Neural mechanisms of oxytocin receptor gene mediating anxiety-related temperament

详细信息    查看全文

• 作者：Junping Wang (1)
  Wen Qin (1)
  Bing Liu (2)
  Yuan Zhou (3)
  Dawei Wang (1)
  Yunting Zhang (1)
  Tianzi Jiang (2)
  Chunshui Yu (1) (4)
  
• 关键词：Amygdala ; Anxiety ; Imaging genetics ; Oxytocin receptor ; Single nucleotide polymorphism
• 刊名：Brain Structure and Function
• 出版年：2014
• 出版时间：September 2014
• 年：2014
• 卷：219
• 期：5
• 页码：1543-1554
• 全文大小：2,293 KB
• 参考文献：1. Adewuya AO, Ola BA, Aloba OO (2007) Prevalence of major depressive disorders and a validation of the Beck Depression Inventory among Nigerian adolescents. Eur Child Adolesc Psychiatry 16:287鈥?92 CrossRef
  2. Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L, Mathews VP, Kalnin A, Lowe MJ (2005) Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biol Psychiatry 57:1079鈥?088 CrossRef
  3. Ashburner J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38:95鈥?13 CrossRef
  4. Baeken C, De Raedt R, Ramsey N, Van Schuerbeek P, Hermes D, Bossuyt A, Leyman L, Vanderhasselt MA, De Mey J, Luypaert R (2009) Amygdala responses to positively and negatively valenced baby faces in healthy female volunteers: influences of individual differences in harm avoidance. Brain Res 1296:94鈥?03 CrossRef
  5. Bakermans-Kranenburg MJ, Van IJzendoorn MH (2008) Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Soc Cogn Affect Neurosci 3:128鈥?34 CrossRef
  6. Bale TL, Davis AM, Auger AP, Dorsa DM, McCarthy MM (2001) CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J Neurosci 21:2546鈥?552
  7. Beck A, Steer R (1990) Beck Anxiety Inventory Manual. Th Psychological Corporation Harcourt Brace Jovaovich, Inc, San Antonio
  8. Bigos KL, Weinberger DR (2010) Imaging genetics鈥攄ays of future past. Neuroimage 53(3):804鈥?09 CrossRef
  9. Buckholtz JW, Callicott JH, Kolachana B, Hariri AR, Goldberg TE, Genderson M, Egan MF, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008) Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality. Mol Psychiatry 13:313鈥?24 CrossRef
  10. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7:477鈥?84 CrossRef
  11. Carter CS (1992) Oxytocin and sexual behavior. Neurosci Biobehav Rev 16:131鈥?44 CrossRef
  12. Choleris E, Devidze N, Kavaliers M, Pfaff DW (2008) Steroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety. Prog Brain Res 170:291鈥?03 CrossRef
  13. Cloninger CR (1987a) A systematic method for clinical description and classification of personality variants. A proposal. Arch General Psychiatry 44:573鈥?88 CrossRef
  14. Cloninger CR (1987b) Neurogenetic adaptive mechanisms in alcoholism. Science 236:410鈥?16 CrossRef
  15. Cloninger CR, Svrakic DM, Przybeck TR (1993) A psychobiological model of temperament and character. Arch Gen Psychiatry 50:975鈥?90 CrossRef
  16. Dannlowski U, Ohrmann P, Konrad C, Domschke K, Bauer J, Kugel H, Hohoff C, Schoning S, Kersting A, Baune BT, Mortensen LS, Arolt V, Zwitserlood P, Deckert J, Heindel W, Suslow T (2009) Reduced amygdala-prefrontal coupling in major depression: association with MAOA genotype and illness severity. Int J Neuropsychopharmacol 12:11鈥?2 CrossRef
  17. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC (2007) Oxytocin improves 鈥渕ind-reading鈥?in humans. Biol Psychiatry 61:731鈥?33 CrossRef
  18. Eickhoff SB, Heim S, Zilles K, Amunts K (2006) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. NeuroImage 32:570鈥?82 CrossRef
  19. Feldman R, Zagoory-Sharon O, Weisman O, Schneiderman I, Gordon I, Maoz R, Shalev I, Ebstein RP (2012) Sensitive parenting is associated with plasma oxytocin and polymorphisms in the OXTR and CD38 genes. Biol Psychiatry 72:175鈥?81 CrossRef
  20. Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145鈥?148 CrossRef
  21. Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629鈥?83
  22. Gong Y (1982) Manual for the Wechsler adult intelligence scale: Chinese revision. Map Press, Hunan
  23. Good CD, Johnsrude I, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage 14:685鈥?00 CrossRef
  24. Grucza RA, Przybeck TR, Spitznagel EL, Cloninger CR (2003) Personality and depressive symptoms: a multi-dimensional analysis. J Affect Disord 74:123鈥?30 CrossRef
