Oxytocin Attenuates Amygdala Reactivity to Fear in Generalized Social Anxiety Disorder
Open accessAbstract
Patients with generalized social anxiety disorder (GSAD) exhibit heightened activation of the amygdala in response to social cues conveying threat (eg, fearful/angry faces). The neuropeptide oxytocin (OXT) decreases anxiety and stress, facilitates social encounters, and attenuates amygdala reactivity to threatening faces in healthy subjects. The goal of this study was to examine the effects of OXT on fear-related amygdala reactivity in GSAD and matched healthy control (CON) subjects. In a functional magnetic resonance imaging study utilizing a double-blind placebo-controlled within-subjects design, we measured amygdala activation to an emotional face matching task of fearful, angry, and happy faces following acute intranasal administration of OXT (24 IU or 40.32 μg) and placebo in 18 GSAD and 18 CON subjects. Both the CON and GSAD groups activated bilateral amygdala to all emotional faces during placebo, with the GSAD group exhibiting hyperactivity specifically to fearful faces in bilateral amygdala compared with the CON group. OXT had no effect on amygdala activity to emotional faces in the CON group, but attenuated the heightened amygdala reactivity to fearful faces in the GSAD group, such that the hyperactivity observed during the placebo session was no longer evident following OXT (ie, normalization). These findings suggest that OXT has a specific effect on fear-related amygdala activity, particularly when the amygdala is hyperactive, such as in GSAD, thereby providing a brain-based mechanism of the impact of OXT in modulating the exaggerated processing of social signals of threat in patients with pathological anxiety.
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Many have posited that the amygdala is an important therapeutic target for the management of GSAD.
“Heightened amygdala reactivity has been strongly linked to these social threat-related impairments and many have posited that the amygdala is an important therapeutic target for the management of GSAD (Labuschagne et al, 2010;Phan et al, 2006).”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
Heightened amygdala reactivity has been strongly linked to social threat-related impairments in GSAD.
“Heightened amygdala reactivity has been strongly linked to these social threat-related impairments and many have posited that the amygdala is an important therapeutic target for the management of GSAD (Labuschagne et al, 2010;Phan et al, 2006).”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
In GSAD patients, OXT attenuated or normalized the hyperactive amygdala reactivity to fearful faces.
“We have extended these studies to examine the effects of OXT on amygdala reactivity to social threat in GSAD (Labuschagne et al, 2010) and found that OXT attenuated (or normalized) the hyperactive amygdala reactivity to fearful faces in GSAD patients.”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
The effects of OXT on amygdala reactivity to fearful faces in GSAD were not observed in response to angry or happy faces.
“These effects were not observed in response to angry or happy faces.”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
There was a significant group by drug interaction on left amygdala reactivity to fearful faces, such that OXT attenuated or normalized the hyperactive amygdala reactivity to fearful faces in GSAD patients.
“We first confirmed using a whole-brain, 2 (session: PBO, OXT)  2 (group: HC, GSAD) analysis of variance (ANOVA) that consistent with Labuschagne et al (2010), there was a significant group  drug interaction on left amygdala reactivity to fearful faces (peak MNI coordinates: ( À 24, À 2, À 22), Z ¼ 2.77, k ¼ 81, po0.05, small volume corrected), such that OXT attenuated (or normalized) the hypera”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
The EFMT task has been used in previous pharmaco-fMRI studies to probe drug effects on amygdala activation and amygdala functional connectivity.
“The EFMT task has previously been described in detail elsewhere (Labuschagne et al, 2010), and has been used in previous pharmaco-fMRI studies to probe drug effects on amygdala activation (Kirsch et al, 2005;Paulus et al, 2005;Phan et al, 2008;Labuschagne et al, 2010) and amygdala functional connectivity (Gorka et al, 2013).”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
The divergent effects of oxytocin in GSAD versus HC are consistent with two other oxytocin administration studies from the authors' group.
“This finding of divergent effects is consistent with the two other OXT administration studies from our group (Dodhia et al, 2014;Labuschagne et al, 2010)”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Labuschagne et al, 2010
The authors had previously shown that acute oxytocin exerted effects on the amygdala and mPFC/ACC during the processing of threat and other negative emotions.
“We had previously shown that acute OXT exerted effects on the amygdala and mPFC/ACC during the processing of threat and other negative emotions (Labuschagne et al, 2010(Labuschagne et al, , 2011)).”
From Modulation of Resting-State Amygdala-Frontal Functional Connectivity by Oxytocin in Generalized Social Anxiety Disorder (2014) · cites this paper as Labuschagne et al, 2010
In a recent task-based study, the authors showed that oxytocin attenuates heightened activity in the amygdala of generalized social anxiety disorder patients after viewing fearful faces.
“In two recent task-based studies, we showed that OXT attenuates heightened activity in the amygdala of GSAD patients after viewing fearful faces (Labuschagne et al, 2010)”
From Modulation of Resting-State Amygdala-Frontal Functional Connectivity by Oxytocin in Generalized Social Anxiety Disorder (2014) · cites this paper as Labuschagne et al, 2010
OT administration decreases amygdala activation to fearful faces in healthy and anxious humans.
