Sex differences in the functional connectivity of the amygdalae in association with cortisol

NeuroImage

Volumn 134, Issue , 2016, Pages 410-423

  Kogler, Lydia ^a,g,h   Müller, Veronika I ^b,c   Seidel, Eva Maria ^d   Boubela, Roland ^e   Kalcher, Klaudius ^e   Moser, Ewald ^e,f   Habel, Ute ^b,g,h,i   Gur, Ruben C ^f   Eickhoff, Simon B ^b,c   Derntl, Birgit ^a,b,g,h  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c Department of Orthopedic Surgery   (Germany)

^d UNIVERSITY OF VIENNA   (Austria)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g Julich Aachen Research Alliance   (Germany)

^h RWTH AACHEN UNIVERSITY   (Germany)

ⁱ JARA BRAIN Institute 1: Structure Function Relationship   (Germany)

Author keywords

Cortisol; Frontal cortex; Hippocampus; Resting state; Striatum; Task independent

Indexed keywords

HYDROCORTISONE; SEX HORMONE;

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; HYDROCORTISONE BLOOD LEVEL; IMAGE ANALYSIS; IMAGE PROCESSING; INFERIOR FRONTAL GYRUS; MALE; MIDDLE TEMPORAL GYRUS; NEUROIMAGING; NEUROMODULATION; NORMAL HUMAN; PARIETO-OCCIPITAL SULCUS; POSTCENTRAL GYRUS; PRIORITY JOURNAL; SEX DIFFERENCE; SUPPLEMENTARY MOTOR AREA; VOXEL BASED MORPHOMETRY; AMYGDALA; BRAIN MAPPING; METABOLISM; NERVE CELL NETWORK; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; SALIVA; SEX FACTOR; TISSUE DISTRIBUTION;

ADULT; AMYGDALA; BRAIN MAPPING; FEMALE; GONADAL STEROID HORMONES; HUMANS; HYDROCORTISONE; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; NEURAL PATHWAYS; SALIVA; SEX FACTORS; TISSUE DISTRIBUTION;

EID: 84963942474     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.03.064     Document Type: Article

References (116)