  25. Guyer AE, Lau JY, McClure-Tone EB, Parrish J, Shiffrin ND, Reynolds RC, Chen G, Blair RJ, Leibenluft E, Fox NA, Ernst M, Pine DS, Nelson EE (2008) Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Arch Gen Psychiatry 65:1303鈥?312 CrossRef
  26. Hakamata Y, Iwase M, Iwata H, Kobayashi T, Tamaki T, Nishio M, Matsuda H, Ozaki N, Inada T (2009) Gender difference in relationship between anxiety-related personality traits and cerebral brain glucose metabolism. Psychiatry Res 173:206鈥?11 CrossRef
  27. Hammock EAD, Young LJ (2006) Oxytocin, vasopressin and pair bonding: implications for autism. Philos Trans R Soc B: Biol Sci 361:2187鈥?198 CrossRef
  28. Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U (2003) Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 54:1389鈥?398 CrossRef
  29. Huber D, Veinante P, Stoop R (2005) Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308:245鈥?48 CrossRef
  30. Inoue T, Kimura T, Azuma C, Inazawa J, Takemura M, Kikuchi T, Kubota Y, Ogita K, Saji F (1994) Structural organization of the human oxytocin receptor gene. J Biol Chem 269:32451鈥?2456
  31. Inoue H, Yamasue H, Tochigi M, Abe O, Liu X, Kawamura Y, Takei K, Suga M, Yamada H, Rogers MA, Aoki S, Sasaki T, Kasai K (2010) Association between the oxytocin receptor gene and amygdalar volume in healthy adults. Biol Psychiatry 68:1066鈥?072 CrossRef
  32. Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ (2007) Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci 27:8877鈥?884 CrossRef
  33. Kalamatianos T, Faulkes CG, Oosthuizen MK, Poorun R, Bennett NC, Coen CW (2010) Telencephalic binding sites for oxytocin and social organization: a comparative study of eusocial naked mole-rats and solitary cape mole-rats. J Comp Neurol 518:1792鈥?813 CrossRef
  34. Kim HS, Sherman DK, Sasaki JY, Xu J, Chu TQ, Ryu C, Suh EM, Graham K, Taylor SE (2010) Culture, distress, and oxytocin receptor polymorphism (OXTR) interact to influence emotional support seeking. Proc Natl Acad Sci USA 107:15717鈥?5721 CrossRef
  35. Kirsch P, Esslinger C, Chen Q, Mier D, Lis S, Siddhanti S, Gruppe H, Mattay VS, Gallhofer B, Meyer-Lindenberg A (2005) Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 25:11489鈥?1493 CrossRef
  36. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673鈥?76 CrossRef
  37. Kronenberg G, Tebartz van Elst L, Regen F, Deuschle M, Heuser I, Colla M (2009) Reduced amygdala volume in newly admitted psychiatric in-patients with unipolar major depression. J Psychiatr Res 43:1112鈥?117 CrossRef
  38. Krueger F, Parasuraman R, Iyengar V, Thornburg M, Weel J, Lin M, Clarke E, McCabe K, Lipsky RH (2012) Oxytocin receptor genetic variation promotes human trust behavior. Front Human Neurosci 6:4
  39. Li Y, Qin W, Jiang T, Zhang Y, Yu C (2012) Sex-dependent correlations between the personality dimension of harm avoidance and the resting-state functional connectivity of amygdala subregions. PLoS ONE 7:e35925 CrossRef
  40. Lucht MJ, Barnow S, Sonnenfeld C, Rosenberger A, Grabe HJ, Schroeder W, Volzke H, Freyberger HJ, Herrmann FH, Kroemer H, Rosskopf D (2009) Associations between the oxytocin receptor gene (OXTR) and affect, loneliness and intelligence in normal subjects. Prog Neuropsychopharmacol Biol Psychiatry 33:860鈥?66 CrossRef
  41. Luders E, Narr KL, Thompson PM, Rex DE, Jancke L, Steinmetz H, Toga AW (2004) Gender differences in cortical complexity. Nat Neurosci 7:799鈥?00 CrossRef
  42. Miettunen J, Veijola J, Lauronen E, Kantojarvi L, Joukamaa M (2007) Sex differences in Cloninger鈥檚 temperament dimensions鈥揳 meta-analysis. Compr Psychiatry 48:161鈥?69 CrossRef
  43. Milad MR, Rauch SL (2007) The role of the orbitofrontal cortex in anxiety disorders. Ann NY Acad Sci 1121:546鈥?61 CrossRef
  44. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97鈥?13 CrossRef
  45. Phillips ML, Drevets WC, Rauch SL, Lane R (2003) Neurobiology of emotion perception II: implications for major psychiatric disorders. Biol Psychiatry 54:515鈥?28 CrossRef