“This is also agreement with decreasing amygdala activation to fearful faces in healthy (45), as well as anxious (46), humans with OT administration.”
From Neuroendocrinology of Parental Response to Baby‐Cry (2011) · cites this paper as [46]
IN-OT attenuates heightened amygdala reactivity to fearful faces in patients with generalized social anxiety disorder (GSAD).
“Importantly, IN-OT attenuates heightened amygdala reactivity to fearful faces in patients with generalized social anxiety disorder (GSAD) (Labuschagne et al. 2010).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Labuschagne et al. 2010
OT reduces anxiety, fear, and stress, in part by dampening amygdala activity.
“there are increasing evidence for the role of OT in reducing anxiety, fear, and stress, in part by dampening amygdala activity”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Labuschagne et al. 2010
IN-OT restores functional connectivity between subcortical regions such as amygdala and frontal areas, including the ACC and mPFC, in patients with generalized anxiety disorders.
“IN-OT restores functional connectivity between subcortical regions such as amygdala and frontal areas, including the ACC and mPFC”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Labuschagne et al. 2010
IN-OT reduces heightened amygdala reactivity to fearful faces in patients with generalized anxiety disorders.
“reduces the heightened amygdala reactivity to fearful faces in patients with generalized anxiety disorders”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Labuschagne et al. 2010
The tested type of intranasal OT delivery, but not peripherally delivered OT that produces similar blood levels, replicates prior findings of reduced right amygdala activation in response to emotional stimuli after OT treatment.
“Results indicate that the tested type of intranasal OT delivery -but not peripherally delivered OT that produces similar blood levels -replicates prior findings of reduced right amygdala activation in response to emotional stimuli after OT treatment (Domes et al., 2007;Labuschagne et al., 2010;Petrovic et al., 2008).”
From Low dose intranasal oxytocin delivered with Breath Powered device dampens amygdala response to emotional stimuli: A peripheral effect-controlled within-subjects randomized dose-response fMRI trial (2016) · cites this paper as Labuschagne et al., 2010
Other studies have reported similar results after administration of 24 IU, but dosages are difficult to compare between experiments as these studies used traditional nasal spray devices to administer OT.
“Of note, other studies have reported similar results after administration of 24 IU (Domes et al., 2007;Kanat et al., 2015;Labuschagne et al., 2010), however, the dosages are difficult to compare between experiments as these studies used traditional nasal spray devices to administer OT.”
From Low dose intranasal oxytocin delivered with Breath Powered device dampens amygdala response to emotional stimuli: A peripheral effect-controlled within-subjects randomized dose-response fMRI trial (2016) · cites this paper as Labuschagne et al., 2010
Oxytocin normalized abnormal neural responses to negative social stimuli in patients with social anxiety disorder.
“normalized the abnormal neural responses to negative social stimuli in patients with social anxiety disorder (32, 33).”
From Placebo treatment facilitates social trust and approach behavior (2018) · cites this paper as [32]
Some research indicates that OXT could be influential in the treatment of established SAD and PTSD.
“Some research indicates that OXT could be influential in the treatment of established SAD (Labuschagne et al, 2010) and PTSD (Olff et al, 2014).”
From Oxytocin Facilitates Pavlovian Fear Learning in Males (2016) · cites this paper as Labuschagne et al, 2010
OT administration effects may be especially beneficial in those who lack proficiency in fear regulation or social functioning.
“This fits with the hypothesis that OT administration effects may be especially beneficial in those who lack proficiency in fear regulation (Labuschagne et al, 2010) or social functioning (Olff et al, 2013;Weisman and Feldman, 2013).”
From Intranasal oxytocin administration dampens amygdala reactivity towards emotional faces in male and female PTSD patients (2016) · cites this paper as Labuschagne et al, 2010
OT administration dampened amygdala reactivity toward emotional stimuli in healthy males, males with GSAD, and females with BPD, although findings for females have been mixed.
“In addition, functional MRI (fMRI) studies have shown that OT administration dampened amygdala reactivity toward emotional stimuli in healthy males (Kirsch et al, 2005), males with generalized social anxiety disorder (GSAD; Labuschagne et al, 2010) and females with borderline personality disorder (BPD; Bertsch et al, 2013), although findings for females have been mixed (Domes et al, 2010).”
From Intranasal oxytocin administration dampens amygdala reactivity towards emotional faces in male and female PTSD patients (2016) · cites this paper as Labuschagne et al, 2010
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Localization of oxytocin receptor messenger ribonucleic acid in the rat brain.