1. Achim M., Lepage M. Neural correlates of memory for items and for associations: an event-related functional magnetic resonance imaging study. J. Cogn. Neurosci. 2005, 14:652-667.
2. Alarcón G., Cservenka A., Rudolph M.D., Fair D.A., Nagel B.J. Developmental sex differences in resting state functional connectivity of amygdala sub-regions. NeuroImage 2015, 115:235-244. 10.1016/j.neuroimage.2015.04.013.
3. Albert K., Pruessner J., Newhouse P. Estradiol levels modulate brain activity and negative responses to psychosocial stress across the menstrual cycle. Psychoneuroendocrinology 2015, 59:14-24. 10.1016/j.psyneuen.2015.04.022.
4. Andreano J.M., Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. NeuroImage 2010, 53:1286-1293. 10.1016/j.neuroimage.2010.07.011.Menstrual.
5. Andreano J.M., Arjomandi H., Cahill L. Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology 2008, 33:874-882. 10.1016/j.psyneuen.2008.03.009.
6. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26:839-851. 10.1016/j.neuroimage.2005.02.018.
7. Beck A., Schlagenhauf F., Wüstenberg T., Hein J., Kienast T., Kahnt T., Schmack K., Hägele C., Knutson B., Heinz A., Wrase J. Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol. Psychiatry 2009, 66:734-742. 10.1016/j.biopsych.2009.04.035.
8. Behrens T.E., Johansen-Berg H., Woolrich M.W., Smith S.M., Wheeler-Kingshott C.A., Boulby P.A., Barker G.J., Sillery E.L., Sheehan K., Ciccarelli O., Thompson A.J., Brady J.M., Matthews P.M. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 2003, 6:750-757.
9. Bingel U., Lorenz J., Schoell E., Weiller C., Büchel C. Mechanisms of placebo analgesia: rACC recruitment of a subcortical antinociceptive network. Pain 2006, 120:8-15. 10.1016/j.pain.2005.08.027.
10. Bludau S., Eickhoff S.B., Mohlberg H., Caspers S., Laird A.R., Fox P.T., Schleicher A., Zilles K., Amunts K. Cytoarchitecture, probability maps and functions of the human frontal pole. NeuroImage 2014, 93:260-275. 10.1016/j.neuroimage.2013.05.052.
11. Bluhm R.L., Williamson P.C., Osuch E.A., Frewen P.A., Stevens T.K., Boksman K., Neufeld R.W.J., Théberge J., Lanius R.A. Alterations in default network connectivity in posttraumatic stress disorder related to early-life trauma. J. Psychiatry Neurosci. 2009, 34:187-194.
12. Boubela R.N., Kalcher K., Huf W., Seidel E.-M., Derntl B., Pezawas L., Nasel C., Moser E. fMRI measurements of amygdala activation are confounded by stimulus correlated signal fluctuation in nearby veins draining distant brain regions. Sci. Rep. 2015, 5:10499. 10.1038/srep10499.
13. Britton J.C., Phan K.L., Taylor S.F., Fig L.M., Liberzon I. Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biol. Psychiatry 2005, 57:832-840. 10.1016/j.biopsych.2004.12.025.
14. Brown V.M., LaBar K.S., Haswell C.C., Gold A.L., Mid-Atlantic-MIRECC-Workgroup, McCarthy G., Morey R.A. Altered resting-state functional connectivity of basolateral and centromedial amygdala complexes in posttraumatic stress disorder. Neuropsychopharmacology 2014, 39:351-359. 10.1038/npp.2013.197.
15. Buchanan T.W., Tranel D. Stress and emotional memory retrieval: Effects of sex and cortisol response. Neurobiol. Learn. Mem. 2008, 89:134-141. 10.1016/j.nlm.2007.07.003.Stress.
16. Cahill L. Why sex matters for neuroscience. Nat. Rev. Neurosci. 2006, 7:477-484. 10.1038/nrn1909.
17. Caspers S., Geyer S., Schleicher A., Mohlberg H., Amunts K., Zilles K. The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. NeuroImage 2006, 33:430-448.
18. Cavanna A.E., Trimble M.R. The Precuneus: A Review of Its Functional Anatomy and Behavioural Correlates 2006, 564-583. 10.1093/brain/awl004.
19. Chung K.C., Peisen F., Kogler L., Radke S., Turetsky B.I., Freiherr J., Derntl B. The influence of menstrual cycle and androstadienone on female stress reaction: an fMRI study. Front. Hum. Neurosci. 2016.
20. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joëls M. Brain corticosteroid receptor balance in health and disease*. Endocr. Rev. 1998, 19:269-301.
21. Derntl B., Habel U., Windischberger C., Robinson S., Kryspin-Exner I., Gur R.C., Moser E. General and specific responsiveness of the amygdala during explicit emotion recognition in females and males. BMC Neurosci. 2009, 10:1-14. 10.1186/1471-2202-10-91.
22. Derntl B., Windischberger C., Robinson S., Lamplmayr E., Kryspin-exner I., Gur R.C. Facial Emotion Recognition and Amygdala Activation are Associated with Menstrual Cycle Phase 2008, 10.1016/j.psyneuen.2008.04.014.
23. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004, 130:355-391. 10.1037/0033-2909.130.3.355.
24. Diorio D., Viau V., Meaney J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 1993, 13:3839-3847.
25. 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. 10.1002/hbm.20903.
26. Duchesne A., Pruessner J.C. Association between subjective and cortisol stress response depends on the menstrual cycle phase. Psychoneuroendocrinology 2013, 38:3155-3159. 10.1016/j.psyneuen.2013.08.009.
27. Eickhoff S.B., Müller V.I. Functional connectivity. Brain Mapping-An Encyclopedic Reference. Volume 2: Anatomy and Physiology, Systems 2015, 187-201.
28. Eickhoff S.B., Amunts K., Mohlberg H., Zilles K. The human parietal operculum. II. Stereotaxic maps and correlations with functional imaging results. Cereb. Cortex 2006, 16:268-279.
29. Eickhoff S.B., Jbabdi S., Caspers S., Laird A.R., Fox P.T., Zilles K., Behrens T.E.J. Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J. Neurosci. 2010, 30:6409-6421. 10.1523/JNEUROSCI.5664-09.2010.
30. Eickhoff S.B., Schleicher A., Zilles K., Amunts K. The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cereb. Cortex 2006, 16:254-267.
31. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 2005, 25:1325-1335. 10.1016/j.neuroimage.2004.12.034.
32. Engert V., Smallwood J., Singer T. Mind your thoughts: associations between self-generated thoughts and stress-induced and baseline levels of cortisol and alpha-amylase. Biol. Psychol. 2014, 103:283-291. 10.1016/j.biopsycho.2014.10.004.
33. Engman J., Linnman C., Van Dijk K.R.A., Milad M.R. Amygdala subnuclei resting-state functional connectivity sex and estrogen differences. Psychoneuroendocrinology 2016, 63:34-42. 10.1016/j.psyneuen.2015.09.012.
34. Evans G.W., Swain J.E., King A.P., Wang X., Javanbakht A., Ho S.S., Angstadt M., Phan K.L., Xie H., Liberzon I. Childhood cumulative risk exposure and adult amygdala volume and function. J. Neurosci. Res. 2015, 10.1002/jnr.23681.
35. Forni-Santos L., Osório F.L. Influence of gener in the recognition of basic facial expression: A critical literature review. World J. Psychiatry 2015, 5:342-351. 10.5498/wjp.v5.i3.342.
36. Fox K.C.R., Spreng R.N., Ellamil M., Andrews-Hanna J.R., Christoff K. The wandering brain: meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes. NeuroImage 2015, 111:611-621. 10.1016/j.neuroimage.2015.02.039.
37. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S.J. Functional connectivity: The principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab. 1993, 13:5-14.
38. Giedd J.N., Raznahan A., Mills K.L., Lenroot R.K. Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biol. Sex Differ. 2012, 3:1. 10.1186/2042-6410-3-19.
39. Goldin P.R., Manber-ball T., Werner K., Heimberg R., Gross J.J. Neural mechanisms of cognitive reappraisal of negative self-beliefs in social anxiety disorder. BPS 2009, 66:1091-1099. 10.1016/j.biopsych.2009.07.014.
40. Grossman M., Wood W. Sex differences in intensity of emotional experience: a social role interpretation. J. Pers. Soc. Psychol. 1993, 65:1010-1022.
41. Habel U., Klein T.M., Kellermann T., Shah N.J., Schneider F. Same or different? Neural correlates of happy and sad mood in healthy males. NeuroImage 2005, 26:206-214. 10.1016/j.neuroimage.2005.01.014.
