. Grossman, P., & Taylor, E. W. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74, 263-285. doi: 10.1016/j.biopsycho.2005.11.014
26. Hajcak, G., McDonald, N., & Simons, R. F. (2003). To err is autonomic: Error-related brain potentials, ANS activity, and post-error compensatory behavior. Psychophysiology, 40, 895-903. doi: 10.1111/1469-8986.00107
27. Hajcak, G., McDonald, N., & Simons, R. F. (2004). Error-related psychophysiology and negative affect. Brain Cognition, 56, 189-197. doi: 10.1016/j.bandc.2003.11.001
28. Hirsh, J. B., & Inzlicht, M. (2008). The devil you know: Neuroticism predicts neural response to uncertainty. Psychological Science, 19, 962-967. doi: 10.1111/j.1467-9280.2008.02183.x
29. Holroyd, C. B., & Coles, M. G. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109, 679-709. doi: 10.1037/0033-295X.109.4.679
30. Homberg, J. R., & Lesch, K. P. (2011). Looking on the bright side of serotonin transporter gene variation. Biological Psychiatry, 69, 513-519. doi: 10.1016/j.biopsych.2010.09.024
31. Hu, X. Z., Lipsky, R. H., Zhu, G., Akhtar, L. A., Taubman, J., Greenberg, B. D., ... Goldman, D. (2006). Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. American Journal of Human Genetics, 78, 815-826. doi: 10.1086/503850
32. Jedema, H. P., Gianaros, P. J., Greer, P. J., Kerr, D. D., Liu, S., Higley, J. D., ... Bradberry, C. W. (2010). Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Molecular Psychiatry, 15, 512-522, 446. doi: 10.1038/mp.2009.90
33. Jordan, D. (2005). Vagal control of the heart: Central serotonergic (5-HT) mechanisms. Experimental Physiology, 90, 175-181. doi: 10.1113/expphysiol.2004.029058
34. Jovanovic, H., Lundberg, J., Karlsson, P., Cerin, A., Saijo, T., Varrone, A., ... Nordstrom, A. L. (2008). Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. Neuroimage, 39, 1408-1419. doi: 10.1016/j.neuroimage.2007.10.016
35. Karg, K., Burmeister, M., Shedden, K., & Sen, S. (2011). The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: Evidence of genetic moderation. Archives of General Psychiatry, 68, 444-454. doi: 10.1001/archgenpsychiatry.2010.189
36. Kuepper, Y., Wielpuetz, C., Alexander, N., Mueller, E., Grant, P., & Hennig, J. (2012). 5-HTTLPR S-allele: A genetic plasticity factor regarding the effects of life events on personality? Genes, Brain and Behavior, 11, 643-650. doi: 10.1111/j.1601-183X.2012.00783.x
37. Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., ... Murphy, D. L. (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
38. Li, Q., Wichems, C., Heils, A., Van De Kar, L. D., Lesch, K. P., & Murphy, D. L. (1999). Reduction of 5-hydroxytryptamine (5-HT)(1A)-mediated temperature and neuroendocrine responses and 5-HT(1A) binding sites in 5-HT transporter knockout mice. Journal of Pharmacology and Experimental Therapeutics, 291, 999-1007.
39. Light, K. C., Dolan, C. A., Davis, M. R., & Sherwood, A. (1992). Cardiovascular responses to an active coping challenge as predictors of blood pressure patterns 10 to 15 years later. Psychosomatic Medicine, 54, 217-230.
40. Manaker, S., & Verderame, H. M. (1990). Organization of serotonin 1A and 1B receptors in the nucleus of the solitary tract. Journal of Comparative Neurology, 301, 535-553.
41. Margraf, J. (1994). Mini-DIPS: Diagnostisches Kurz-Interview bei psychischen Störungen [Mini-DIPS: Short Diagnostic Interview for Mental Disorders]. Berlin, Germany: Springer.
42. Matthews, K. A., Zhu, S., Tucker, D. C., & Whooley, M. A. (2006). Blood pressure reactivity to psychological stress and coronary calcification in the Coronary Artery Risk Development in Young Adults Study. Hypertension, 47, 391-395. doi: 10.1161/01.HYP.0000200713.44895.38
43. McCaffery, J. M., Bleil, M., Pogue-Geile, M. F., Ferrell, R. E., & Manuck, S. B. (2003). Allelic variation in the serotonin transporter gene-linked polymorphic region (5-HTTLPR) and cardiovascular reactivity in young adult male and female twins of European-American descent. Psychosomatic Medicine, 65, 721-728.