  46. Pietras T, Witusik A, Panek M, Zielinska-Wyderkiewicz E, Kuna P, Gorski P (2012) Intensity of depression in pedagogy students. Polski merkuriusz lekarski: organ Polskiego Towarzystwa Lekarskiego 32:163鈥?66
  47. Ramnani N, Behrens TE, Penny W, Matthews PM (2004) New approaches for exploring anatomical and functional connectivity in the human brain. Biol Psychiatry 56:613鈥?19 CrossRef
  48. Rimmele U, Hediger K, Heinrichs M, Klaver P (2009) Oxytocin makes a face in memory familiar. J Neurosci 29:38鈥?2 CrossRef
  49. Rodrigues SM, Saslow LR, Garcia N, John OP, Keltner D (2009) Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc Natl Acad Sci USA 106:21437鈥?1441 CrossRef
  50. Roy AK, Shehzad Z, Margulies DS, Kelly AM, Uddin LQ, Gotimer K, Biswal BB, Castellanos FX, Milham MP (2009) Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 45:614鈥?26 CrossRef
  51. Saphire-Bernstein S, Way BM, Kim HS, Sherman DK, Taylor SE (2011) Oxytocin receptor gene (OXTR) is related to psychological resources. Proc Natl Acad Sci USA 108:15118鈥?5122 CrossRef
  52. Scantamburlo G, Hansenne M, Fuchs S, Pitchot W, Marechal P, Pequeux C, Ansseau M, Legros JJ (2007) Plasma oxytocin levels and anxiety in patients with major depression. Psychoneuroendocrinology 32:407鈥?10 CrossRef
  53. 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. Am J Med Genetics Part B: Neuropsychiatric Genetics 127:85鈥?9 CrossRef
  54. Smeltzer MD, Curtis JT, Aragona BJ, Wang Z (2006) Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci Lett 394:146鈥?51 CrossRef
  55. Smith DJ, Duffy L, Stewart ME, Muir WJ, Blackwood DH (2005) High harm avoidance and low self-directedness in euthymic young adults with recurrent, early-onset depression. J Affect Disord 87:83鈥?9 CrossRef
  56. Sotres-Bayon F, Bush DE, LeDoux JE (2004) Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11:525鈥?35 CrossRef
  57. Spampinato MV, Wood JN, De Simone V, Grafman J (2009) Neural correlates of anxiety in healthy volunteers: a voxel-based morphometry study. J Neuropsychiatry Clin Neurosci 21:199鈥?05 CrossRef
  58. Starcevic V, Uhlenhuth EH, Fallon S, Pathak D (1996) Personality dimensions in panic disorder and generalized anxiety disorder. J Affect Disord 37:75鈥?9 CrossRef
  59. Svrakic DM, Draganic S, Hill K, Bayon C, Przybeck TR, Cloninger CR (2002) Temperament, character, and personality disorders: etiologic, diagnostic, treatment issues. Acta Psychiatr Scand 106:189鈥?95 CrossRef
  60. Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk MM, Young LJ, Nishimori K (2005) Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci USA 102:16096鈥?6101 CrossRef
  61. Thomas KM, Drevets WC, Dahl RE, Ryan ND, Birmaher B, Eccard CH, Axelson D, Whalen PJ, Casey BJ (2001) Amygdala response to fearful faces in anxious and depressed children. Arch Gen Psychiatry 58:1057鈥?063 CrossRef
  62. Tost H, Kolachana B, Hakimi S, Lemaitre H, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2010) A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc Natl Acad Sci USA 107:13936鈥?3941 CrossRef
  63. Westlye LT, Bjornebekk A, Grydeland H, Fjell AM, Walhovd KB (2011) Linking an anxiety-related personality trait to brain white matter microstructure: diffusion tensor imaging and harm avoidance. Arch Gen Psychiatry 68:369鈥?77 CrossRef
  64. Wu S, Jia M, Ruan Y, Liu J, Guo Y, Shuang M, Gong X, Zhang Y, Yang X, Zhang D (2005) Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biol Psychiatry 58:74鈥?7 CrossRef
  65. Yamasue H, Abe O, Suga M, Yamada H, Inoue H, Tochigi M, Rogers M, Aoki S, Kato N, Kasai K (2008) Gender-common and -specific neuroanatomical basis of human anxiety-related personality traits. Cereb Cortex 18:46鈥?2 CrossRef
  66. Yoshida MTY, Inoue K, Kimura T, Young LJ, Onaka T, Nishimori K (2009) Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29:2259鈥?271 CrossRef
  67. Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048鈥?054 CrossRef
  68. Zak PJ, Stanton AA, Ahmadi S (2007) Oxytocin increases generosity in humans. PLoS ONE 2:e1128 CrossRef
  69. Zink CF, Meyer-Lindenberg A (2012) Human neuroimaging of oxytocin and vasopressin in social cognition. Horm Behav 61:400鈥?09 CrossRef
  
