Impact of FAAH genetic variation on fronto-amygdala function during emotional processing

  • Anne GärtnerEmail author
  • Denise Dörfel
  • Kersten Diers
  • Stephanie H. Witt
  • Alexander Strobel
  • Burkhard Brocke
Original Paper


Recent translational studies identified a common endocannabinoid polymorphism, FAAH C385A, in the gene for the fatty acid amide hydrolase (FAAH). This polymorphism alters endocannabinoid anandamide levels, which are known to be involved in the fronto-amygdala circuitry implicated in mood regulation and anxiety-like behaviors. While it has been shown that the variant that selectively enhances fronto-amygdala connectivity at rest is associated with decreased anxiety-like behaviors, no study so far has investigated whether this finding of FAAH-related differential plasticity extends to task-related differential functional expression and regulation during negative emotional processing. Using an imaging genetics approach, this study aimed to replicate and extend prior findings by examining functional activity and task-related connectivity in fronto-amygdala regions during emotion reactivity and emotional down-regulation of negative affect. Therefore, 48 healthy young adults underwent a functional MRI resting state measurement, completed an emotion regulation paradigm and provided self-reports on anxiety and use of emotion regulation strategies. In line with previous studies, preliminary evidence suggests that A-allele carriers demonstrate stronger fronto-amygdala connectivity during rest. In addition, exploratory whole-brain analyses indicate differential functional activity of A-allele carriers during emotion reactivity and emotion regulation. There were no associations with anxiety-related self-reports and use of emotional regulation strategies. Further research using larger samples and polygenic approaches is indicated to clarify the precise role and its underlying mechanisms in emotion processing.


FAAH C385A Fronto-amygdala Amygdala Emotion reactivity Emotion regulation Individual differences Functional connectivity fMRI Genetics 



This research was funded by the Deutsche Forschungsgemeinschaft (SFB 940, project A5) to AS, KD and BB. We thank Fanny Weber-Göricke for her valuable help in data acquisition.

Author contributions

AG, KD, BB and AS designed the research; KD performed the measurements; AG and KD conducted the analyses; SHW was responsible for DNA extraction and genotyping; AG, DD, BB, AS and SHW wrote the paper. The final version of the paper was approved by all authors.

Compliance with ethical standards

Conflict of interest

None of the authors has a conflict of interest to declare.

Supplementary material

406_2018_944_MOESM1_ESM.docx (21.1 mb)
Supplementary material 1 (DOCX 21658 kb)