44. Meng, X.-L., Rosenthal, R., & Rubin, D. B. (1992). Comparing correlated correlation coefficients. Psychological Bulletin, 111, 172-175. doi: 10.1037/0033-2909.111.1.172
45. Miltner, W. H. R., Braun, C. H., & Coles, M. G. H. (1997). Event-related brain potentials following incorrect feedback in a time-estimation task: Evidence for a "generic" neural system for error detection. Journal of Cognitive Neuroscience, 9, 788-798.
46. Minelli, A., Bonvicini, C., Scassellati, C., Sartori, R., & Gennarelli, M. (2011). The influence of psychiatric screening in healthy populations selection: A new study and meta-analysis of functional 5-HTTLPR and rs25531 polymorphisms and anxiety-related personality traits. BMC Psychiatry, 11, 50. doi: 10.1186/1471-244X-11-50
47. Mueller, E. M., Evers, E. A., Wacker, J., & van der Veen, F. M. (2012). Acute tryptophan depletion attenuates brain-heart coupling following external feedback. Frontiers in Human Neuroscience, 6, 77. doi: 10.3389/fnhum.2012.00077
48. Mueller, E. M., Makeig, S., Stemmler, G., Hennig, J., & Wacker, J. (2011). Dopamine effects on human error processing depend on catechol-O-methyltransferase VAL158MET genotype. Journal of Neuroscience, 31, 15818-15825. doi: 10.1523/JNEUROSCI.2103-11.2011
49. Mueller, E. M., Stemmler, G., & Wacker, J. (2010). Single-trial electroencephalogram predicts cardiac acceleration: A time-lagged P-correlation approach for studying neurovisceral connectivity. Neuroscience, 166, 491-500. doi: 10.1016/j.neuroscience.2009.12.051
50. Osinsky, R., Reuter, M., Kupper, Y., Schmitz, A., Kozyra, E., Alexander, N., & Hennig, J. (2008). Variation in the serotonin transporter gene modulates selective attention to threat. Emotion, 8, 584-588. doi: 10.1037/a0012826
51. Ostendorf, F., & Angleitner, A. (2004). NEO-Persönlichkeitsinventar nach Costa und McCrae, revidierte Form (NEO-PI-R) [NEO Personality Inventory by Costa and McCrae, revised ed.]. Göttingen, Germany: Hogrefe.
52. Otten, L. J., Gaillard, A. W., & Wientjes, C. J. (1995). The relation between event-related brain potential, heart rate, and blood pressure responses in an S1-S2 paradigm. Biological Psychology, 39, 81-102. doi: 10.1016/0301-0511(94)00969-5
53. Pacheco, J., Beevers, C. G., Benavides, C., McGeary, J., Stice, E., & Schnyer, D. M. (2009). Frontal-limbic white matter pathway associations with the serotonin transporter gene promoter region (5-HTTLPR) polymorphism. Journal of Neuroscience, 29, 6229-6233. doi: 10.1523/JNEUROSCI.0896-09.2009
54. Patrick, C. J., Durbin, C. E., & Moser, J. S. (2012). Reconceptualizing antisocial deviance in neurobehavioral terms. Developmental Psychopathology, 24, 1047-1071.
55. Pezawas, L., Meyer-Lindenberg, A., Drabant, E. M., Verchinski, B. A., Munoz, K. E., Kolachana, B. S., ... Weinberger, D. R. (2005). 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: A genetic susceptibility mechanism for depression. Nature Neuroscience, 8, 828-834. doi: 10.1038/nn1463
56. Pizzagalli, D. A., Jahn, A. L., & O'Shea, J. P. (2005). Toward an objective characterization of an anhedonic phenotype: A signal-detection approach. Biological Psychiatry, 57, 319-327. doi: 10.1016/j.biopsych.2004.11.026
57. Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A polyvagal theory. Psychophysiology, 32, 301-318. doi: 10.1111/j.1469-8986.1995.tb01213.x
58. Ramage, A. G., & Villalón, C. M., 2008. 5-Hydroxytryptamine and cardiovascular regulation. Trends in Pharmacological Sciences, 29, 472-481. doi: 10.1016/j.tips.2008.06.009
59. Risch, N., Herrell, R., Lehner, T., Liang, K. Y., Eaves, L., Hoh, J., ... Merikangas, K. R. (2009). Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: A meta-analysis. Journal of the American Medical Association, 301, 2462-2471. doi: 10.1001/jama.2009.878
60. Santesso, D. L., Bogdan, R., Birk, J. L., Goetz, E. L., Holmes, A. J., & Pizzagalli, D. A. (2012). Neural responses to negative feedback are related to negative emotionality in healthy adults. Social Cognitive & Affective Neuroscience, 7, 794-803. doi: 10.1093/scan/nsr054
61. Sato, A., Yasuda, A., Ohira, H., Miyawaki, K., Nishikawa, M., Kumano, H., & Kuboki, T. (2005). Effects of value and reward magnitude on feedback negativity and P300. NeuroReport, 16, 407-411. doi: 10.1097/00001756-200503150-00020
62. Schinka, J. A., Busch, R. M., & Robichaux-Keene, N. (2004). A meta-analysis of the association between the serotonin transporter gene polymorphism (5-HTTLPR) and trait anxiety. Molecular Psychiatry, 9, 197-202. doi: 10.1038/sj.mp.4001405