42. Hartley C.A., Phelps E.A. Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacol. Rev. 2010, 35:136-146. 10.1038/npp.2009.121.
43. Henckens M.J.A.G., Van Wingen G.A., Joe M. Time-dependent effects of corticosteroids on human amygdala processing. J. Neurosci. 2010, 30:12725-12732. 10.1523/JNEUROSCI.3112-10.2010.
44. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernández G. Time-dependent effects of cortisol on selective attention and emotional interference: a functional MRI study. Front. Integr. Neurosci. 2012, 6:66. 10.3389/fnint.2012.00066.
45. Hidalgo V., Pulopulos M.M., Puig-Perez S., Espin L., Gomez-Amor J., Salvador A. Acute stress affects free recall and recognition of pictures differently depending on age and sex. Behav. Brain Res. 2015, 292:393-402. 10.1016/j.bbr.2015.07.011.
46. Holmes C.J., Hoge R., Collins L., Woods R., Toga A.W. Enhancement of MR images using registration for signal averaging. J. Comput. Assist. Tomogr. 1998, 22:324-333.
47. Jabbi M., Swart M., Keysers C. Empathy for positive and negative emotions in the gustatory cortex 2007, 34:1744-1753. 10.1016/j.neuroimage.2006.10.032.
48. Kajantie E., Phillips D.I.W. The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 2006, 31:151-178. 10.1016/j.psyneuen.2005.07.002.
49. Kirschbaum C., Kudielka B.M., Gaab J., Schommer N.C., Hellhammer D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 1999, 61:154-162.
50. Kirschbaum C., Wüst S., Hellhammer D. Consistent sex differences in cortisol responses to psychological stress. Psychosom. Med. 1992, 54:648-657.
51. Kloet E.R.De, Joëls M., Holsboer F. Stress and the brain: from adaption to disease. Nat. Rev. Neurosci. 2005, 6:463-475. 10.1038/nrn1683.
52. Kogler L., Gur R.C., Derntl B. Sex differences in cognitive regulation of psychosocial achievement stress: brain and behavior. Hum. Brain Mapp. 2015, 36:1028-1042. 10.1002/hbm.22683.
53. Kogler L., Müller V.I., Chang A., Eickhoff S.B., Fox P.T., Gur R.C., Derntl B. Psychosocial versus physiological stress-meta-analyses on the deactivations and activations of the neural correlates of stress reactions. Neuroimage 2015.
54. Kring A.M., Gordon A.H. Sex differences in emotion: expression, experience, and physiology. J. Pers. Soc. Psychol. 1998, 74:686-703.
55. Kudielka B.M., Hellhammer J., Hellhammer D.H., Wolf O.T., Pirke K.M., Varadi E., Pilz J., Kirschbaum C. Sex differences in endocrine and psychological responses to psychosocial stress in healthy elderly subjects and the impact of a 2-week dehydroepiandrosterone treatment. J. Clin. Endocrinol. Metab. 1998, 83:1756-1761. 10.1210/jc.83.5.1756.
56. Kühn S., Vanderhasselt M.-A., De Raedt R., Gallinat J. The neural basis of unwanted thoughts during resting state. Soc. Cogn. Affect. Neurosci. 2014, 9:1320-1324. 10.1093/scan/nst117.
57. Lee T., Josephs O., Dolan R.J., Critchley H.D. Imitating expressions: emotion-specific neural substrates in facial mimicry. Soc. Cogn. Affect. Neurosci. 2006, 122-135. 10.1093/scan/nsl012.
58. Longe O., Randall B., Stamatakis E.A., Tyler L.K. Grammatical categories in the brain: the role of morphological structure. Cereb. Cortex 2007, 17:1812-1820. 10.1093/cercor/bhl099.
59. Lonsdorf T.B., Haaker J., Schümann D., Sommer T., Bayer J., Brassen S., Bunzeck N., Gamer M., Kalisch R. Sex differences in conditioned stimulus discrimination during context-dependent fear learning and its retrieval in humans: the role of biological sex, contraceptives and menstrual cycle phases. J. Psychiatry Neurosci. 2015, 40:140336. 10.1503/140336.
60. Lopez-Larson M.P., Anderson J.S., Ferguson M.A., Yurgelun-Todd D. Local brain connectivity and association with gender and age. Dev. Cogn. Neurosci. 2011, 1:187-197. 10.1016/j.dcn.2010.10.001.Local.
