Oxytocin's effect on resting-state functional connectivity varies by age and sex

Psychoneuroendocrinology

Volumn 69, Issue , 2016, Pages 50-59

  Ebner, Natalie C ^a,b   Chen, Huaihou ^b,c   Porges, Eric ^b   Lin, Tian ^a   Fischer, Håkan ^d   Feifel, David ^e   Cohen, Ronald A ^b  

^a University of Florida   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Amygdala; Medial prefrontal cortex; Oxytocin; Resting state functional connectivity; Sex

Indexed keywords

OXYTOCIN; PLACEBO;

ABSENCE OF SIDE EFFECTS; ADULT; AGE; AGED; AMYGDALOID NUCLEUS; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG SELF ADMINISTRATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MEDIAL PREFRONTAL CORTEX; NORMAL HUMAN; PRIORITY JOURNAL; RESTING STATE FUNCTIONAL CONNECTIVITY; RESTING STATE NETWORK; SEX DIFFERENCE; AMYGDALA; BRAIN; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; IMAGE PROCESSING; INTRANASAL DRUG ADMINISTRATION; MEMBRANE POTENTIAL; METABOLISM; MIDDLE AGED; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX;

ADMINISTRATION, INTRANASAL; ADULT; AGE FACTORS; AMYGDALA; BRAIN; DOUBLE-BLIND METHOD; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMBRANE POTENTIALS; MIDDLE AGED; NEURAL PATHWAYS; OXYTOCIN; PREFRONTAL CORTEX; SEX FACTORS;

EID: 84961627413     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2016.03.013     Document Type: Article

References (70)

