Oxytocin, brain physiology, and functional connectivity: A review of intranasal oxytocin fMRI studies

Psychoneuroendocrinology

Volumn 38, Issue 7, 2013, Pages 962-974

  Bethlehem, Richard A I ^a,c   van Honk, Jack ^a,b   Auyeung, Bonnie ^c   Baron Cohen, Simon ^c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amygdala; FMRI; Functional connectivity; Neural communication; Oxytocin; Social brain

Indexed keywords

DOPAMINE; OXYTOCIN; SEROTONIN; SEX HORMONE;

AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ANTERIOR INSULA; ANXIETY; ASSOCIATION CORTEX; BRAIN FUNCTION; BRAIN REGION; CAUDATE NUCLEUS; CEREBROSPINAL FLUID LEVEL; DOPAMINERGIC SYSTEM; DRUG HALF LIFE; DRUG MECHANISM; DRUG POTENTIATION; EMOTION; FEAR; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; INFERIOR FRONTAL GYRUS; LIMBIC CORTEX; MIDDLE TEMPORAL SULCUS; NERVE CELL NETWORK; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NONHUMAN; ORBITAL CORTEX; PARAHIPPOCAMPAL GYRUS; PHARMACODYNAMICS; PRECUNEUS; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SOCIAL BEHAVIOR; SUPRAMARGINAL GYRUS; VENTROMEDIAL PREFRONTAL CORTEX;

ADMINISTRATION, INTRANASAL; BRAIN; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; NERVE NET; OXYTOCIN;

EID: 84877921211     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.10.011     Document Type: Review

References (89)