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Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3044 · Cited by 1,688 · see citing works
Self-citationSocial effects of oxytocin in humans: context and person matter
Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.002 · Cited by 1,572 · see citing works
Intranasal delivery of biologics to the central nervous system
Lochhead, J. J., & Thorne, R. G. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2011.11.002 · Cited by 1,214 · see citing works
Handbook of Religion and Health
Koenig, H. G., VanderWeele, T. J., & Peteet, J. R. (2023) · doi:10.1093/oso/9780190088859.001.0001 · Cited by 1,150 · see citing works
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999 · see citing works
Neumann, I. D., & Landgraf, R. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.08.004 · Cited by 954 · see citing works
Evaluation of intranasal delivery route of drug administration for brain targeting
Erdő, F., Bors, L. A., Farkas, D., Bajza, Á., & Gizurarson, S. S. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.10.009 · Cited by 756 · see citing works
Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice
Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., & Landgraf, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.03.003 · Cited by 511 · see citing works
“These and clinical studies on social anxiety (Guastella et al., 2010; Labuschagne et al., 2010) and schizophrenia (Feifel et al.”
BackgroundOxytocin in general anxiety and social fear: a translational approach
Neumann, I. D., & Slattery, D. A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.004 · Cited by 468 · see citing works
Gender differences in social anxiety disorder: A review
Asher, M., Asnaani, A., & Aderka, I. M. (2017) · Clinical Psychology Review · doi:10.1016/j.cpr.2017.05.004 · Cited by 457 · see citing works
Brühl, A. B., Delsignore, A., Komossa, K., & Weidt, S. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.003 · Cited by 439 · see citing works
“Three other publications focused on the effects of a single application of intranasal oxytocin (Labuschagne et al., 2010, , in press, Dodhia et al., in press) in SAD patients.”
InfluentialBos, P. A., Panksepp, J., Bluthé, R.-M., & Honk, J. V. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.01.002 · Cited by 429 · see citing works
Singewald, N., Schmuckermair, C., Whittle, N., Holmes, A., & Ressler, K. J. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.004 · Cited by 390 · see citing works
“…has been demonstrated to reduce stress-induced cortisol release in humans (de Oliveira et al., 2012; Heinrichs et al., 2003; Quirin et al., 2011), and to attenuate AMY hyperactivity as well as AMY-hindbrain coupling in anxiety patients [(Kirsch et al., 2005; Labuschagne et al., 2010)].”
BackgroundLukas, M., Toth, I., Reber, S. O., Slattery, D. A., Veenema, A. H., & Neumann, I. D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.95 · Cited by 403 · see citing works
“Similarly, in human studies intranasal OT application reduced hyperresponsivity of the amygdala to facial cues in socially anxious patients, while not affecting the response observed in normal patients (Labuschagne et al, 2010).”
BackgroundBakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.34 · Cited by 383 · see citing works
“In a study using fMRI, the effects of a single intranasal OT administration (24 IU) on neural reactivity to angry and fearful faces in 18 SAD patients and 18 matched healthy controls were examined.(100) When watching fearful faces, SAD patients showed heightened bilateral amygdala activation compared with controls.”
BackgroundVan IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.008 · Cited by 365 · see citing works
Skrundz, M., Bolten, M., Nast, I., Hellhammer, D. H., & Meinlschmidt, G. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.74 · Cited by 349 · see citing works
De Dreu, C. K. W., & Kret, M. E. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.03.020 · Cited by 297 · see citing works
“Finally, oxytocin blunts attention to negative social cues such as angry faces and displays of dominance (38–41), and in patients with anxiety disorders, intranasal oxytocin attenuates hyperactivity in the amygdala when social cues conveying threat are displayed (42).”
BackgroundBethlehem, R. A. I., van Honk, J., Auyeung, B., & Baron-Cohen, S. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.10.011 · Cited by 285 · see citing works
“This could support the hypothesis suggested by Labuschagne et al. (2010, 2011) that OT modulates the 'extremes'.”
BackgroundMethodResultInfluentialProsocial effects of oxytocin and clinical evidence for its therapeutic potential
Striepens, N., Kendrick, K. M., Maier, W., & Hurlemann, R. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.07.001 · Cited by 283 · see citing works
“To date only one neuroimaging study has investigated the effect of OXT on fear-related amygdala reactivity to threatening faces in patients with generalized SAD and found, as expected, that it reduced the amygdala hyper-reactivity in SAD patients to levels seen in controls [113].”
BackgroundDabrowska, J., Hazra, R., Ahern, T. H., Guo, J.-D., McDonald, A. J., Mascagni, F., Muller, J. F., Young, L. J., & Rainnie, D. G. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.003 · Cited by 274 · see citing works
“The results of our study suggest that this delayed effect may be consistent with an indirect activation of the OT system (Windle et al., 1997; Labuschagne et al., 2010).”
Predicting treatment response in social anxiety disorder from functional magnetic resonance imaging.