61. Luke K.-K., Liu H.-L., Wai Y.-Y., Wan Y.-L., Tan L.H. Functional anatomy of syntactic and semantic processing in language comprehension. Hum. Brain Mapp. 2002, 16:133-145. 10.1002/hbm.10029.
62. Lupien S.J., Parent S., Evans A.C., Tremblay R.E., David P., Corbo V. Larger Amygdala but No Change in Hippocampal Volume in 10-Year-Old Children Exposed to Maternal Depressive Symptomatology Since Birth I 2011, 10.1073/pnas.1105371108/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1105371108.
63. Maki P.M., Mordecai K.L., Rubin L.H., Sundermann E., Savarese A., Eatough E., Drogos L. Menstrual cycle effects on cortisol responsivity and emotional retrieval following a psychosocial stressor. Horm. Behav. 2015, 74:201-208. 10.1016/j.yhbeh.2015.06.023.
64. Maren S., Holmes A. Stress and fear extinction. Neuropsychopharmacol. Rev. 2015, 1-22. 10.1038/npp.2015.180.
65. Mason M.F., Norton M.I., Van Horn J.D., Wegner D.M., Grafton S.T., Macrae C.N. Wandering minds: the default network and stimulus-independent thoughts. Science 2007, 315:393-395.
66. McCarthy M.M., Arnold A.P., Ball G.F., Blaustein J.D., De Vries G.J. Sex differences in the brain: the not so inconvenient truth. J. Neurosci. 2012, 32:2241-2247. 10.1523/JNEUROSCI.5372-11.2012.Sex.
67. McEwen B.S., Gianaros P.J. Central role of the brain in stress and adaption: links to socioeconomic status, health, and disease. Ann. N. Y. Acad. Sci. 2010, 118611:190-222. 10.1111/j.1749-6632.2009.05331.x.Central.
68. McRae K., Ochsner K.N., Mauss I.B., Gabrieli J.J.D., Gross J.J. Gender differences in emotion regulation: an fMRI study of cognitive reappraisal. Group Process. Intergr. Relat. 2008, 11:143-162. 10.1177/1368430207088035.
69. Megreya A.M., Bindemann M., Havard C. Sex differences in unfamiliar face identification: evidence from matching tasks. Acta Psychol. 2011, 137:83-89. 10.1016/j.actpsy.2011.03.003.
70. Miller D.I., Halpern D.F. The new science of cognitive sex differences. Trends Cogn. Sci. 2014, 18:37-45. 10.1016/j.tics.2013.10.011.
71. Mogil J.S. Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon. Nat. Rev. Neurosci. 2012, 13:859-866. 10.1038/nrn3360.
72. Montoya E.R., Bos P.A., Terburg D., Rosenberger L.A., Van Honk J. Cortisol administration induces global down-regulation of the brain's reward circuitry. Psychoneuroendocrinology 2014, 47:31-42. 10.1016/j.psyneuen.2014.04.022.
73. Morin A., Hamper B. Self-reflection and the inner voice: activation of the left inferior frontal gyrus during perceptual and conceptual self-referential thinking. Open Neuroimaging J. 2012, 6:78-89. 10.2174/1874440001206010078.
74. Müller V.I., Cieslik E.C., Laird A.R., Fox P.T., Eickhoff S.B. Dysregulated left inferior parietal activity in schizophrenia and depression: functional connectivity and characterization. Front. Hum. Neurosci. 2013, 7:268. 10.3389/fnhum.2013.00268.
75. Müller V.I., Langner R., Cieslik E.C., Rottschy C., Eickhoff S.B. Interindividual differences in cognitive flexibility: influence of gray matter volume, functional connectivity and trait impulsivity. Brain Struct. Funct. 2015, 220:2401-2414. 10.1007/s00429-014-0797-6.
76. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. NeuroImage 2009, 44:893-905. 10.1016/j.neuroimage.2008.09.036.The.
77. Myers K.M., Davis M. Mechanisms of fear extinction. Mol. Psychiatry 2007, 12:120-150. 10.1038/sj.mp.4001939.
78. Napadow V., LaCount L., Park K., As-Sanie S., Clauw D.J., Harris R.E. Intrinsic brain connectivity in fibromyalgia is associated with chronic pain intensity. Arthritis Rheum. 2010, 62:2545-2555. 10.1002/art.27497.Intrinsic.
79. Neufang S., Specht K., Hausmann M., Konrad K. Sex differences and the impact of steroid hormones on the developing human brain. Cereb. Cortex 2009, 19:464-473. 10.1093/cercor/bhn100.
80. Nolen-Hoeksema S. Emotion regulation and psychopathology: the role of gender. Annu. Rev. Clin. Psychol. 2012, 8:161-187. 10.1146/annurev-clinpsy-032511-143109.