1. Adolphs R., Tranel D., Damasio A.R. The human amygdala in social judgment. Nature 1998, 393:470-474.
2. Agnati L.F., Zoli M., Stromberg I., Fuxe K. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience 1995, 69:711-726.
3. Ashwin C., Chapman E., Colle L., Baron-Cohen S. Impaired recognition of negative basic emotions in autism: a test of the amygdala theory. Soc. Neurosci. 2006, 1:349-363.
4. Atzil S., Hendler T., Feldman R. Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers. Neuropsychopharmacology 2011, 36:2603-2615.
5. Bale T.L., Dorsa D.M. Regulation of oxytocin receptor messenger ribonucleic acid in the ventromedial hypothalamus by testosterone and its metabolites. Endocrinology 1995, 136:5135-5138.
6. Bale T.L., Dorsa D.M. Sex differences in and effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the ventromedial hypothalamus. Endocrinology 1995, 136:27-32.
7. Bale T.L., Pedersen C.A., Dorsa D.M. CNS oxytocin receptor mRNA expression and regulation by gonadal steroids. Adv. Exp. Med. Biol. 1995, 395:269-280.
8. Baron-Cohen S., Ring H.A., Bullmore E.T., Wheelwright S., Ashwin C., Williams S.C. The amygdala theory of autism. Neurosci. Biobehav. Rev. 2000, 24:355-364.
9. Baron-Cohen S., Wheelwright S., Hill J., Raste Y., Plumb I. The " Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J. Child Psychol. Psychiatry 2001, 42:241-251.
10. 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.
11. Baskerville T.A., Allard J., Wayman C., Douglas A.J. Dopamine-oxytocin interactions in penile erection. Eur. J. Neurosci. 2009, 30:2151-2164.
12. 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.
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., Bluthe R.M., Honk J.V. 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. Buijs R.M. Vasopressin and oxytocin-their role in neurotransmission. Pharmacol. Ther. 1983, 22:127-141.
16. Buijs R.M., De Vries G.J., Van Leeuwen F.W., Swaab D.F. Vasopressin and oxytocin: distribution and putative functions in the brain. Prog. Brain Res. 1983, 60:115-122.
17. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 1995, 19:303-314.
18. Carter C.S., Grippo A.J., Pournajafi-Nazarloo H., Ruscio M.G., Porges S.W. Oxytocin, vasopressin and sociality. Prog. Brain Res. 2008, 170:331-336.
19. De Dreu C.K., Greer L.L., Handgraaf M.J., Shalvi S., Van Kleef G.A. Oxytocin modulates selection of allies in intergroup conflict. Proc. Biol. Sci. 2012, 279:1150-1154.
20. De Dreu C.K., Greer L.L., Handgraaf M.J., Shalvi S., Van Kleef G.A., Baas M., Ten Velden F.S., Van Dijk E., Feith S.W. The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 2010, 328:1408-1411.
21. De Dreu C.K., Greer L.L., Van Kleef G.A., Shalvi S., Handgraaf M.J. Oxytocin promotes human ethnocentrism. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:1262-1266.
22. de Vries G.J. Sex differences in vasopressin and oxytocin innervation of the brain. Prog. Brain Res. 2008, 170:17-27.
23. de Vries G.J., Buijs R.M., Swaab D.F. Ontogeny of the vasopressinergic neurons of the supprachiasmatic nucleus and their extrahypothalamic projections in the rat brain - presence of a sex difference in the lateral septum. Brain Res. 1981, 218:67-78.
24. Domes G., Heinrichs M., Glascher J., Buchel 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., Heinrichs M., Michel A., Berger C., Herpertz S.C. Oxytocin improves " mind-reading" in humans. Biol. Psychiatry 2007, 61:731-733.
26. 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.
27. DSM Diagnostic and Statistical Manual of Mental Disorders: DSM-IV 1994, American Psychiatric Association, Washington, DC.
28. Du Vigneaud V., Ressler C., Swan J.M., Roberts C.W., Katsoyannis P.G., Gordon S. The synthesis of an octapeptide amide with hormonal activity of oxytocin. J. Am. Chem. Soc. 1953, 75:1.
29. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S. Functional connectivity: the principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab. 1993, 13:5-14.
30. Gabor C.S., Phan A., Clipperton-Allen A.E., Kavaliers M., Choleris E. Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav. Neurosci. 2012, 126:97-109.
31. Gamer M., Zurowski B., Buchel C. Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:9400-9405.
32. Gordon I., Martin C., Feldman R., Leckman J.F. Oxytocin and social motivation. Dev. Cogn. Neurosci. 2011, 1:471-493.
33. Hariri A.R., Tessitore A., Mattay V.S., Fera F., Weinberger D.R. The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 2002, 17:317-323.
