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Brief Report| Volume 62, ISSUE 10, P1187-1190, November 15, 2007

Oxytocin Attenuates Amygdala Responses to Emotional Faces Regardless of Valence

      Background

      Oxytocin is known to reduce anxiety and stress in social interactions as well as to modulate approach behavior. Recent studies suggest that the amygdala might be the primary neuronal basis for these effects.

      Methods

      In a functional magnetic resonance imaging study using a double-blind, placebo-controlled within-subject design, we measured neural responses to fearful, angry, and happy facial expressions after intranasal application of 24 IU oxytocin compared with placebo.

      Results

      Oxytocin reduced right-sided amygdala responses to all three face categories even when the emotional content of the presented face was not evaluated explicitly. Exploratory whole brain analysis revealed modulatory effects in prefrontal and temporal areas as well as in the brainstem.

      Conclusions

      Results suggest a modulatory role of oxytocin on amygdala responses to facial expressions irrespective of their valence. Reduction of amygdala activity to positive and negative stimuli might reflect reduced uncertainty about the predictive value of a social stimulus and thereby facilitates social approach behavior.

      Key Words

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      References

        • Ferguson J.N.
        • Young L.J.
        • Insel T.R.
        The neuroendocrine basis of social recognition.
        Front Neuroendocrinol. 2002; 23: 200-224
        • Neumann I.D.
        • Kromer S.A.
        • Toschi N.
        • Ebner K.
        Brain oxytocin inhibits the (re)activity of the hypothalamo–pituitary–adrenal axis in male rats: Involvement of hypothalamic and limbic brain regions.
        Regul Pept. 2000; 96: 31-38
        • Young L.J.
        • Wang Z.
        The neurobiology of pair bonding.
        Nat Neurosci. 2004; 7: 1048-1054
        • Carter C.S.
        Neuroendocrine perspectives on social attachment and love.
        Psychoneuroendocrinology. 1998; 23: 779-818
        • Pedersen C.A.
        • Ascher J.A.
        • Monroe Y.L.
        • Prange Jr, A.J.
        Oxytocin induces maternal behavior in virgin female rats.
        Science. 1982; 216: 648-650
        • Heinrichs M.
        • Baumgartner T.
        • Kirschbaum C.
        • Ehlert U.
        Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress.
        Biol Psychiatry. 2003; 54: 1389-1398
        • Heinrichs M.
        • Meinlschmidt G.
        • Neumann I.
        • Wagner S.
        • Kirschbaum C.
        • Ehlert U.
        • et al.
        Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women.
        J Clin Endocrinol Metab. 2001; 86: 4798-4804
        • Kosfeld M.
        • Heinrichs M.
        • Zak P.J.
        • Fischbacher U.
        • Fehr E.
        Oxytocin increases trust in humans.
        Nature. 2005; 435: 673-676
        • Domes G.
        • Heinrichs M.
        • Michel A.
        • Berger C.
        • Herpertz S.C.
        Oxytocin improves “mind-reading” in humans.
        Biol Psychiatry. 2007; 61: 731-733
        • Bale T.L.
        • Davis A.M.
        • Auger A.P.
        • Dorsa D.M.
        • McCarthy M.M.
        CNS region-specific oxytocin receptor expression: Importance in regulation of anxiety and sex behavior.
        J Neurosci. 2001; 21: 2546-2552
        • Huber D.
        • Veinante P.
        • Stoop R.
        Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala.
        Science. 2005; 308: 245-248
        • 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
        • Ferguson J.N.
        • Aldag J.M.
        • Insel T.R.
        • Young L.J.
        Oxytocin in the medial amygdala is essential for social recognition in the mouse.
        J Neurosci. 2001; 21: 8278-8285
        • Davis M.
        • Whalen P.J.
        The amygdala: Vigilance and emotion.
        Mol Psychiatry. 2001; 6: 13-34
        • Adolphs R.
        Recognizing emotion from facial expressions: Psychological and neurological mechanisms.
        Behav Cogn Neurosci Rev. 2002; 1: 21-61
        • Glascher J.
        • Tuscher O.
        • Weiller C.
        • Buchel C.
        Elevated responses to constant facial emotions in different faces in the human amygdala: An fMRI study of facial identity and expression.
        BMC Neurosci. 2004; 5: 45
        • Morris J.S.
        • Friston K.J.
        • Buchel C.
        • Frith C.D.
        • Young A.W.
        • Calder A.J.
        • et al.
        A neuromodulatory role for the human amygdala in processing emotional facial expressions.
        Brain. 1998; 121: 47-57
        • Phan K.L.
        • Wager T.
        • Taylor S.F.
        • Liberzon I.
        Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI.
        Neuroimage. 2002; 16: 331-348
        • 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
        • Yang T.T.
        • Menon V.
        • Eliez S.
        • Blasey C.
        • White C.D.
        • Reid A.J.
        • et al.
        Amygdalar activation associated with positive and negative facial expressions.
        Neuroreport. 2002; 13: 1737-1741
        • Fitzgerald D.A.
        • Angstadt M.
        • Jelsone L.M.
        • Nathan P.J.
        • Phan K.L.
        Beyond threat: Amygdala reactivity across multiple expressions of facial affect.
        Neuroimage. 2006; 30: 1441-1448
        • Kirsch P.
        • Esslinger C.
        • Chen Q.
        • Mier D.
        • Lis S.
        • Siddhanti S.
        • et al.
        Oxytocin modulates neural circuitry for social cognition and fear in humans.
        J Neurosci. 2005; 25: 11489-11493
        • 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
        • Steyer R.
        • Schwenkmezger P.
        • Notz P.
        • Eid M.
        Der Mehrdimensionale Befindlichkeitsfragebogen MDBF [Multidimensional mood questionnaire].
        Hogrefe, Göttingen, Germany1997
        • Eckman P.
        • Friesen W.V.
        Pictures of Facial Affect.
        Consulting Psychologists, Palo Alto, California1976
        • Tzourio-Mazoyer N.
        • Landeau B.
        • Papathanassiou D.
        • Crivello F.
        • Etard O.
        • Delcroix N.
        • et al.
        Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.
        Neuroimage. 2002; 15: 273-289
        • 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
        • Hsu M.
        • Bhatt M.
        • Adolphs R.
        • Tranel D.
        • Camerer C.F.
        Neural systems responding to degrees of uncertainty in human decision-making.
        Science. 2005; 310: 1680-1683
        • Adolphs R.
        • Spezio M.
        Role of the amygdala in processing visual social stimuli.
        Prog Brain Res. 2006; 156: 363-378
        • Haxby J.V.
        • Hoffman E.A.
        • Gobbini M.I.
        The distributed human neural system for face perception.
        Trends Cogn Sci. 2000; 4: 223-233
        • Dalton K.M.
        • Nacewicz B.M.
        • Johnstone T.
        • Schaefer H.S.
        • Gernsbacher M.A.
        • Goldsmith H.H.
        • et al.
        Gaze fixation and the neural circuitry of face processing in autism.
        Nat Neurosci. 2005; 8: 519-526
        • Herpertz S.C.
        • Dietrich T.M.
        • Wenning B.
        • Krings T.
        • Erberich S.G.
        • Willmes K.
        • et al.
        Evidence of abnormal amygdala functioning in borderline personality disorder: A functional MRI study.
        Biol Psychiatry. 2001; 50: 292-298
        • Phan K.L.
        • Fitzgerald D.A.
        • Nathan P.J.
        • Tancer M.E.
        Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia.
        Biol Psychiatry. 2006; 59: 424-429