1. Akaishi T., Sakuma Y. Estrogen excites oxytocinergic: but not vasopressinergic cells in the paraventricular nucleus of female rat hypothalamus. Brain Res. 1985, 335:302-305.
2. Altemus M., Jacobson K.R., Debellis M., Kling M., Pigott T., Murphy D.L., Gold P.W. Normal CSF oxytocin and NPY levels in OCD. Biol. Psychiatry 1999, 45:931-933.
3. Andari E., Duhamel J., Zalla T., Herbrecht E., Leboyer M., Sirigu A. Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc. Natl. Acad. Sci. U. S. A 2010, 107:4389-4394.
4. Bale T.L., Dorsa D.M. Cloning, novel promoter sequence, and estrogen regulation of a rat oxytocin receptor gene. Endocrinology 1997, 138:1151-1158.
5. Banks S.J., Eddy K.T., Angstadt M., Nathan P.J., Phan K.L. Amygdala-frontal connectivity during emotion regulation. Soc. Cogn. Affect. Neurosci. 2007, 2:303-312.
6. Bartz J.A., Zaki J., Bolger N., Hollander E., Ludwig N.N., Kolevzon A., Ochsner K.N. Oxytocin selectively improves empathic accuracy. Psychol. Sci. 2010, 21:1426-1428.
7. Bartz J.A., Zaki J., Bolger N., Ochsner K.N. Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 2011, 15:301-309.
8. Baumgartner T., Heinrichs M., Vonlanthen A., Fischbacher U., Fehr E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 2008, 58:639-650.
9. Behzadi Y., Restom K., Liau J., Liu T.T. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 2007, 37:90-101.
10. Bethlehem R.A.I., van Honk J., Auyeung B., Baron-Cohen S. Oxytocin, brain physiology, and functional connectivity: a review of intranasal oxytocin fMRI studies. Psychoneuroendocrinology 2013, 38:962-974.
11. Bickart K.C., Hollenbeck M.C., Barrett L.F., Dickerson B.C. Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. J. Neurosci. 2012, 32:14729-14741.
12. Birn R.M., Molloy E.K., Patriat R., Parker T., Meier T.B., Kirk G.R., Nair V.A., Meyerand M.E., Prabhakaran V. The effect of scan length on the reliability of resting-state fMRI connectivity estimates. Neuroimage 2013, 83:550-558.
13. Born J., Lange T., Kern W., McGregor G.P., Bickel U., Fehm H.L. Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 2002, 5:514-516.
14. Bos P.A., Panksepp J., Bluthé R., van Honk J. Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front. Neuroendocrinol. 2012, 33:17-35.
15. Brandt J., Spencer M., Folstein M. The telephone interview for cognitive status. Neuropsychiatry Neuropsychol. Behav. Neurol. 1988, 1:111-117.
16. Braun U., Plichta M.M., Esslinger C., Sauer C., Haddad L., Grimm O., Mier D., Mohnke S., Heinz A., Erk S., Walter H. Test-retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures. Neuroimage 2012, 59:1404-1412.
17. Campbell A., Ruffman T., Murray J.E., Glue P. Oxytocin improves emotion recognition for older males. Neurobiol. Aging 2014, 35:2246-2248.
18. Carter C.S. Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders?. Behav. Brain Res. 2007, 176:170-186.
19. Champagne F., Diorio J., Sharma S., Meaney M.J. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc. Natl. Acad. Sci. 2001, 98:12736-12741.
20. Dadds M.R., Moul C., Cauchi A., Dobson-Stone C., Hawes D.J., Brennan J., Ebstein R.E. Methylation of the oxytocin receptor gene and oxytocin blood levels in the development of psychopathy. Dev. Psychopathol. 2014, 26:33-40.
21. De Dreu C.K.W. Oxytocinergic circuitry motivates group loyalty. Mechanisms of Social Connection: From Brain to Group 2014, American Psychological Association, Washington DC, US, pp. 391-407. M. Mikulincer, R.P. Shaver (Eds.).
22. Desikan R.S., Ségonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Buckner R.L., Dale A.M., Maguire R.P., Hyman B.T., Albert M.S., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
23. Dodhia S., Hosanagar A., Fitzgerald D.A., Labuschagne I., Wood A.G., Nathan P.J., Phan K.L. Modulation of resting-state amygdala-frontal functional connectivity by oxytocin in generalized social anxiety disorder. Neuropsychopharmacology 2014, 39:2061-2069.
24. Domes G., Heinrichs M., Gläscher J., Büchel C., Braus D.F., Herpertz S.C. Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol. Psychiatry 2007, 62:1187-1190.
25. Domes G., Lischke A., Berger C., Grossmann A., Hauenstein K., Heinrichs M., Herpertz S.C. Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 2010, 35:83-93.
26. Dunbar R.I.M. The social brain hypothesis. Evol. Anthropol. 1998, 6:178-190.
27. Ebner N.C., Maura G.M., MacDonald K., Westberg L., Fischer H. Oxytocin and socioemotional aging: current knowledge and future trends. Front. Hum. Neurosci. 2013, 7:487.
28. Ebner N.C., Horta M., Lin T., Fischer H., Cohen R.A., Feifel D. Oxytocin modulates meta-mood as a function of age and sex. Front. Aging Neurosci. 2015, 7:175.
29. Ebner N.C., Kamin H., Diaz V., Cohen R.A., MacDonald K. Hormones as difference makers in cognitive and socioemotional aging processes. Front. Emot. Sci. 2015, 5:1595.
30. Ellenbogen M.A., Linnen A.M., Cardoso C., Joober R. Intranasal oxytocin attenuates the human acoustic startle response independent of emotional modulation. Psychophysiology 2014, 51:1169-1177.
31. Fan Y., Herrera-Melendez A.L., Pestke K., Feeser M., Aust S., Otte C., Pruessner J.C., Böker H., Bajbouj M., Grimm S. Early life stress modulates amygdala-prefrontal functional connectivity: implications for oxytocin effects. Hum. Brain Mapp. 2014, 35:5328-5339.
32. Farmer J., Reupert A. Understanding autism and understanding my child with autism: an evaluation of a group parent education program in rural Australia. Aust. J. Rural Health 2013, 21:20-27.
33. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
34. Frazier J.A., Chiu S., Breeze J.L., Makris N., Lange N., Kennedy D.N., Herbert M.R., Bent E.K., Koneru V.K., Dieterich M.E., Hodge S.M., Rauch S.L., Grant P.E., Cohen B.M., Seidman L.J., Caviness V.S., Biederman J. Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. Am. J. Psychiatry 2005, 162:1256-1265.
35. Gimpl G., Fahrenholz F. The oxytocin receptor system structure, function, and regulation. Physiol. Rev. 2001, 81:629-683.