63. Sen, S., Burmeister, M., & Ghosh, D. (2004). Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 127B, 85-89.
64. Thayer, J. F., & Lane, R. D. (2007). The role of vagal function in the risk for cardiovascular disease and mortality. Biological Psychology, 74, 224-242. doi: 10.1016/j.biopsycho.2005.11.013
65. Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 33, 81-88. doi: 10.1016/j.neubiorev.2008.08.004
66. Thayer, J. F., Smith, M., Rossy, L. A., Sollers, J. J., & Friedman, B. H. (1998). Heart period variability and depressive symptoms: Gender differences. Biological Psychiatry, 44, 304-306. doi: 10.1016/S0006-3223(98)00008-0
67. Thor, K. B., Blitz-Siebert, A., & Helke, C. J. (1992). Autoradiographic localization of 5HT1 binding sites in autonomic areas of the rat dorsomedial medulla oblongata. Synapse, 10, 217-227. doi: 10.1002/syn.890100305
68. Treiber, F. A., Kamarck, T., Schneiderman, N., Sheffield, D., Kapuku, G., & Taylor, T. (2003). Cardiovascular reactivity and development of preclinical and clinical disease states. Psychosomatic Medicine, 65, 46-62.
69. van der Veen, F. M., van der Molen, M. W., Crone, E. A., & Jennings, J. R. (2004). Phasic heart rate responses to performance feedback in a time production task: Effects of information versus valence. Biological Psychology, 65, 147-161.
70. Vulturar, R., Chis, A., Ungureanu, L., & Miu, A. C. (2012). Respiratory sinus arrhythmia and serotonin transporter promoter gene polymorphisms: Taking a triallelic approach makes a difference. Psychophysiology, 49, 1412-1416. doi: 10.1111/j.1469-8986.2012.01445.x
71. Wacker, J., Mueller, E. M., Hennig, J., & Stemmler, G. (2012). How to consistently link extraversion and intelligence to the catechol-O-methyltransferase (COMT) gene: On defining and measuring psychological phenotypes in neurogenetic research. Journal of Personality and Social Psychology, 102, 427-444. doi: 10.1037/a0026544
72. Wager, T. D., Waugh, C. E., Lindquist, M., Noll, D. C., Fredrickson, B. L., & Taylor, S. F. (2009). Brain mediators of cardiovascular responses to social threat Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage, 47, 821-835. doi: 10.1016/j.neuroimage.2009.05.043
73. Wilhelm, K., Mitchell, P. B., Niven, H., Finch, A., Wedgwood, L., Scimone, A., ... Schofield, P. R. (2006). Life events, first depression onset and the serotonin transporter gene. British Journal of Psychiatry, 188, 210-215. doi: 10.1192/bjp.bp.105.009522
74. Williams, R. B., Marchuk, D. A., Gadde, K. M., Barefoot, J. C., Grichnik, K., Helms, M. J., ... Siegler, I. C. (2001). Central nervous system serotonin function and cardiovascular responses to stress. Psychosomatic Medicine, 63, 300-305.
75. Williams, R. B., Marchuk, D. A., Siegler, I. C., Barefoot, J. C., Helms, M. J., Brummett, B. H., ... Schanberg, S. M. (2008). Childhood socioeconomic status and serotonin transporter gene polymorphism enhance cardiovascular reactivity to mental stress. Psychosomatic Medicine, 70, 32-39. doi: 10.1097/PSY.0b013e31815f66c3
76. Zalsman, G., Huang, Y. Y., Oquendo, M. A., Burke, A. K., Hu, X. Z., Brent, D. A., ... Mann, J. J. (2006). Association of a triallelic serotonin transporter gene promoter region (5-HTTLPR) polymorphism with stressful life events and severity of depression. American Journal of Psychiatry, 163, 1588-1593. doi: 10.1176/appi.ajp.163.9.1588