  1. 1.
    Abler B, Kessler H (2009) Emotion regulation questionnaire—Eine deutschsprachige Fassung des ERQ von Gross und John. Diagnostica 55(3):144–152. CrossRefGoogle Scholar
  2. 2.
    Ashton CH, Moore PB (2011) Endocannabinoid system dysfunction in mood and related disorders: endocannabinoids in mood disorders. Acta Psychiatr Scand 124(4):250–261. PubMedCrossRefGoogle Scholar
  3. 3.
    Banks SJ, Eddy KT, Angstadt M, Nathan PJ, Phan KL (2007) Amygdala–frontal connectivity during emotion regulation. Soc Cogn Affect Neurosci 2(4):303–312. PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage 37(1):90–101. PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Boileau I, Tyndale RF, Williams B, Mansouri E, Westwood DJ, Foll BL, Tong J et al (2015) The fatty acid amide hydrolase C385A variant affects brain binding of the positron emission tomography tracer [11 C]CURB. J Cereb Blood Flow Metab 35(8):1237–1240. PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Borkenau P, Ostendorf F (1993) NEO-Fünf-Faktoren Inventar (NEO-FFI) nach Costa und McCrae. Z Klin Psychol Psychother 28(2):145–146. CrossRefGoogle Scholar
  7. 7.
    Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108(3):624–652PubMedCrossRefGoogle Scholar
  8. 8.
    Brühl AB, Kaffenberger T, Herwig U (2010) Serotonergic and noradrenergic modulation of emotion processing by single dose antidepressants. Neuropsychopharmacology 35(2):521–533. PubMedCrossRefGoogle Scholar
  9. 9.
    Buhle JT, Silvers JA, Wager TD, Lopez R, Onyemekwu C, Kober H, Ochsner KN et al (2014) Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb Cortex 24(11):2981–2990. PubMedCrossRefGoogle Scholar
  10. 10.
    Casey BJ, Glatt CE, Lee FS (2015) Treating the developing versus developed brain: translating preclinical mouse and human studies. Neuron 86(6):1358–1368. PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Chhatwal JP, Ressler KJ (2007) Modulation of fear and anxiety by the endogenous cannabinoid system. CNS Spectr 12(03):211–220. PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Chiang KP (2004) Reduced cellular expression and activity of the P129T mutant of human fatty acid amide hydrolase: evidence for a link between defects in the endocannabinoid system and problem drug use. Hum Mol Genet 13(18):2113–2119. PubMedCrossRefGoogle Scholar
  13. 13.
    Conzelmann A, Reif A, Jacob C, Weyers P, Lesch K-P, Lutz B, Pauli P (2012) A polymorphism in the gene of the endocannabinoid-degrading enzyme FAAH (FAAH C385A) is associated with emotional–motivational reactivity. Psychopharmacology 224(4):573–579. PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH (2001) Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci 98(16):9371–9376. PubMedCrossRefGoogle Scholar
  15. 15.
    Cravatt BF, Giang DK, Mayfield S, Boger DL, Lerner RA, Gilula NB (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384(6604):83–87. PubMedCrossRefGoogle Scholar
  16. 16.
    Critchley HD (2004) The human cortex responds to an interoceptive challenge. Proc Natl Acad Sci 101(17):6333–6334. PubMedCrossRefGoogle Scholar
  17. 17.
    Critchley HD, Mathias CJ, Josephs O, O’Doherty J, Zanini S, Dewar B-K, Dolan RJ et al (2003) Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126(10):2139–2152. PubMedCrossRefGoogle Scholar
  18. 18.
    Fonseca de FR, Ramos JA, Bonnin A, Fernández-Ruiz JJ (1993) Presence of cannabinoid binding sites in the brain from early postnatal ages. NeuroReport 4(2):135–138. CrossRefGoogle Scholar
  19. 19.
    Diers K, Weber F, Brocke B, Strobel A, Schönfeld S (2014) Instructions matter: a comparison of baseline conditions for cognitive emotion regulation paradigms. Front Psychol. PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Dincheva I, Drysdale AT, Hartley CA, Johnson DC, Jing D, King EC, Lee FS et al (2015) FAAH genetic variation enhances fronto-amygdala function in mouse and human. Nature Commun 6:6395. CrossRefGoogle Scholar
  21. 21.
    Dörfel D, Lamke J-P, Hummel F, Wagner U, Erk S, Walter H (2014) Common and differential neural networks of emotion regulation by detachment, reinterpretation, distraction, and expressive suppression: a comparative fMRI investigation. NeuroImage 101:298–309. PubMedCrossRefGoogle Scholar
  22. 22.
    Eickhoff SB, Paus T, Caspers S, Grosbras M-H, Evans AC, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. NeuroImage 36(3):511–521. PubMedCrossRefGoogle Scholar
  23. 23.