36. Goldstein J.M., Seidman L.J., Makris N., Ahern T., O'Brien L.M., Caviness V.S., Kennedy D.N., Faraone S.V., Tsuang M.T. Hypothalamic abnormalities in schizophrenia: sex effects and genetic vulnerability. Biol. Psychol. 2007, 61:935-945.
37. Gosling S.D., Rentfrow P.J., Swann W.B. A very brief measure of the big-five personality domains. J. Res. Personality 2003, 37:504-528.
38. Guastella A.J., Hickie I.B., McGuinness M.M., Otis M., Woods E.A., Disinger H.M., Chan H., Chen T.F., Banati R.B. Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology 2013, 38:612-625.
39. Gur R., Mozley L., Mozley P., Resnick S., Karp J., Alavi A., Arnold S. Sex differences in regional cerebral glucose metabolism during a resting state. Science 1995, 267:528-531.
40. Huang C., Hsieh W., Lee P., Peng L., Liu L., Lee W., Huang J., Chen L., Lin C. Age-related changes in resting-state networks of a large sample size of healthy elderly. CNS Neurosci. Ther. 2015, 21(10):817-825. First Published Online. http://onlinelibrary.wiley.com/doi/10.1111/cns.2015.21.issue-10/issuetoc.
41. Huber D., Veinante P., Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 2005, 308:245-248.
42. Huffmeijer R., van Ijzendoorn M.H., Bakermans-Kranenburg M.J. Ageing and oxytocin: a call for extending human oxytocin research to ageing populations-a mini-review. Gerontology 2013, 59:32-39.
43. Hutchison R.M., Womelsdorf T., Allen E.A., Bandettini P.A., Calhoun V.D., Corbetta M., Della Penna S., Duyn J.H., Glover G.H., Gonzalez-Castillo J., Handwerker D.A. Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage 2013, 80:360-378.
44. Insel T.R. The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 2010, 65:768-779.
45. Kanat M., Heinrichs M., Domes G. Oxytocin and the social brain: neural mechanisms and perspectives in human research. Brain Res. 2014, 1580:160-171.
46. Kirsch P., Esslinger C., Chen Q., Mier D., Lis S., Siddhanti S., Gruppe H., Mattay V.S., Gallhofer B., Meyer-Lindenberg A. Oxytocin modulates neural circuitry for social cognition and fear in humans. J. Neurosci. 2005, 25:11489-11493.
47. Kovács B., Kéri S. Off-label intranasal oxytocin use in adults is associated with increased amygdala-cingulate resting-state connectivity. Eur. Psychiatry 2015, 30:542-547.
48. Kumar J., Vollm B., Palaniyappan L. Oxytocin affects the connectivity of the precuneus and the amygdala a randomized, double-blinded, placebo-controlled neuroimaging trial. Int. J. Neuropsychopharmacol. 2015, 18:1-7.
49. Lischke A., Gamer M., Berger C., Grossmann A., Hauenstein K., Heinrichs M., Herpertz S.C., Domes G. Oxytocin increases amygdala reactivity to threatening scenes in females. Psychoneuroendocrinology 2012, 37:1431-1438.
50. Macdonald K., Feifel D. Oxytocin in schizophrenia: a review of evidence for its therapeutic effects. Acta Neuropsychiatr. 2012, 24:130-146.
51. Macdonald K.S. Sex, receptors, and attachment: a review of individual factors influencing response to oxytocin. Front. Neurosci. 2013, 6:194.
52. Makris N., Goldstein J.M., Kennedy D., Hodge S.M., Caviness V.S., Faraone S.V., Tsuang M.T., Seidman L.J. Decreased volume of left and total anterior insular lobule in schizophrenia. Schizophr. Res. 2006, 83:155-171.
53. Meyer-Lindenberg A., Domes G., Kirsch P., Heinrichs M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 2011, 12:524-538.
54. Pedersen C.A., Caldwell J.D., Walker C., Ayers G., Mason G.A. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 1994, 108:1163-1171.
55. Pessoa L. On the relationship between emotion and cognition. Nat. Rev. Neurosci. 2008, 9:148-158.
56. Petrovic P., Kalisch R., Singer T., Dolan R.J. Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J. Neurosci. 2008, 28:6607-6615.
57. 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.
58. Prater K.E., Hosanagar A., Klumpp H., Angstadt M., Phan K.L. Aberrant amygdala-frontal cortex connectivity during perception of fearful faces and at rest in generalized social anxiety disorder. Depress. Anxiety 2013, 30:234-241.
59. Quiñones-Jenab V., Jenab S., Ogawa S., Adan R.A., Burbach J.P.H., Pfaff D.W. Effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the uterus, pituitary, and forebrain of the female rat. Neuroendocrinology 1997, 65:9-17.
60. Rey A. Lexamen Clinique en Psychologie 1964, Presses Universitaires de France.
61. Riem M.M.E., van IJzendoorn M.H., Tops M., Boksem M.A.S., Rombouts S.A.R.B., Bakermans-Kranenburg M.J. Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal. Eur. Neuropsychopharmacol. 2013, 23:1288-1295.
62. Rilling J.K., DeMarco A.C., Hackett P.D., Chen X., Gautam P., Stair S., Haroon E., Thompson R., Ditzen B., Patel R., Pagnoni G. Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction. Psychoneuroendocrinology 2014, 39:237-248.
63. Sergerie K., Chochol C., Armony J.L. The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 2008, 32:811-830.
64. Sripada C.S., Phan K.L., Labuschagne I., Welsh R., Nathan P.J., Wood A.G. Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex. Int. J. Neuropsychopharmacol. 2013, 16:255-260.
65. Vasudevan N., Davidkova G., Zhu Y.S., Koibuchi N., Chin W.W., Pfaff D. Differential interaction of estrogen receptor and thyroid hormone receptor isoforms on the rat oxytocin receptor promoter leads to differences in transcriptional regulation. Neuroendocrinology 2001, 74:309-324.
66. 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.
67. Wechsler D. WAIS-R: Manual: Wechsler Adult Intelligence Scale-Revised 1981, Psychological Corporation, New York.
68. Wei M., Russell D.W., Mallinckrodt B., Vogel D.L. The experiences in close relationship scale (ECR)-short form: reliability, validity, and factor structure. J. Pers. Assess. 2007, 88:187-204.
69. Whitfield-Gabrieli S., Nieto-Castanon A. Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012, 2:125-141.
70. Young L.J., Wang Z., Donaldson R., Rissman E.F. Estrogen receptor α is essential for induction of oxytocin receptor by estrogen. Neuroreport 1998, 9:933-936.