Doehrmann, O., Ghosh, S. S., Polli, F. E., Reynolds, G. O., Horn, F., Keshavan, A., Triantafyllou, C., Saygin, Z. M., Whitfield-Gabrieli, S., Hofmann, S. G., et al. (2013) · JAMA Psychiatry · doi:10.1001/2013.jamapsychiatry.5 · Cited by 262 · see citing works
Cochran, D. M., Fallon, D., Hill, M., & Frazier, J. A. (2013) · Harvard Review of Psychiatry · doi:10.1097/hrp.0b013e3182a75b7d · Cited by 267 · see citing works
“viewing emotional faces.(96,97) Relative to the control group, patients with GSAD displayed hyperactivity of the bilateral amygdala when viewing fearful faces(96) and hyperactivity of the medial prefrontal cortex extending into the anterior cingulate cortex when viewing sad faces.”
BackgroundQuintana, D. S., Lischke, A., Grace, S., Scheele, D., Ma, Y., & Becker, B. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00864-7 · Cited by 263 · see citing works
Oxytocin facilitates protective responses to aversive social stimuli in males
Striepens, N., Scheele, D., Kendrick, K. M., Becker, B., Schäfer, L., Schwalba, K., Reul, J., Maier, W., & Hurlemann, R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208852109 · Cited by 242 · see citing works
“26 and 27), and subjects with social phobia (28).”
BackgroundNeural circuits in anxiety and stress disorders: a focused review
Liberzon, I., Duval, E. R., & Javanbakht, A. (2015) · Therapeutics and Clinical Risk Management · doi:10.2147/tcrm.s48528 · Cited by 262 · see citing works
Auyeung, B., Lombardo, M. V., Heinrichs, M., Chakrabarti, B., Sule, A., Deakin, J. B., Bethlehem, R. A. I., Dickens, L., Mooney, N., Sipple, J. A. N., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2014.146 · Cited by 234 · see citing works
Self-citationThe Role of Oxytocin in Human Affect: A Novel Hypothesis
Kemp, A. H., & Guastella, A. J. (2011) · Current Directions in Psychological Science · doi:10.1177/0963721411417547 · Cited by 228 · see citing works
Puglia, M. H., Lillard, T. S., Morris, J. P., & Connelly, J. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1422096112 · Cited by 216 · see citing works
Genetic origins of social networks in rhesus macaques
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013) · Scientific Reports · doi:10.1038/srep01042 · Cited by 220 · see citing works
Prenatal and postnatal hormone effects on the human brain and cognition
Bonnie Auyeung, B., Lombardo, M. V., & Baron‐Cohen, S. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1268-2 · Cited by 219 · see citing works
Oxytocin facilitates the extinction of conditioned fear in humans
Eckstein, M., Becker, B., Scheele, D., Scholz, C., Preckel, K., Schlaepfer, T. E., Grinevich, V., Kendrick, K. M., Maier, W., & Hurlemann, R. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.10.015 · Cited by 210 · see citing works
Dodhia, S., Hosanagar, A., Fitzgerald, D. A., Labuschagne, I., Wood, A. G., Nathan, P. J., & Phan, K. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.53 · Cited by 209 · see citing works
Self-citationIntranasal delivery of systemic-acting drugs: Small-molecules and biomacromolecules
Fortuna, A. C., Alves, G., Serralheiro, A., Sousa, J., & Falcão, A. C. (2014) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2014.03.004 · Cited by 211 · see citing works
Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex
Sripada, C. S., Phan, K. L., Labuschagne, I., Welsh, R., Nathan, P. J., & Wood, A. G. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000533 · Cited by 197 · see citing works
Self-citationPaloyelis, Y., Doyle, O. M., Zelaya, F. O., Maltezos, S., Williams, S. C., Fotopoulou, A., & Howard, M. A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.10.005 · Cited by 187 · see citing works
Carson, D. S., Berquist, S. W., Trujillo, T. H., Garner, J. P., Hannah, S. L., Hyde, S. A., Sumiyoshi, R. D., Jackson, L. P., Moss, J. K., Strehlow, M. C., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.132 · Cited by 196 · see citing works
Epigenetic regulation of the oxytocin receptor gene: implications for behavioral neuroscience
Kumsta, R., Hummel, E., Chen, F. S., & Heinrichs, M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00083 · Cited by 207 · see citing works
“, 2011), and social anxiety disorder (Guastella et al., 2009; Labuschagne et al., 2010).”
Self-citationDumais, K. M., Bredewold, R., Mayer, T. E., & Veenema, A. H. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.08.012 · Cited by 201 · see citing works
Prater, K. E., Hosanagar, A., Klumpp, H., Angstadt, M., & Luan Phan, K. (2013) · Depression and Anxiety · doi:10.1002/da.22014 · Cited by 194 · see citing works
“previously described by our and other groups in healthy and gSAD subjects.[19,24,25] The EFMT, a variant of the task originally described by Hariri et al.”
Self-citationOxytocin receptor gene methylation: converging multilevel evidence for a role in social anxiety
Ziegler, C., Dannlowski, U., Bräuer, D., Stevens, S., Laeger, I., Wittmann, H., Kugel, H., Dobel, C., Hurlemann, R., Reif, A., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.2 · Cited by 193 · see citing works
Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum
Zoicas, I., Slattery, D. A., & Neumann, I. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.156 · Cited by 189 · see citing works
MacDonald, K., & Feifel, D. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00035 · Cited by 181 · see citing works
“On the other hand, some acute neural responses (attenuation of amygdala activity) are seen in both patient groups (Labuschagne et al., 2010) and normals (Zink and MeyerLindenberg, 2012) (Figure 1).”