    Ellgren M, Artmann A, Tkalych O, Gupta A, Hansen HS, Hansen SH, Hurd YL et al (2008) Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects. Eur Neuropsychopharmacol 18(11):826–834. PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Erk S, Mikschl A, Stier S, Ciaramidaro A, Gapp V, Weber B, Walter H (2010) Acute and sustained effects of cognitive emotion regulation in major depression. J Neurosci 30(47):15726–15734. PubMedCrossRefGoogle Scholar
  25. 25.
    Etkin A, Büchel C, Gross JJ (2015) The neural bases of emotion regulation. Nat Rev Neurosci 16(11):693–700. PubMedCrossRefGoogle Scholar
  26. 26.
    Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15(2):85–93. PubMedCrossRefGoogle Scholar
  27. 27.
    Faul F, Erdfelder E, Buchner A, Lang A-G (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41(4):1149–1160. PubMedCrossRefGoogle Scholar
  28. 28.
    Finger EC, Mitchell DGV, Jones M, Blair RJR (2008) Dissociable roles of medial orbitofrontal cortex in human operant extinction learning. NeuroImage 43(4):748–755. PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Gee DG, Fetcho RN, Jing D, Li A, Glatt CE, Drysdale AT, the Consortium PING et al (2016) Individual differences in frontolimbic circuitry and anxiety emerge with adolescent changes in endocannabinoid signaling across species. Proc Natl Acad Sci 113(16):4500–4505. PubMedCrossRefGoogle Scholar
  30. 30.
    Gottesman II, Gould TD (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160(4):636–645. PubMedCrossRefGoogle Scholar
  31. 31.
    Gottfried JA, Dolan RJ (2004) Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value. Nat Neurosci 7(10):1144–1152. PubMedCrossRefGoogle Scholar
  32. 32.
    Gunduz-Cinar O, Hill MN, McEwen BS, Holmes A (2013) Amygdala FAAH and anandamide: mediating protection and recovery from stress. Trends Pharmacol Sci 34(11):637–644. PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Gunduz-Cinar O, MacPherson KP, Cinar R, Gamble-George J, Sugden K, Williams B, Holmes A et al (2013) Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity. Mol Psychiatry 18(7):813–823. PubMedCrossRefGoogle Scholar
  34. 34.
    Halldorsdottir T, Binder EB (2017) Gene × environment interactions: from molecular mechanisms to behavior. Annu Rev Psychol 68(1):215–241. PubMedCrossRefGoogle Scholar
  35. 35.
    Hariri AR, Gorka A, Hyde LW, Kimak M, Halder I, Ducci F, Manuck SB et al (2009) Divergent effects of genetic variation in endocannabinoid signaling on human threat- and reward-related brain function. Biol Psychiatr 66(1):9–16. CrossRefGoogle Scholar
  36. 36.
    Heng L, Beverley JA, Steiner H, Tseng KY (2011) Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas. Synapse 65(4):278–286. PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Hill MN, Hillard CJ, Bambico FR, Patel S, Gorzalka BB, Gobbi G (2009) The therapeutic potential of the endocannabinoid system for the development of a novel class of antidepressants. Trends Pharmacol Sci 30(9):484–493. PubMedCrossRefGoogle Scholar
  38. 38.
    Hill MN, Patel S (2013) Translational evidence for the involvement of the endocannabinoid system in stress-related psychiatric illnesses. Biol Mood Anxiety Disord 3(1):19. PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Kalisch R (2009) The functional neuroanatomy of reappraisal: time matters. Neurosci Biobehav Rev 33(8):1215–1226. PubMedCrossRefGoogle Scholar
  40. 40.
    Kalisch R, Wiech K, Critchley HD, Dolan RJ (2006) Levels of appraisal: a medial prefrontal role in high-level appraisal of emotional material. NeuroImage 30(4):1458–1466. PubMedCrossRefGoogle Scholar
  41. 41.
    Kanske P, Heissler J, Schönfelder S, Bongers A, Wessa M (2011) How to regulate emotion? Neural networks for reappraisal and distraction. Cereb Cortex 21(6):1379–1388. PubMedCrossRefGoogle Scholar
  42. 42.
    Kerns JG (2004) Anterior cingulate conflict monitoring and adjustments in control. Science 303(5660):1023–1026. PubMedCrossRefGoogle Scholar
  43. 43.
    Kret ME, Ploeger A (2015) Emotion processing deficits: a liability spectrum providing insight into comorbidity of mental disorders. Neurosci Biobehav Rev 52:153–171. PubMedCrossRefGoogle Scholar
  44. 44.
    Krohne HW, Egloff B, Kohlmann CW, Tausch A (1996) Untersuchungen mit einer deutschen Version der “Positive and Negative Affect Schedule” (PANAS). Diagnostica 42:139–156Google Scholar
  45. 45.
    Krüger G, Glover GH (2001) Physiological noise in oxygenation-sensitive magnetic resonance imaging. Magn Reson Med 46(4):631–637PubMedCrossRefGoogle Scholar
  46. 46.
    Lafenêtre P, Chaouloff F, Marsicano G (2007) The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol Res 56(5):367–381. PubMedCrossRefGoogle Scholar
  47. 47.