81. Ochsner K.N., Ray R.D., Cooper J.C., Robertson E.R., Chopra S., Gabrieli J.D.E., Gross J.J. For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 2004, 23:483-499. 10.1016/j.neuroimage.2004.06.030.
82. Pape H.-C., Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev. 2010, 90:419-463. 10.1152/physrev.00037.2009.Plastic.
83. Petersen N., Kilpatrick L.A., Goharzad A., Cahill L. Oral contraceptive pill use and menstrual cycle phase are associated with altered resting state functional connectivity. NeuroImage 2014, 90:24-32. 10.1016/j.neuroimage.2013.12.016.
84. Pletzer B., Kronbichler M., Aichhorn M., Bergmann J., Ladurner G., Kerschbaum H.H. Menstrual cycle and hormonal contraceptive use modulate human brain structure. Brain Res. 2010, 1348:55-62. 10.1016/j.brainres.2010.06.019.
85. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 2012, 59:2142-2154. 10.1016/j.neuroimage.2011.10.018.Spurious.
86. Quaedflieg C.W.E.M., van de Ven V., Meyer T., Siep N., Merckelbach H., Smeets T. Temporal dynamics of stress-induced alternations of intrinsic amygdala connectivity and neuroendocrine levels. PLoS One 2015, 10. 10.1371/journal.pone.0124141.
87. Robinson J.L., Laird A.R., Glahn D.C., Lovallo W.R., Fox P.T. Meta-analytic connectivity modeling: delineating the functional of the human amygdala. Hum. Brain Mapp. 2011, 31:173-184. 10.1002/hbm.20854.Meta-analytic.
88. Robinson S., Moser E., Peper M. fMRI of emotion. FMRI techniques and protocols, neuromethods. Neuromethods 2009, 411-456.
89. Robinson S., Windischberger C., Rauscher A., Moser E. Optimized 3 T EPI of the amygdalae. NeuroImage 2004, 22:203-210. 10.1016/j.neuroimage.2003.12.048.
90. Robinson S.D., Pripfl J., H.B ., Moser E. The impact of EPI voxel size on SNR and BOLD sensitivity in the anterior medio-temporal lobe: a comparative group study of deactivation of the Default Mode. Magn. Reson. Mater. Phys. Biol. Med. 2008, 21:279-290.
91. Roy A.K., Shehzad Z., Margulies D.S., Kelly A.M.C., Uddin L.Q., Gotimer K., Biswal B.B., Castellanos F.X., Milham M.P. Functional connectivity of the human amygdala using resting state fMRI. NeuroImage 2010, 45:614-626. 10.1016/j.neuroimage.2008.11.030.Functional.
92. Ruigrok A.N., Salimi-Khorshidi G., Lai M.C., Baron-Cohen S., Lombardo M.V., Tait R.J., Suckling J. A meta-analysis of sex differences in human brain structure. Neurosci. Biobehav. Rev. 2014, 39:34-50.
93. Saad Z.S., Gotts S.J., Murphy K., Chen G., Jo H.J., Martin A., Cox R.W. Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2012, 2:25-32. 10.1089/brain.2012.0080.
94. Satterthwaite T.D., Elliott M., Gerraty R., Ruparel K., Loughead J., Calkin M.E., Eickhoff S.B., Hakonarson H., Gur R.C., Gur R.E., Wolf D.H. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. NeuroImage 2013, 64:240-256. 10.1016/j.neuroimage.2012.08.052.An.
95. Schilbach L., Bzdok D., Timmermans B., Fox P.T., Laird A.R., Vogeley K., Eickhoff S.B. Introspective minds: using ALE meta-analyses to study commonalities in the neural correlates of emotional processing, social & unconstrained cognition. PLoS One 2012, 7. 10.1371/journal.pone.0030920.
96. Schönberg T., Daw N.D., Joel D., O'Doherty J.P. Reinforcement learning signals in the human striatum distinguish learners from nonlearners during reward-based decision making. J. Neurosci. 2007, 27:12860-12867. 10.1523/JNEUROSCI.2496-07.2007.
97. Stein J.L., Wiedholz L.M., Bassett D.S., Weinberger D.R., Zink C.F., Mattay V.S., Meyer-Lindenberg A. A validated network of effective amygdala connectivity. NeuroImage 2007, 36:736-745. 10.1016/j.neuroimage.2007.03.022.
98. Stevens J.S., Hamann S. Sex differences in brain activation to emotional stimuli: a meta-analysis of neuroimaging studies. Neuropsychologia 2012, 50:1578-1593. 10.1016/j.neuropsychologia.2012.03.011.