BackgroundWigton, R., Radua, J., Allen, P., Averbeck, B., Meyer-Lindenberg, A., McGuire, P., Shergill, S. S., & Fusar-Poli, P. (2015) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.130289 · Cited by 179 · see citing works
Human neuroimaging of oxytocin and vasopressin in social cognition
Zink, C. F., & Meyer-Lindenberg, A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.016 · Cited by 176 · see citing works
“Probing the acute and chronic impact of oxytocin and vasopressin on social cognition neural circuitry in those with mental disorders is relatively underrepresented in the literature, limited to two studies of the influence of oxytocin administration on social emotion-related brain activity in generalized social anxiet…”
BackgroundResultInfluentialMaking room for oxytocin in understanding depression
McQuaid, R. J., McInnis, O. A., Abizaid, A. B., & Anisman, H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.005 · Cited by 172 · see citing works
“Paralleling these findings, intranasal oxytocin administration to humans attenuated amygdala activation elicited by anxiety-provoking social stimuli (Kirsch et al., 2005; Labuschagne et al., 2010; Petrovic et al., 2008).”
BackgroundIntranasal administration of oxytocin: behavioral and clinical effects, a review
Veening, J. G., & Olivier, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.012 · Cited by 169 · see citing works
“Labuschagne et al. (2010) observed a bilateral amygdala activation after showing fearful faces and extended their observations in 2011 (Labuschagne et al., 2011) by showing that in generalizedsocial-anxiety-disorder (GSAD) patients the medial prefrontal cortex and the anterior cingulate cortex…”
BackgroundFeng, C., Hackett, P. D., DeMarco, A. C., Chen, X., Stair, S., Haroon, E., Ditzen, B., Pagnoni, G., & Rilling, J. K. (2015) · Brain Imaging and Behavior · doi:10.1007/s11682-014-9333-9 · Cited by 157 · see citing works
Bandelow, B., Baldwin, D. S., Abelli, M., Altamura, C. A., Dell’Osso, B. M., Domschke, K., Fineberg, N. A., Grünblatt, E., Jarema, M., Maron, E., et al. (2016) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2016.1181783 · Cited by 165 · see citing works
“In an fMRI study, oxytocin attenuated the heightened amygdala reactivity to fearful faces in individuals with SAD (Labuschagne et al. 2010).”
BackgroundStrategies To Deliver Peptide Drugs to the Brain
Lalatsa, A., Schätzlein, A. G., & Uchegbu, I. F. (2014) · Molecular Pharmaceutics · doi:10.1021/mp400680d · Cited by 162 · see citing works
Neural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157 · see citing works
Roles of Oxytocin in Stress Responses, Allostasis and Resilience
Takayanagi, Y., & Onaka, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010150 · Cited by 164 · see citing works
“In patients with generalized social anxiety disorder, hyper-reactivity to fearful faces in the left amygdala has been reported to be attenuated by intranasal oxytocin [80].”
BackgroundOptogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150 · see citing works
“Ormel, J, Von Korff, M., Van den Brink, W., Katon, W., Brilman, E., and Oldehinkel, T. (1993). Depression, anxiety, and social disability show synchrony of change”
BackgroundMethodInfluentialQuintana, D. S., Alvares, G. A., Hickie, I. B., & Guastella, A. J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.011 · Cited by 149 · see citing works
Yamasue, H., Yee, J. R., Hurlemann, R., Rilling, J. K., Chen, F. S., Meyer-Lindenberg, A., & Tost, H. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3327-12.2012 · Cited by 149 · see citing works
“Intranasal OT has also been shown to normalize heightened amygdala and medial prefrontal cortex activity associated with social anxiety disorder (Labuschagne et al., 2010, 2011).”
BackgroundEstrogen Receptors Modulation of Anxiety-Like Behavior
Borrow, A. P., & Handa, R. J. (2017) · Vitamins and Hormones · doi:10.1016/bs.vh.2016.08.004 · Cited by 146 · see citing works
“Plasma OT levels are negatively correlated with anxiety symptoms in depressed patients (Scantamburlo et al., 2007), and intranasal OT administration attenuates emotional fear reactivity in patients with social anxiety disorder (Labuschagne et al., 2010).”
BackgroundNeuroimaging in anxiety disorders
Holzschneider, K., & Mulert, C. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.4/kholzschneider · Cited by 146 · see citing works
“In patients with social anxiety disorder, oxytocin attenuated the heightened amygdala activation in response to fearful faces.(73) Hence, it appears to modulate the exaggerated amygdala activity during confrontation with social stimuli in pathological social anxiety.”