34. Heinrichs M., von Dawans B., Domes G. Oxytocin, vasopressin, and human social behavior. Front. Neuroendocrinol. 2009, 30:548-557.
35. Hirasawa M., Schwab Y., Natah S., Hillard C.J., Mackie K., Sharkey K.A., Pittman Q.J. Dendritically released transmitters cooperate via autocrine and retrograde actions to inhibit afferent excitation in rat brain. J. Physiol. 2004, 559:611-624.
36. Huber D., Veinante P., Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 2005, 308:245-248.
37. Insel T.R., Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:5981-5985.
38. Insel T.R., Shapiro L.E. Oxytocin receptors and maternal behavior. Ann. N.Y. Acad. Sci. 1992, 652:122-141.
39. Ishak W.W., Kahloon M., Fakhry H. Oxytocin role in enhancing well-being: a literature review. J. Affect. Disord. 2011, 130:1-9.
40. Johnson A.E., Coirini H., Insel T.R., McEwen B.S. The regulation of oxytocin receptor binding in the ventromedial hypothalamic nucleus by testosterone and its metabolites. Endocrinology 1991, 128:891-896.
41. Kendrick K.M., Keverne E.B., Baldwin B.A. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 1987, 46:56-61.
42. Kendrick K.M., Keverne E.B., Baldwin B.A., Sharman D.F. Cerebrospinal fluid levels of acetylcholinesterase, monoamines and oxytocin during labour, parturition, vaginocervical stimulation, lamb separation and suckling in sheep. Neuroendocrinology 1986, 44:149-156.
43. Keverne E.B., Levy F., Poindron P., Lindsay D.R. Vaginal stimulation: an important determinant of maternal bonding in sheep. Science 1983, 219:81-83.
44. 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.
45. Knobloch H.S., Charlet A., Hoffmann L.C., Eliava M., Khrulev S., Cetin A.H., Osten P., Schwarz M.K., Seeburg P.H., Stoop R., Grinevich V. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 2012, 73:553-566.
46. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
47. Labuschagne I., Phan K.L., Wood A., Angstadt M., Chua P., Heinrichs M., Stout J.C., Nathan P.J. Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 2010, 35:2403-2413.
48. Labuschagne I., Phan K.L., Wood A., Angstadt M., Chua P., Heinrichs M., Stout J.C., Nathan P.J. Medial frontal hyperactivity to sad faces in generalized social anxiety disorder and modulation by oxytocin. Int. J. Neuropsychopharmacol. 2011, 1-14.
49. Landgraf R., Neumann I.D. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 2004, 25:150-176.
50. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184.
51. Lee H.J., Macbeth A.H., Pagani J.H., Young W.S. Oxytocin: the great facilitator of life. Prog. Neurobiol. 2009, 88:127-151.
52. 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.
53. Liu Y., Wang Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 2003, 121:537-544.
54. Ludwig M., Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 2006, 7:126-136.
55. Marsh A.A., Yu H.H., Pine D.S., Blair R.J. Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology (Berl) 2010, 209:225-232.
56. McCarthy M.M., McDonald C.H., Brooks P.J., Goldman D. An anxiolytic action of oxytocin is enhanced by estrogen in the mouse. Physiol. Behav. 1996, 60:1209-1215.
57. Mens W.B., Laczi F., Tonnaer J.A., de Kloet E.R., van Wimersma Greidanus T.B. Vasopressin and oxytocin content in cerebrospinal fluid and in various brain areas after administration of histamine and pentylenetetrazol. Pharmacol. Biochem. Behav. 1983, 19:587-591.
58. 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.
59. Modahl C., Green L., Fein D., Morris M., Waterhouse L., Feinstein C., Levin H. Plasma oxytocin levels in autistic children. Biol. Psychiatry 1998, 43:270-277.
60. Morris J.F., Pow D.V. Widespread release of peptides in the central nervous system: quantitation of tannic acid-captured exocytoses. Anat. Rec. 1991, 231:437-445.
61. Norman G.J., Hawkley L., Luhmann M., Ball A.B., Cole S.W., Berntson G.G., Cacioppo J.T. Variation in the oxytocin receptor gene influences neurocardiac reactivity to social stress and HPA function: a population based study. Horm. Behav. 2012, 61:134-139.
62. Pedersen C.A., Prange A.J. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:6661-6665.
63. 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.
64. Pfister H.P., Muir J.L. Influence of exogenously administered oxytocin on central noradrenaline, dopamine and serotonin levels following psychological stress in nulliparous female rats (Rattus norvegicus). Int. J. Neurosci. 1989, 45:221-229.