    Lange MD, Daldrup T, Remmers F, Szkudlarek HJ, Lesting J, Guggenhuber S, Pape HC et al (2017) Cannabinoid CB1 receptors in distinct circuits of the extended amygdala determine fear responsiveness to unpredictable threat. Mol Psychiatry 22(10):1422–1430. PubMedCrossRefGoogle Scholar
  48. 48.
    Lang PJ, Bradley MM, Cuthbert BN (1999) International affective picture system (IAPS): instruction manual and affective ratings (Vol. Center for Research in Psychophysiology). University of Florida, GainesvilleGoogle Scholar
  49. 49.
    Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait-Angstinventar (STAI). Beltz, WeinheimGoogle Scholar
  50. 50.
    Lazary J, Eszlari N, Juhasz G, Bagdy G (2016) Genetically reduced FAAH activity may be a risk for the development of anxiety and depression in persons with repetitive childhood trauma. Eur Neuropsychopharmacol 26(6):1020–1028. PubMedCrossRefGoogle Scholar
  51. 51.
    Lee TT-Y, Gorzalka BB (2012) Timing is everything: evidence for a role of corticolimbic endocannabinoids in modulating hypothalamic–pituitary–adrenal axis activity across developmental periods. Neuroscience 204:17–30. PubMedCrossRefGoogle Scholar
  52. 52.
    Lee TT-Y, Hill MN, Hillard CJ, Gorzalka BB (2013) Temporal changes in N-acylethanolamine content and metabolism throughout the peri-adolescent period. Synapse 67(1):4–10. PubMedCrossRefGoogle Scholar
  53. 53.
    Leppänen JM (2006) Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Curr Opin Psychiatry 19(1):34–39. PubMedCrossRefGoogle Scholar
  54. 54.
    Lichtman AH, Shelton CC, Advani T, Cravatt BF (2004) Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain 109(3):319–327. PubMedCrossRefGoogle Scholar
  55. 55.
    Lieberman MD, Cunningham WA (2009) Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 4(4):423–428. PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Lieb W, Manning AK, Florez JC, Dupuis J, Cupples LA, McAteer JB, Fox CS et al (2009) Variants in the CNR1 and the FAAH genes and adiposity traits in the community. Obesity 17(4):755–760. PubMedCrossRefGoogle Scholar
  57. 57.
    Long LE, Lind J, Webster M, Weickert C (2012) Developmental trajectory of the endocannabinoid system in human dorsolateral prefrontal cortex. BMC Neurosci 13(1):87. PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Lövheim H (2012) A new three-dimensional model for emotions and monoamine neurotransmitters. Med Hypotheses 78(2):341–348. PubMedCrossRefGoogle Scholar
  59. 59.
    Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19(3):1233–1239. PubMedCrossRefGoogle Scholar
  60. 60.
    Martin EI, Ressler KJ, Binder E, Nemeroff CB (2009) The neurobiology of anxiety disorders: brain imaging, genetics, and psychoneuroendocrinology. Psychiatr Clin N Am 32(3):549–575. CrossRefGoogle Scholar
  61. 61.
    McLaren DG, Ries ML, Xu G, Johnson SC (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61(4):1277–1286. PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    McRae K, Jacobs SE, Ray RD, John OP, Gross JJ (2012) Individual differences in reappraisal ability: links to reappraisal frequency, well-being, and cognitive control. J Res Pers 46(1):2–7. CrossRefGoogle Scholar
  63. 63.
    Micale V, Di Marzo V, Sulcova A, Wotjak CT, Drago F (2013) Endocannabinoid system and mood disorders: priming a target for new therapies. Pharmacol Ther 138(1):18–37. PubMedCrossRefGoogle Scholar
  64. 64.
    Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL (2007) A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatr 62(10):1191–1194. CrossRefGoogle Scholar
  65. 65.
    Moreira FA, Kaiser N, Monory K, Lutz B (2008) Reduced anxiety-like behaviour induced by genetic and pharmacological inhibition of the endocannabinoid-degrading enzyme fatty acid amide hydrolase (FAAH) is mediated by CB1 receptors. Neuropharmacology 54(1):141–150. PubMedCrossRefGoogle Scholar
  66. 66.
    Moreira FA, Wotjak CT (2009) Cannabinoids and anxiety. In: Stein MB, Steckler T (eds) Behavioral neurobiology of anxiety and its treatment, vol 2. Springer, Berlin, pp 429–450. CrossRefGoogle Scholar
  67. 67.
    Murphy K, Birn RM, Bandettini PA (2013) Resting-state fMRI confounds and cleanup. NeuroImage 80:349–359. PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Myers AJ, Williams L, Gatt JM, McAuley-Clark EZ, Dobson-Stone C, Schofield PR, Nemeroff CB (2014) Variation in the oxytocin receptor gene is associated with increased risk for anxiety, stress and depression in individuals with a history of exposure to early life stress. J Psychiatr Res 59:93–100. PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Ochsner KN, Bunge SA, Gross JJ, Gabrieli JDE (2002) Rethinking feelings: an fMRI study of the cognitive regulation of emotion. J Cogn Neurosci 14(8):1215–1229. PubMedCrossRefGoogle Scholar