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Bowen, M. T., Carson, D. S., Spiro, A., Arnold, J. C., & McGregor, I. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027237 · Cited by 143 · see citing works
Intranasal Oxytocin Normalizes Amygdala Functional Connectivity in Posttraumatic Stress Disorder
Koch, S. B. J., van Zuiden, M., Nawijn, L., Frijling, J. L., Veltman, D. J., & Olff, M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.1 · Cited by 132 · see citing works
Acheson, D., Feifel, D., de Wilde, S., Mckinney, R., Lohr, J., & Risbrough, V. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3099-4 · Cited by 141 · see citing works
“This dose has been shown to produce anxiolytic effects in healthy humans (de Oliveira et al. 2012; Labuschagne et al. 2010).”
BackgroundLabuschagne, I., Phan, K. L., WOOD, A. G., Angstadt, M., Chua, P. M.-L., Heinrichs, M., Stout, J. C., & Nathan, P. J. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001489 · Cited by 139 · see citing works
“…have shown that patients with GSAD exhibit heightened activation of the amygdala in response to social cues conveying threat and/or negative feedback such as fearful, angry, contemptuous and/or disgusted faces (Evans et al. 2008; Labuschagne et al. 2010; Phan et al. 2006; Stein et al. 2002).”
BackgroundMethodInfluentialSelf-citationHarari-Dahan, O., & Bernstein, A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.007 · Cited by 135 · see citing works
Herpertz, S. C., & Bertsch, K. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15020216 · Cited by 139 · see citing works
“While, for instance, oxytocin dampens amygdala response in individuals with social anxiety (90), it enhances amygdala activity in individuals with autism spectrum disorder (91) who experience low interest in their conspecifics.”
BackgroundFan, Y., Herrera-Meléndez, A. L., Pestke, K., Feeser, M., Aust, S., Otte, C., Pruessner, J. C., Böker, H., Bajbouj, M., & Grimm, S. (2014) · Human Brain Mapping · doi:10.1002/hbm.22553 · Cited by 134 · see citing works
Oxytocin in postnatally depressed mothers: Its influence on mood and expressed emotion
Mah, B. L., van IJzendoorn, M. H., Smith, R., & Bakermans‐Kranenburg, M. J. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.10.005 · Cited by 135 · see citing works
“OT administration has been found to produce no effect on mood in both community samples (Kirsch et al., 2005; Rockliff et al., 2011) and a clinical sample of participants with anxiety disorders (Labuschagne et al., 2010).”
Oxytocin facilitates accurate perception of competition in men and kinship in women
Fischer-Shofty, M., Levkovitz, Y., & Shamay-Tsoory, S. G. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr100 · Cited by 132 · see citing works
Lukas, M., & Neumann, I. D. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.011 · Cited by 136 · see citing works
Gorka, S. M., Fitzgerald, D. A., Labuschagne, I., Hosanagar, A., Wood, A. G., Nathan, P. J., & Phan, K. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.168 · Cited by 131 · see citing works
“The current study is a novel analysis of existing fMRI data from our previous study on the neural effects of OXT in a sample of HC and GSAD subjects (Labuschagne et al, 2010).”
BackgroundMethodResultInfluentialSelf-citationSex-specific effects of stress on oxytocin neurons correspond with responses to intranasal oxytocin
Steinman, M. Q., Duque-Wilckens, N., Greenberg, G. D., Hao, R., Campi, K. L., Laredo, S. A., Laman-Maharg, A., Manning, C. E., Doig, I. E., Lopez, E. M., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.10.007 · Cited by 131 · see citing works
“Deficits in social processes and exaggerated responses to threat are common in stress-induced psychiatric disorders (10,11), so there has been strong interest in investigating OT as a potential therapeutic agent (12,13).”
Ma, Y., Shamay-Tsoory, S., Han, S., & Zink, C. F. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.10.009 · Cited by 131 · see citing works
“Thus, one line of research has investigated how OT modulates affective neural responses in such patients [12,45,56,60].”
BackgroundInfluentialLong-term exposure to intranasal oxytocin in a mouse autism model
Bales, K. L., Solomon, M., Jacob, S., Crawley, J. N., Silverman, J. L., Larke, R. H., Sahagún, E., Puhger, K. R., Pride, M. C., & Mendoza, S. P. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.117 · Cited by 131 · see citing works
Wong, R. Y., Oxendine, S. E., & Godwin, J. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-348 · Cited by 128 · see citing works
“Oxytocin is thought to affect many social behaviors in humans [73] including having anxiolytic effects [74,75].”
Effect of oxytocin on craving and stress response in marijuana-dependent individuals: A pilot study
McRae-Clark, A. L., Baker, N. L., Maria, M. M.-S., & Brady, K. T. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3062-4 · Cited by 124 · see citing works
“In agreement, neuroimaging studies demonstrate that intranasal administration of oxytocin attenuates amygdala activation following stressful and fearful stimuli (Baumgartner et al. 2008; Domes et al. 2007; Kirsch et al. 2005; Labuschagne et al. 2010).”
