Hormonal Cycles, Brain Network Connectivity, and Windows of Vulnerability to Affective Disorder

Trends in Neurosciences

Volumn 41, Issue 10, 2018, Pages 660-676

  Andreano, Joseph M ^a   Touroutoglou, Alexandra ^a   Dickerson, Brad ^a   Barrett, Lisa Feldman ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; HORMONE; PROGESTERONE;

AMYGDALA; ANXIETY DISORDER; DEPRESSION; DISEASE SEVERITY; ENDOCRINE SYSTEM; FUNCTIONAL CONNECTIVITY; HORMONE RELEASE; HUMAN; MEDIAL PREFRONTAL CORTEX; MEMORY; MENSTRUAL CYCLE; MOOD DISORDER; NEUROIMAGING; NONHUMAN; PANIC; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; STIMULUS RESPONSE; STRESS; AFFECT; ANIMAL; BRAIN MAPPING; NERVE TRACT; PHYSIOLOGY; PSYCHOLOGY;

AFFECT; ANIMALS; BRAIN MAPPING; HUMANS; MEMORY; MENSTRUAL CYCLE; MOOD DISORDERS; NEURAL PATHWAYS;

EID: 85052739698     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2018.08.007     Document Type: Review

References (122)

1. Kessler, R.C., et al. Sex and depression in the National Comorbidity Survey. II: cohort effects. J. Affect. Disord. 30 (1994), 15–26.
2. Regier, D.A., et al. The de facto US mental and addictive disorders service system. Epidemiologic catchment area prospective 1-year prevalence rates of disorders and services. Arch. Gen. Psychiatry 50 (1993), 85–94.
3. Breslau, N., The epidemiology of trauma, PTSD, and other posttrauma disorders. Trauma Violence Abuse 10 (2009), 198–210.
4. Kessler, R.C., et al. Posttraumatic stress disorder in the National Comorbidity Survey. Arch. Gen. Psychiatry 52 (1995), 1048–1060.
5. Luxton, D.D., et al. Gender differences in depression and PTSD symptoms following combat exposure. Depress. Anxiety 27 (2010), 1027–1033.
6. Altemus, M., et al. Sex differences in anxiety and depression clinical perspectives. Front. Neuroendocrinol. 35 (2014), 320–330.
7. van Wingen, G.A., et al. Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience 191 (2011), 38–45.
8. Breslau, J., et al. Sex differences in recent first-onset depression in an epidemiological sample of adolescents. Transl. Psychiatry, 7, 2017, e1139.
9. Bebbington, P.E., et al. The influence of age and sex on the prevalence of depressive conditions: report from the National Survey of Psychiatric Morbidity. Psychol. Med. 28 (1998), 9–19.
10. Patten, S.B., et al. The association between major depression prevalence and sex becomes weaker with age. Soc. Psychiatry Psychiatr. Epidemiol. 51 (2016), 203–210.
11. Stuart-Parrigon, K., Stuart, S., Perinatal depression: an update and overview. Curr. Psychiatry Rep., 16, 2014, 468.
12. Freeman, E.W., et al. Associations of hormones and menopausal status with depressed mood in women with no history of depression. Arch. Gen. Psychiatry 63 (2006), 375–382.
13. Endicott, J., The menstrual cycle and mood disorders. J. Affect. Disord. 29 (1993), 193–200.
14. Ling, F.W., Recognizing and treating premenstrual dysphoric disorder in the obstetric, gynecologic, and primary care practices. J. Clin. Psychiatry 61 (2000), 9–16.
15. Pinkerton, J.V., et al. Menstrual cycle-related exacerbation of disease. Am. J. Obstet. Gynecol. 203 (2010), 221–231.
16. Hsiao, M.C., et al. Premenstrual symptoms and premenstrual exacerbation in patients with psychiatric disorders. Psychiatry Clin. Neurosci. 58 (2004), 186–190.
17. McLeod, D.R., et al. The influence of premenstrual syndrome on ratings of anxiety in women with generalized anxiety disorder. Acta Psychiatr. Scand. 88 (1993), 248–251.
18. Holsen, L.M., et al. Stress response circuitry hypoactivation related to hormonal dysfunction in women with major depression. J. Affect. Disord. 131 (2011), 379–387.