65. Pincus D., Kose S., Arana A., Johnson K., Morgan P.S., Borckardt J., Herbsman T., Hardaway F., George M.S., Panksepp J., Nahas Z. Inverse effects of oxytocin on attributing mental activity to others in depressed and healthy subjects: a double-blind placebo controlled FMRI study. Front. Psychiatry 2010, 1:134.
66. Riem M.M., Bakermans-Kranenburg M.J., Pieper S., Tops M., Boksem M.A., Vermeiren R.R., van Ijzendoorn M.H., Rombouts S.A. Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol. Psychiatry 2011, 70:291-297.
67. Riem M.M., van Ijzendoorn M.H., Tops M., Boksem M.A., Rombouts S.A., Bakermans-Kranenburg M.J. No laughing matter: intranasal oxytocin administration changes functional brain connectivity during exposure to infant laughter. Neuropsychopharmacology 2012, 37:1257-1266.
68. Rilling J.K., DeMarco A.C., Hackett P.D., Thompson R., Ditzen B., Patel R., Pagnoni G. Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology 2012, 37:447-461.
69. Ross H.E., Cole C.D., Smith Y., Neumann I.D., Landgraf R., Murphy A.Z., Young L.J. Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 2009, 162:892-903.
70. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30:534-547.
71. Saphire-Bernstein S., Way B.M., Kim H.S., Sherman D.K., Taylor S.E. Oxytocin receptor gene (OXTR) is related to psychological resources. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:15118-15122.
72. Singer T., Snozzi R., Bird G., Petrovic P., Silani G., Heinrichs M., Dolan R.J. Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Emotion 2008, 8:781-791.
73. Skuse D.H., Gallagher L. Dopaminergic-neuropeptide interactions in the social brain. Trends Cogn. Sci. 2009, 13:27-35.
74. Smeltzer M.D., Curtis J.T., Aragona B.J., Wang Z. Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci. Lett. 2006, 394:146-151.
75. 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. 2012, 1-6.
76. Strathearn L., Fonagy P., Amico J., Montague P.R. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 2009, 34:2655-2666.
77. Striepens N., Kendrick K.M., Maier W., Hurlemann R. Prosocial effects of oxytocin and clinical evidence for its therapeutic potential. Front. Neuroendocrinol. 2011, 32:426-450.
78. Thompson R.R., George K., Walton J.C., Orr S.P., Benson J. Sex-specific influences of vasopressin on human social communication. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:7889-7894.
79. Torrealba F., Carrasco M.A. A review on electron microscopy and neurotransmitter systems. Brain Res. Brain Res. Rev. 2004, 47:5-17.
80. van den Heuvel M.P., Hulshoff Pol H.E. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur. Neuropsychopharmacol. 2010, 20:519-534.
81. Viviani D., Charlet A., van den Burg E., Robinet C., Hurni N., Abatis M., Magara F., Stoop R. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 2011, 333:104-107.
82. Walum H., Lichtenstein P., Neiderhiser J.M., Reiss D., Ganiban J.M., Spotts E.L., Pedersen N.L., Anckarsater H., Larsson H., Westberg L. Variation in the oxytocin receptor gene is associated with pair-bonding and social behavior. Biol. Psychiatry 2012, 71:419-426.
83. Welchew D.E., Ashwin C., Berkouk K., Salvador R., Suckling J., Baron-Cohen S., Bullmore E. Functional disconnectivity of the medial temporal lobe in Asperger's syndrome. Biol. Psychiatry 2005, 57:991-998.
84. Whalen P.J., Rauch S.L., Etcoff N.L., McInerney S.C., Lee M.B., Jenike M.A. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 1998, 18:411-418.
85. Windle R.J., Shanks N., Lightman S.L., Ingram C.D. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 1997, 138:2829-2834.
86. Wittfoth-Schardt D., Grunding J., Wittfoth M., Lanfermann H., Heinrichs M., Domes G., Buchheim A., Gundel H., Waller C. Oxytocin modulates neural reactivity to children's faces as a function of social salience. Neuropsychopharmacology 2012, 37:1799-1807.
87. Yoshida M., Takayanagi Y., Inoue K., Kimura T., Young L.J., Onaka T., Nishimori K. Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J. Neurosci. 2009, 29:2259-2271.
88. Young L.J., Wang Z. The neurobiology of pair bonding. Nat. Neurosci. 2004, 7:1048-1054.
89. Zimmerman E.A., Robinson A.G., Husain M.K., Acosta M., Frantz A.G., Sawyer W.H. Neurohypophysial peptides in the bovine hypothalamus: the relationship of neurophysin I to oxytocin, and neurophysin II to vasopressin in supraoptic and paraventricular regions. Endocrinology 1974, 95:931-936.