BackgroundInfluentialThe effects of oxytocin on social cognition and behaviour in frontotemporal dementia
Jesso, S., Morlog, D., Ross, S., Pell, M. D., Pasternak, S., Mitchell, D. G. V., KERTESZ, A. E., & Finger, E. C. (2011) · Brain · doi:10.1093/brain/awr171 · Cited by 129 · see citing works
“that the effects of oxytocin on facial expression processing in healthy adults may be mediated via oxytocin-induced reductions in amygdala activation during threatening and fearful stimuli (Kirsch et al., 2005; Domes et al., 2007a; Labuschagne et al., 2010); however, in females, oxytocin may increase amygdala activity…”
BackgroundRoles of Oxytocin Neurones in the Control of Stress, Energy Metabolism, and Social Behaviour
Onaka, T., Takayanagi, Y., & Yoshida, M. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02300.x · Cited by 123 · see citing works
Positive maternal mental health, parenting, and child development
Phua, D. Y., Kee, M. Z. L., & Meaney, M. J. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.09.028 · Cited by 124 · see citing works
Koch, S. B. J., van Zuiden, M., Nawijn, L., Frijling, J. L., Veltman, D. J., & Olff, M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.11.018 · Cited by 123 · see citing works
“Notably, in this study no effect of OT on amygdala reactivity was found in healthy controls, suggesting that OT might be most effective in dampening amygdala responsiveness in pathological states, for example when the amygdala is hyperresponsive (Labuschagne et al., 2010), as in PTSD.”
BackgroundGrace, S. A., Rossell, S. L., Heinrichs, M., Kordsachia, C., & Labuschagne, I. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.05.031 · Cited by 120 · see citing works
“Of greatest community interest, IN-OXT provides a unique therapeutic tool for conditions characterised by anxiety and social dysfunction such as social anxiety (Labuschagne et al., 2010) and autism (Domes et al., 2013).”
InfluentialSelf-citationOxytocin and the social brain: Neural mechanisms and perspectives in human research
Kanat, M., Heinrichs, M., & Domes, G. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.003 · Cited by 122 · see citing works
“Administration of OT reduced this neural hyperreactivity in social anxiety, supporting the assumption that OT may reduce stress reactivity and exert anxiolytic effects by modulating activation in neural correlates of threat processing (Labuschagne et al., 2011, 2010).”
BackgroundInfluentialSelf-citationLawson, E. A., Holsen, L. M., Santin, M., Meenaghan, E. M., Eddy, K. T., Becker, A. E., Herzog, D. B., Goldstein, J. M., & Klibanski, A. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1702 · Cited by 121 · see citing works
Bethlehem, R. A. I., Baron-Cohen, S., van Honk, J., Auyeung, B., & Bos, P. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00048 · Cited by 120 · see citing works
Oxytocin in the socioemotional brain: implications for psychiatric disorders
Kirsch, P. (2015) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2015.17.4/pkirsch · Cited by 122 · see citing works
Oxytocin and postpartum depression: Delivering on what's known and what's not
Kim, S., Soeken, T. A., CROMER, S. J., Martinez, S. R., Hardy, L. R., & Strathearn, L. (2013) · Brain Research · doi:10.1016/j.brainres.2013.11.009 · Cited by 116 · see citing works
Cagna, F. D., Fusar‐Poli, L., Damiani, S., Rocchetti, M., Giovanna, G., Mori, A., Politi, P., & Brondino, N. (2019) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2019.17.1.1 · Cited by 118 · see citing works
“Of note, Fang et al. (2014),31) Fang et al. (2017),32) Dodhia et al. (2014),34) Gorka et al. (2015),35) Labuschagne et al. (2010)36) and Labuschagne et al. (2012)37) reported results of trials with overlapping samples, but focusing on different outcomes and outcome measures.”
Oxytocin and social functioning
Jones, C., Barrera, I., Brothers, S., Ring, R., & Wahlestedt, C. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.2/cjones · Cited by 132 · see citing works
Phan, K. L., Coccaro, E. F., Angstadt, M., Kreger, K. J., Mayberg, H. S., Liberzon, I., & Stein, M. B. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.10.003 · Cited by 114 · see citing works
“fMRI Task Brain activation was assessed using a modified version of the Emotional Face Matching Task [EFMT] (30), which has been previously validated and described in our pharmacological fMRI studies in healthy (31) and gSP (32) subjects.”
MethodSelf-citationOxytocin and Autism: A Systematic Review of Randomized Controlled Trials
Preti, A., Melis, M., Siddi, S., Vellante, M., Doneddu, G., & Fadda, R. (2014) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/cap.2013.0040 · Cited by 114 · see citing works
“…with generalized social anxiety disorder, acute intra-nasal oxytocin (24IU) reduced amygdala hyperactivity caused by the presentation of threatening stimuli (fearful face), and also decreased medial prefrontal hyperactivity caused by negative stimuli (sad faces) (Labuschagne et al. 2010, 2011).”