19. Young, E.A., et al. Alteration in the hypothalamic-pituitary-ovarian axis in depressed women. Arch. Gen. Psychiatry 57 (2000), 1157–1162.
20. Skovlund, C.W., et al. Association of hormonal contraception with depression. JAMA Psychiatry 73 (2016), 1154–1162.
21. Skovlund, C.W., et al. Association of hormonal contraception with suicide attempts and suicides. Am. J. Psychiatry 175 (2018), 336–342.
22. Pletzer, B., et al. Menstrual cycle and hormonal contraceptive-dependent changes in intrinsic connectivity of resting-state brain networks correspond to behavioral changes due to hormonal status. Brain Connect. 6 (2016), 572–585.
23. Allen, A.M., et al. Determining menstrual phase in human biobehavioral research: a review with recommendations. Exp. Clin. Psychopharmacol. 24 (2016), 1–11.
24. Johnson, S., et al. Can apps and calendar methods predict ovulation with accuracy?. Curr. Med. Res. Opin. 34 (2018), 1587–1594.
25. Menon, V., Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. 15 (2011), 483–506.
26. Lindquist, K.A., et al. The brain basis of positive and negative affect: evidence from a meta-analysis of the human neuroimaging literature. Cereb. Cortex 26 (2016), 1910–1922.
27. Raz, G., et al. Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences. Cogn. Affect. Behav. Neurosci. 16 (2016), 709–723.
28. Brakowski, J., et al. Resting state brain network function in major depression – depression symptomatology, antidepressant treatment effects, future research. J. Psychiatr. Res. 92 (2017), 147–159.
29. Andrews-Hanna, J.R., et al. Functional-anatomic fractionation of the brain's default network. Neuron 65 (2010), 550–562.
30. Dickerson, B.C., et al. Prefrontal-hippocampal-fusiform activity during encoding predicts intraindividual differences in free recall ability: an event-related functional-anatomic MRI study. Hippocampus 17 (2007), 1060–1070.
31. Wager, T.D., et al. A Bayesian model of category-specific emotional brain responses. PLoS Comput. Biol., 11, 2015, e1004066.
32. Vogt, B.A., Midcingulate cortex: structure, connections, homologies, functions and diseases. J. Chem. Neuroanat. 74 (2016), 28–46.
33. Seeley, W.W., et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27 (2007), 2349–2356.
34. Gianaros, P.J., Wager, T.D., Brain–body pathways linking psychological stress and physical health. Curr. Dir. Psychol. Sci. 24 (2015), 313–321.
35. Touroutoglou, A., et al. Amygdala task-evoked activity and task-free connectivity independently contribute to feelings of arousal. Hum. Brain Mapp. 35 (2014), 5316–5327.
36. Andreano, J.M., et al. Resting connectivity between salience nodes predicts recognition memory. Soc. Cogn. Affect. Neurosci. 12 (2017), 948–955.
37. Kleckner, I.R., et al. Evidence for a large-scale brain system supporting allostasis and interoception in humans. Nat. Hum. Behav., 1, 2013, 0069.
38. van den Heuvel, M.P., Sporns, O., Network hubs in the human brain. Trends Cogn. Sci. 17 (2013), 683–696.
39. Kaiser, R.H., et al. Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry 72 (2015), 603–611.
40. Williams, L.M., Defining biotypes for depression and anxiety based on large-scale circuit dysfunction: a theoretical review of the evidence and future directions for clinical translation. Depress. Anxiety 34 (2017), 9–24.
41. Manoliu, A., et al. Insular dysfunction within the salience network is associated with severity of symptoms and aberrant inter-network connectivity in major depressive disorder. Front. Hum. Neurosci., 7, 2013, 930.
42. Koch, S.B., et al. Aberrant resting-state brain activity in posttraumatic stress disorder: a meta-analysis and systematic review. Depress. Anxiety 33 (2016), 592–605.
43. Li, W., et al. Amygdala network dysfunction in late-life depression phenotypes: relationships with symptom dimensions. J. Psychiatr. Res. 70 (2015), 121–129.
44. Cullen, K.R., et al. Abnormal amygdala resting-state functional connectivity in adolescent depression. JAMA Psychiatry 71 (2014), 1138–1147.