99. Strathearn L., Li J., Fonagy P., Montague P.R. What's in a smile? Maternal brain responses to infant facial cues. Pediatrics 2008, 122:40-51. 10.1542/peds.2007-1566.What.
100. Tamres L., Janicki D., Helgeson V. Sex differences in coping behavior: a meta-analytic review and an examination of relative coping. Personal. Soc. Psychol. Rev. 2002, 6:2-30. 10.1207/S15327957PSPR0601.
101. Taylor S.E., Klein L.C., Lewis B.P., Gruenewald T.L., Gurung R.A.R., Updegraff J.A. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol. Rev. 2000, 107:411-429.
102. Tottenham N., Hare T.A., Quinn B.T., McCarry T.W., Nurse M., Gilhooly T., Milner A., Galvan A., Davidson M.C., Eigsti I.-M., Thomas K.M., Freed P., Booma E.S., Gunnar M., Altemus M., Aronson J., Casey B.J. Prolonged institutional rearing is associated with atypically larger amygdala volume and difficulties in emotion regulation. Dev. Sci. 2010, 13:1-26. 10.1111/j.1467-7687.2009.00852.x.Prolonged.
103. Trapnell P.D., Campbell J.D. Private self-consciousness and the five-factor model of personality: distinguishing rumination from reflection. J. Pers. Soc. Psychol. 1999, 76:284-304.
104. Turner J., Laird A. The cognitive paradigm ontology: design and application. Neuroinformatics 2012, 10:57-66. 10.1007/s12021-011-9126-x.The.
105. Tusche A., Smallwood J., Bernhardt B.C., Singer T. Classifying the wandering mind: revealing the affective content of thoughts during task-free rest periods. NeuroImage 2014, 97:107-116. 10.1016/j.neuroimage.2014.03.076.
106. Ulrich-Lai Y., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 2009, 10:397-409. 10.1016/j.biotechadv.2011.08.021.Secreted.
107. Urry H.L., van Reekum C.M., Johnstone T., Kalin N.H., Thurow M.E., Schaefer H.S., Jackson C.a., Frye C.J., Greischar L.L., Alexander A.L., Davidson R.J. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J. Neurosci. 2006, 26:4415-4425. 10.1523/JNEUROSCI.3215-05.2006.
108. Vaisvaser S., Lin T., Admon R., Podlipsky I., Greenman Y., Stern N., Fruchter E., Wald I., Pine D.S., Tarrasch R., Bar-Haim Y., Hendler T. Neural traces of stress: cortisol related sustained enhancement of amygdala-hippocampal functional connectivity. Front. Hum. Neurosci. 2013, 7:313. 10.3389/fnhum.2013.00313.
109. Veer I.M., Oei N.Y.L., Spinhoven P., van Buchem M.a., Elzinga B.M., Rombouts S.a.R.B. Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures. NeuroImage 2011, 57:1534-1541. 10.1016/j.neuroimage.2011.05.074.
110. Veer I.M., Oei N.Y.L., Spinhoven P., Van Buchem M.A., Elzinga B.M., Rombouts S.A.R.B. Endogenous cortisol is associated with functional connectivity between the amygdala and medial prefrontal cortex. Psychoneuroendocrinology 2012, 37:1039-1047. 10.1016/j.psyneuen.2011.12.001.
111. Vogel S., Klumpers F., Krugers H.J., Fang Z., Oplaat K.T., Oitzl M.S., Joëls M., Fernández G. Blocking the mineralocorticoid receptor in humans prevents the stress-induced enhancement of centromedial amygdala connectivity with the dorsal striatum. Neuropsychopharmacology 2015, 40:947-956. 10.1038/npp.2014.271.
112. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: The PANAS scales. J. Pers. Soc. Psychol. 1988, 54:1063-1070.
113. Weissenbacher A., Kasess C., Gerstl F., Lanzenberger R., Moser E., Windischberger C. Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. NeuroImage 2009, 47:1408-1416. 10.1016/j.neuroimage.2009.05.005.
114. Winston J.S., Doherty J.O., Kilner J.M., Perrett D.I., Dolan R.J. Brain systems for assessing facial attractiveness. Neuropsychologia 2007, 45:195-206. 10.1016/j.neuropsychologia.2006.05.009.
115. Wolf O.T., Schommer N.C., Hellhammer D.H., McEwen B.S., Kirschbaum C. The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 2001, 26:711-720.
116. World Health Organization Gender in Mental Health Research 2004, World Heal. Organ, Geneva.