  70. 70.
    Ochsner KN, Gross JJ (2008) Cognitive emotion regulation: insights from social cognitive and affective neuroscience. Curr Dir Psychol Sci 17(2):153–158. PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JDE, Gross JJ (2004) For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23(2):483–499. PubMedCrossRefGoogle Scholar
  72. 72.
    Ochsner KN, Silvers JA, Buhle JT (2012) Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion: functional imaging studies of emotion regulation. Ann N Y Acad Sci 1251(1):E1–E24. PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    O’Reilly JX, Woolrich MW, Behrens TEJ, Smith SM, Johansen-Berg H (2012) Tools of the trade: psychophysiological interactions and functional connectivity. Soc Cogn Affect Neurosci 7(5):604–609. PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Patricelli MP, Cravatt BF (2001) Proteins regulating the biosynthesis and inactivation of neuromodulatory fatty acid amides. In: Vitamins and hormones, vol 62, pp 95–131. Elsevier.
  75. 75.
    Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2(6):417–424. PubMedCrossRefGoogle Scholar
  76. 76.
    Phillips ML, Ladouceur CD, Drevets WC (2008) A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13(9):833–857. CrossRefGoogle Scholar
  77. 77.
    Ruehle S, Rey AA, Remmers F, Lutz B (2012) The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol 26(1):23–39. PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Schiller D, Delgado MR (2010) Overlapping neural systems mediating extinction, reversal and regulation of fear. Trends Cogn Sci 14(6):268–276. PubMedCrossRefGoogle Scholar
  79. 79.
    Sipe JC, Chiang K, Gerber AL, Beutler E, Cravatt BF (2002) A missense mutation in human fatty acid amide hydrolase associated with problem drug use. Proc Natl Acad Sci 99(12):8394–8399. PubMedCrossRefGoogle Scholar
  80. 80.
    Sipe JC, Scott TM, Murray S, Harismendy O, Simon GM, Cravatt BF, Waalen J (2010) Biomarkers of endocannabinoid system activation in severe obesity. PLoS One 5(1):e8792. PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Sipe JC, Waalen J, Gerber A, Beutler E (2005) Overweight and obesity associated with a missense polymorphism in fatty acid amide hydrolase (FAAH). Int J Obes 29(7):755–759. CrossRefGoogle Scholar
  82. 82.
    Spagnolo PA, Ramchandani VA, Schwandt ML, Kwako LE, George DT, Mayo LM, Heilig M et al (2016) FAAH gene variation moderates stress response and symptom severity in patients with posttraumatic stress disorder and comorbid alcohol dependence. Alcohol Clin Exp Res 40(11):2426–2434. PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Joliot M et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289. PubMedCrossRefGoogle Scholar
  84. 84.
    Viveros M, Marco E, File S (2005) Endocannabinoid system and stress and anxiety responses. Pharmacol Biochem Behav 81(2):331–342. PubMedCrossRefGoogle Scholar
  85. 85.
    Walter H, von Kalckreuth A, Schardt D, Stephan A, Goschke T, Erk S (2009) The temporal dynamics of voluntary emotion regulation. PLoS One 4(8):e6726. PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Wessa M, Kanske P, Neumeister P, Bode K, Heissler J, Schönfelder S (2010) EmoPicS: Subjektive und psychophysiologische Evaluation neuen Bildmaterials für die klinischbiopsychologische Forschung [EmoPicS: Subjective and psychophysiological evaluation of new imagery for clinical biopsychological research]. Z Klin Psychol Psychother Supplement 1:11–77Google Scholar
  87. 87.
    Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2(3):125–141. PubMedCrossRefGoogle Scholar
  88. 88.
    Yates A, Akanni W, Amode MR, Barrell D, Billis K, Carvalho-Silva D, Flicek P et al (2016) Ensembl 2016. Nucleic Acids Res 44(D1):D710–D716. PubMedCrossRefGoogle Scholar
  89. 89.
    Ziegler C, Richter J, Mahr M, Gajewska A, Schiele MA, Gehrmann A, Domschke K et al (2016) MAOA gene hypomethylation in panic disorder—reversibility of an epigenetic risk pattern by psychotherapy. Transl Psychiatry 6(4):e773–e773. PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Anne Gärtner
    • 1
    Email author
  • Denise Dörfel
    • 1
  • Kersten Diers
    • 1
  • Stephanie H. Witt
    • 2
  • Alexander Strobel
    • 1
  • Burkhard Brocke
    • 1
  1. 1.Faculty of PsychologyTechnische Universität DresdenDresdenGermany
  2. 2.Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, Medical Faculty MannheimUniversity of HeidelbergMannheimGermany

Personalised recommendations