45. Hahn, A., et al. Reduced resting-state functional connectivity between amygdala and orbitofrontal cortex in social anxiety disorder. Neuroimage 56 (2011), 881–889.
46. Sripada, R.K., et al. Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. J. Psychiatry Neurosci. 37 (2012), 241–249.
47. Lanius, R.A., et al. Default mode network connectivity as a predictor of post-traumatic stress disorder symptom severity in acutely traumatized subjects. Acta Psychiatr. Scand. 121 (2010), 33–40.
48. Peters, A.T., et al. Aberrant resting-state functional connectivity in limbic and cognitive control networks relates to depressive rumination and mindfulness: a pilot study among adolescents with a history of depression. J. Affect. Disord. 200 (2016), 178–181.
49. Surguladze, S., et al. A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biol. Psychiatry 57 (2005), 201–209.
50. Anand, A., et al. Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biol. Psychiatry 57 (2005), 1079–1088.
51. Tan, G., et al. Heart rate variability (HRV) and posttraumatic stress disorder (PTSD): a pilot study. Appl. Psychophysiol. Biofeedback 36 (2011), 27–35.
52. Booij, S.H., et al. Chronicity of depressive problems and the cortisol response to psychosocial stress in adolescents: the TRAILS study. Psychoneuroendocrinology 38 (2013), 659–666.
53. Lopez-Duran, N.L., et al. HPA-axis stress reactivity in youth depression: evidence of impaired regulatory processes in depressed boys. Stress 18 (2015), 545–553.
54. Burke, H.M., et al. Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30 (2005), 846–856.
55. Herbert, J., Cortisol and depression: three questions for psychiatry. Psychol. Med. 43 (2013), 449–469.
56. Heim, C., et al. Pituitary–adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284 (2000), 592–597.
57. Yehuda, R., Status of glucocorticoid alterations in post-traumatic stress disorder. Ann. N. Y. Acad. Sci. 1179 (2009), 56–69.
58. Gaddy, M.A., Ingram, R.E., A meta-analytic review of mood-congruent implicit memory in depressed mood. Clin. Psychol. Rev. 34 (2014), 402–416.
59. Coles, M.E., et al. Memory bias for threat in generalized anxiety disorder: the potential importance of stimulus relevance. Cogn. Behav. Ther. 36 (2007), 65–73.
60. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders. 5th edn, 2013, American Psychiatric Association.
61. Scott, J.C., et al. A quantitative meta-analysis of neurocognitive functioning in posttraumatic stress disorder. Psychol. Bull. 141 (2015), 105–140.
62. Bixo, M., et al. Progesterone, 5alpha-pregnane-3,20-dione and 3alpha-hydroxy-5alpha-pregnane-20-one in specific regions of the human female brain in different endocrine states. Brain Res. 764 (1997), 173–178.
63. Bixo, M., et al. Estradiol and testosterone in specific regions of the human female brain in different endocrine states. J. Steroid Biochem. Mol. Biol. 55 (1995), 297–303.
64. Backstrom, T., et al. Allopregnanolone and mood disorders. Prog. Neurobiol. 113 (2014), 88–94.
65. Sripada, R.K., et al. The neurosteroids allopregnanolone and dehydroepiandrosterone modulate resting-state amygdala connectivity. Hum. Brain Mapp. 35 (2014), 3249–3261.
66. Syan, S.K., et al. Influence of endogenous estradiol, progesterone, allopregnanolone, and dehydroepiandrosterone sulfate on brain resting state functional connectivity across the menstrual cycle. Fertil. Steril., 107, 2017 1246–1255 e4.
67. De Bondt, T., et al. Stability of resting state networks in the female brain during hormonal changes and their relation to premenstrual symptoms. Brain Res. 1624 (2015), 275–285.
68. Hjelmervik, H., et al. Resting states are resting traits – an FMRI study of sex differences and menstrual cycle effects in resting state cognitive control networks. PLoS One, 9, 2014, e103492.
69. Lisofsky, N., et al. Hippocampal volume and functional connectivity changes during the female menstrual cycle. Neuroimage 118 (2015), 154–162.
70. Weis, S., et al. Dynamic changes in functional cerebral connectivity of spatial cognition during the menstrual cycle. Hum. Brain Mapp. 32 (2011), 1544–1556.