• 作者单位：Junping Wang (1)
  Wen Qin (1)
  Bing Liu (2)
  Yuan Zhou (3)
  Dawei Wang (1)
  Yunting Zhang (1)
  Tianzi Jiang (2)
  Chunshui Yu (1) (4)
  
  1. Department of Radiology, Tianjin Medical University General Hospital, No. 154, Anshan Road, Heping District, 300052, Tianjin, China
  2. LIAMA Center for Computational Medicine, National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, 100190, Beijing, China
  3. Center for Social and Economic Behavior, Institute of Psychology, Chinese Academy of Sciences, Beijing, China
  4. School of Medical Imaging, Tianjin Medical University, Tianjin, China
  
• ISSN：1863-2661

文摘

A common variant (rs53576) of the OXTR gene has been implicated in a number of socio-emotional phenotypes, such as anxiety-related behavior. Previous studies have demonstrated that A-allele carriers have higher levels of physiological and dispositional stress reactivity and depressive symptomatology compared to those with the GG genotype, but the mediating neural mechanisms remain poorly understood. We combined voxel-based morphometry and resting-state functional connectivity analyses in a large cohort of healthy young Chinese Han individuals to test the hypothesis that the OXTR gene polymorphism influences an anxiety-related temperamental trait, as assessed by the harm avoidance subscale from the Tridimensional Personality Questionnaire via modulating the gray matter volume and resting-state functional connectivity of the brain, especially the limbic system. We revealed that female subjects with the AA genotype showed increased harm avoidance scores relative to G-carrier females. We also found that, compared to female individuals with the GG/GA genotype, female individuals with the AA genotype exhibited significantly smaller amygdala volumes bilaterally (especially the centromedial subregion), with a trend of allele-load-dependence. Compared to female individuals with the GG/GA genotype, female subjects with the AA genotype demonstrated reduced resting-state functional coupling between the prefrontal cortex and amygdala bilaterally, also with an allele-load-dependent trend. Furthermore, the magnitude of prefrontal-amygdala coupling in the left hemisphere was positively correlated with harm avoidance scores in female subjects. Our findings highlight a possible neural pathway by which a naturally occurring variation of the OXTR gene may affect an anxiety-related temperamental trait in female subjects by modulating prefrontal-amygdala functional connectivity.