Kujawa, A., MacNamara, A., Fitzgerald, K. D., Monk, C. S., & Phan, K. L. (2015) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-015-0029-4 · Cited by 113 · see citing works
“Emotional Face-Matching Task Participants completed an emotional face-matching task (Hariri et al. 2002), which has been used to assess ERPs to threat in adult anxiety (Labuschagne et al. 2010; MacNamara et al. 2013).”
Self-citationBrüne, M. (2012) · BMC Medicine · doi:10.1186/1741-7015-10-38 · Cited by 113 · see citing works
“In anxiety disorders, OXT attenuated conditioned fear responses and amygdala activity [44] to become similar to the effects observed in psychologically healthy individuals [45].”
BackgroundNinan, I. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07430.x · Cited by 110 · see citing works
Kelly, A. M., Kingsbury, M. A., Hoffbuhr, K., Schrock, S. E., Waxman, B., Kabelik, D., Thompson, R. R., & Goodson, J. L. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.01.012 · Cited by 106 · see citing works
“Notably, nonapeptides influence social cognition and affiliation behaviors by acting within numerous neural loci where nonapeptides also modulate anxiety (Choleris et al., 2008; Goodson and Thompson, 2010; Labuschagne et al., 2010).”
Neuroendocrinology of Parental Response to Baby‐Cry
Swain, J. E., Kim, P., & Ho, S. S. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02212.x · Cited by 106 · see citing works
Toth, I., Neumann, I. D., & Slattery, D. A. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2702-4 · Cited by 107 · see citing works
“…also found in humans (Heinrichs et al. 2003), as OXT was shown to reduce the activation of the amygdala to threatening faces, thereby reducing the autonomic and behavioral manifestation of fear in healthy volunteers and social anxiety disorder patients (Kirsch et al. 2005; Labuschagne et al. 2010).”
Oxytocin in learning and addiction: From early discoveries to the present
Sarnyai, Z., & Kovács, G. L. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.11.019 · Cited by 106 · see citing works
“OXT administration has been shown to attenuate HPA axis activation via the amygdala, a key brain area involved in fear and anxiety behaviors (Labuschagne et al., 2010).”
BackgroundRDoC-based categorization of amygdala functions and its implications in autism
Hennessey, T., Andari, E., & Rainnie, D. G. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.04.007 · Cited by 105 · see citing works
A brief history of oxytocin and its role in modulating psychostimulant effects
Carson, D. S., Guastella, A. J., Taylor, E. R., & McGregor, I. S. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881112473788 · Cited by 105 · see citing works
“For example, Labuschagne et al. (2010) showed that an acute intranasal dose of OT (24 IU) attenuated amygdala hyperactivity resulting from the presentation of threatening stimuli (fearful faces) in patients with generalized social anxiety disorder.”
BackgroundAn affective neuroscience model of boosting resilience in adults
Tabibnia, G. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.05.005 · Cited by 109 · see citing works
Quintana, D. S., Westlye, L. T., Alnæs, D., Rustan, Ø. G., Kaufmann, T., Smerud, K. T., Mahmoud, R. A., Djupesland, P. G., & Andreassen, O. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.04.010 · Cited by 102 · see citing works
Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress.
Grimm, S., Pestke, K., Feeser, M., Aust, S., Weigand, A., Wang, J., Wingenfeld, K., Pruessner, J., Marca, R. L., Böker, H., et al. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu020 · Cited by 100 · see citing works
- Authors
- Labuschagne, I., Phan, K. L., Wood, A., Angstadt, M., Chua, P., Heinrichs, M., Stout, J. C., & Nathan, P. J.
- Affiliations
- Monash University (AU)
- University of Michigan (US)
- Royal Children's Hospital (AU)
- University of Freiburg (DE)
- University of Cambridge (GB)
- Corresponding author
- Nathan, Pradeep J
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2010-08-18
- Volume
- 35
- Issue
- 12
- Pages
- 2403-2413
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC3055328
- OpenAlex
- W2116280488
- Cited by
- 549
- References
- 91
- Citations by year
- 2026: 14 · 2025: 13 · 2024: 20 · 2023: 62 · 2022: 22 · 2021: 22 · 2020: 47 · 2019: 27 · 2018: 35 · 2017: 48 · 2016: 37 · 2015: 54 · 2014: 44 · 2013: 43 · 2012: 28
- FWCI
- 45.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Bank (Australian Catholic University) (submittedVersion)
- Own your potential (DEAKIN) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
- Aston Publications Explorer (Aston University) (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (114788)
- National Institute of Mental Health (MH076198, K23MH076198)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- oxytocin, generalized social anxiety disorder, amygdala reactivity, fear, emotional face processing, amygdala hyperactivity, intranasal administration, social danger
- MeSH terms
- Administration, Intranasal, Adult, Amygdala, Anxiety Disorders, Brain Mapping, Double-Blind Method, Facial Expression, Fear, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Oxytocin, Placebos, Psychomotor Performance
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