71. Petersen, N., et al. Oral contraceptive pill use is associated with localized decreases in cortical thickness. Hum. Brain Mapp. 36 (2015), 2644–2654.
72. Wetherill, R.R., et al. Influence of menstrual cycle phase on resting-state functional connectivity in naturally cycling, cigarette-dependent women. Biol. Sex Differ., 7, 2016, 24.
73. Engman, J., et al. Hormonal cycle and contraceptive effects on amygdala and salience resting-state networks in women with previous affective side effects on the pill. Neuropsychopharmacology 43 (2018), 555–563.
74. Thimm, M., et al. Menstrual cycle effects on selective attention and its underlying cortical networks. Neuroscience 258 (2014), 307–317.
75. van Wingen, G.A., et al. Progesterone selectively increases amygdala reactivity in women. Mol. Psychiatry 13 (2008), 325–333.
76. Makovac, E., et al. Alterations in amygdala–prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biol. Psychiatry 80 (2016), 786–795.
77. Ottowitz, W.E., et al. Evaluation of prefrontal-hippocampal effective connectivity following 24 hours of estrogen infusion: an FDG-PET study. Psychoneuroendocrinology 33 (2008), 1419–1425.
78. Chang, C., et al. Association between heart rate variability and fluctuations in resting-state functional connectivity. Neuroimage 68 (2013), 93–104.
79. Kiem, S.A., et al. Resting state functional MRI connectivity predicts hypothalamus-pituitary-axis status in healthy males. Psychoneuroendocrinology 38 (2013), 1338–1348.
80. Thomason, M.E., et al. Stress-induced activation of the HPA axis predicts connectivity between subgenual cingulate and salience network during rest in adolescents. J. Child Psychol. Psychiatry 52 (2011), 1026–1034.
81. Hakamata, Y., et al. Amygdala-centred functional connectivity affects daily cortisol concentrations: a putative link with anxiety. Sci. Rep., 7, 2017, 8313.
82. Ossewaarde, L., et al. Neural mechanisms underlying changes in stress-sensitivity across the menstrual cycle. Psychoneuroendocrinology 35 (2010), 47–55.
83. Gingnell, M., et al. Menstrual cycle effects on amygdala reactivity to emotional stimulation in premenstrual dysphoric disorder. Horm. Behav. 62 (2012), 400–406.
84. Andreano, J.M., Cahill, L., Menstrual cycle modulation of medial temporal activity evoked by negative emotion. Neuroimage 53 (2010), 1286–1293.
85. Ossewaarde, L., et al. Menstrual cycle-related changes in amygdala morphology are associated with changes in stress sensitivity. Hum. Brain Mapp. 34 (2013), 1187–1193.
86. Albert, K., et al. Estradiol levels modulate brain activity and negative responses to psychosocial stress across the menstrual cycle. Psychoneuroendocrinology 59 (2015), 14–24.
87. Goldstein, J.M., et al. Sex differences in stress response circuitry activation dependent on female hormonal cycle. J. Neurosci. 30 (2010), 431–438.
88. McKinley, P.S., et al. The impact of menstrual cycle phase on cardiac autonomic regulation. Psychophysiology 46 (2009), 904–911.
89. Sato, N., Miyake, S., Cardiovascular reactivity to mental stress: relationship with menstrual cycle and gender. J. Physiol. Anthropol. Appl. Hum. Sci. 23 (2004), 215–223.
90. Carter, J.R., Lawrence, J.E., Effects of the menstrual cycle on sympathetic neural responses to mental stress in humans. J. Physiol. 585 (2007), 635–641.
91. Carney, R.M., et al. Depression, heart rate variability, and acute myocardial infarction. Circulation 104 (2001), 2024–2028.
92. Childs, E., et al. Cardiovascular, hormonal, and emotional responses to the TSST in relation to sex and menstrual cycle phase. Psychophysiology 47 (2010), 550–559.
93. Kirschbaum, C., et al. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus–pituitary–adrenal axis. Psychosom. Med. 61 (1999), 154–162.
94. Andreano, J.M., et al. Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology 33 (2008), 874–882.
95. Ertman, N., et al. Progesterone at encoding predicts subsequent emotional memory. Learn. Mem. 18 (2011), 759–763.
96. Nielsen, S.E., et al. Postlearning stress differentially affects memory for emotional gist and detail in naturally cycling women and women on hormonal contraceptives. Behav. Neurosci. 128 (2014), 482–493.
97. Zoladz, P.R., et al. Post-learning stress enhances long-term memory and differentially influences memory in females depending on menstrual stage. Acta Psychol. (Amst.) 160 (2015), 127–133.
98. Felmingham, K.L., et al. The impact of progesterone on memory consolidation of threatening images in women. Psychoneuroendocrinology 37 (2012), 1896–1900.
99. Ferree, N.K., et al. Influences of menstrual cycle position and sex hormone levels on spontaneous intrusive recollections following emotional stimuli. Conscious. Cogn. 20 (2011), 1154–1162.
100. Soni, M., et al. Identification of a narrow post-ovulatory window of vulnerability to distressing involuntary memories in healthy women. Neurobiol. Learn. Mem. 104 (2013), 32–38.
101. Dolcos, F., et al. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42 (2004), 855–863.
102. Kilpatrick, L., Cahill, L., Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage. Neuroimage 20 (2003), 2091–2099.
103. Ritchey, M., et al. Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. Cereb. Cortex 18 (2008), 2494–2504.
104. Buchanan, T.W., Lovallo, W.R., Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26 (2001), 307–317.
105. Cahill, L., Alkire, M.T., Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiol. Learn. Mem. 79 (2003), 194–198.
106. Woolley, C.S., McEwen, B.S., Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336 (1993), 293–306.
107. Oyola, M.G., Handa, R.J., Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity. Stress 20 (2017), 476–494.
108. Graham, B.M., Daher, M., Estradiol and progesterone have opposing roles in the regulation of fear extinction in female rats. Neuropsychopharmacology 41 (2016), 774–780.
109. Rivera, R., et al. The mechanism of action of hormonal contraceptives and intrauterine contraceptive devices. Am. J. Obstet. Gynecol. 181 (1999), 1263–1269.
110. Klasen, F., et al. Risk and protective factors for the development of depressive symptoms in children and adolescents: results of the longitudinal BELLA study. Eur. Child Adolesc. Psychiatry 24 (2015), 695–703.
111. Harlow, B.L., Signorello, L.B., Factors associated with early menopause. Maturitas 35 (2000), 3–9.
112. Steiner, M., et al. Effect of fluoxetine on menstrual cycle length in women with premenstrual dysphoria. Obstet. Gynecol. 90 (1997), 590–595.
113. Yao, Z., et al. Gender differences in brain activity and the relationship between brain activity and differences in prevalence rates between male and female major depressive disorder patients: a resting-state fMRI study. Clin. Neurophysiol. 125 (2014), 2232–2239.
114. Fine, J.G., et al. Gender differences in BOLD activation to face photographs and video vignettes. Behav. Brain Res. 201 (2009), 137–146.
115. Ingalhalikar, M., et al. Sex differences in the structural connectome of the human brain. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 823–828.
116. Wang, G., et al. Sex differences in connectivity of the subgenual anterior cingulate cortex. Pain 155 (2014), 755–763.
117. Wrase, J., et al. Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study. Neurosci. Lett. 348 (2003), 41–45.
118. Hofer, P., et al. Testosterone in the brain: neuroimaging findings and the potential role for neuropsychopharmacology. Eur. Neuropsychopharmacol. 23 (2013), 79–88.
119. Rosenberg, L., Park, S., Verbal and spatial functions across the menstrual cycle in healthy young women. Psychoneuroendocrinology 27 (2002), 835–841.
120. Sherwin, B.B., Estrogen and cognitive functioning in women: lessons we have learned. Behav. Neurosci. 126 (2012), 123–127.
121. Barton, M., et al. Alike but not the same: anatomic heterogeneity of estrogen receptor-mediated vasodilation. J. Cardiovasc. Pharmacol. 62 (2013), 22–25.
122. Sun, F.W., et al. Youthful brains in older adults: preserved neuroanatomy in the default mode and salience networks contributes to youthful memory in superaging. J. Neurosci. 36 (2016), 9659–9668.