Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans
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The neuropeptide oxytocin enhances the processing of positive social stimuli and improves the capacity to effectively attend the eye region of conspecifics. To investigate the neural basis of these effects, we combined intranasal oxytocin administration with high-resolution functional magnetic resonance imaging in a unique emotion classification task. Emotional faces were briefly presented while controlling for the initial fixation, and measuring subsequent eye movements. Oxytocin had differential effects on the activity of specific amygdala subregions. On the one hand, it attenuated activation in lateral and dorsal regions of the anterior amygdala for fearful faces but enhanced activity for happy expressions, thus indicating a shift of the processing focus toward positive social stimuli. On the other hand, oxytocin increased the likelihood of reflexive gaze shifts toward the eye region irrespective of the depicted emotional expression. This gazing pattern was related to an increase of activity in the posterior amygdala and an enhanced functional coupling of this region to the superior colliculi. Thus, different behavioral effects of oxytocin seem to be closely related its specific modulatory influence on subregions within the human amygdala.
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Intranasal administration of 24 IU OT affects brain activity in humans.
“This dose, administered intranasally, has been shown in nonhuman primates to increase OT levels in cerebrospinal fluid significantly (54) and to modulate social behavior (65), as well as to affect brain activity (66) and phasic activity of the parasympathetic nervous system (67) in humans.”
From Oxytocin under opioid antagonism leads to supralinear enhancement of social attention (2017) · cites this paper as [66]
Separate oxytocin-application studies in humans indicate that there may be differential amygdala reactivity to fearful faces and fearful/threatening scenes in men and women.
“separate OXT-application studies in humans have indicated that there may be differential amygdala reactivity to fearful faces and fearful/threatening scenes in men (14, 15) and women (16, 17).”
From Oxytocin, the peptide that bonds the sexes also divides them (2016) · cites this paper as [14]
Previous studies indicate that oxytocin may induce sex-dependent changes in amygdala activation to emotional stimuli, but in opposite directions to the present findings.
“Previous studies on amygdala responses to fearful faces and fearful/threatening scenes (14 -17, 30) and social risk (31) have also indicated that OXT may induce sex-dependent changes in amygdala activation to emotional stimuli.”
From Oxytocin, the peptide that bonds the sexes also divides them (2016) · cites this paper as [14]
Activity of amygdala subregions is modulated by OXT.
“and the activity of amygdala subregions is also modulated by OXT (Gamer et al., 2010).”
From Oxytocin Modulates Social Distance between Males and Females (2012) · cites this paper as Gamer et al., 2010
In humans, alterations in amygdala responses to positive and negative emotions have been reported in neuropsychiatric conditions such as autism and schizophrenia, in association with OXTR genetic variants or following intranasal OXT.
“In humans, alterations in amygdala responses to positive and negative emotions have been reported in neuropsychiatric conditions, such as autism and schizophrenia [72,73], in association with OXTR genetic variants [41,102] or following intranasal OXT [33,36,38,103].”
From Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice (2019) · cites this paper as [103]
The insula and amygdala seem to be key target regions in the brain, with oxytocin modulating amygdala responsiveness to emotional faces or social stimuli in general.
“In this context, the insula17 as well as the amygdala seem to be key target regions in the brain, with oxytocin modulating amygdala responsiveness to emotional faces18–22 or social stimuli in general23.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [21]
Studies examining neural responses to aversive stimuli in men without an ASD diagnosis have repeatedly demonstrated decreased amygdala activation, interpreted as a neural mechanism underlying oxytocin's anxiolytic effects.
“These studies have repeatedly demonstrated decreased amygdala activation, which has been interpreted as a neural mechanism underlying oxytocin’s anxiolytic effects18,20,21.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [21]
Intranasal OXT administration in healthy humans attenuates activation of the amygdala to social stimuli.
“attenuating activation of amygdala to social stimuli (Baumgartner et al, 2008;Domes et al, 2007a;Gamer et al, 2010;Kirsch et al, 2005)”
From Chronic and acute intranasal oxytocin produce divergent social effects in mice (2014) · cites this paper as Gamer et al, 2010
Gamer and colleagues found that oxytocin's effects on amygdala activity elicited by emotional faces was dependent on the valence of stimuli but the effects of oxytocin on enhancement of gaze shifts towards the eyes was valence independent.
“Gamer and colleagues found that oxytocin’s effects on amygdala activity elicited by emotional faces was dependent on the valence of stimuli but the effects of oxytocin on enhancement of gaze shifts towards the eyes was valence independent (Gamer et al., 2010).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Gamer et al., 2010
Oxytocin suppresses amygdala activation for fearful faces but enhances activity for happy faces.
“In addition, oxytocin suppresses amygdala activation for fearful faces but enhances activity for happy faces (Gamer et al., 2010).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Gamer et al., 2010
Oxytocin decreases amygdala activation during the perception of fear-inducing or aversive social stimuli.
“Oxytocin decreases amygdala activation during the perception of fear-inducing or aversive social stimuli; it has been suggested that this explains the stress-reducing effects of oxytocin (Gamer et al., 2010;Riem et al., 2011).”
From Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal (2013) · cites this paper as Gamer et al., 2010
Decreased amygdala activation might be the underlying neural mechanism of the anxiolytic effects of oxytocin.
“Because projections between the amygdala and brainstem are involved in fear behavior and arousal (LeDoux, 2000) it has been suggested that decreased amygdala activation might be the underlying neural mechanism of the anxiolytic effects of oxytocin (Gamer et al., 2010;Riem et al., 2011).”
From Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal (2013) · cites this paper as Gamer et al., 2010
Research in humans has almost exclusively focused on oxytocin's role in prosocial behavior, largely ignoring its potential effects on ingestive behavior and metabolism.
“Research in humans has almost exclusively focused on the role of oxytocin in the regulation of prosocial behavior, including trust, attachment, and sexual behavior (2–5), largely ignoring potential effects of the neuropeptide on ingestive behavior and metabolism.”
From Oxytocin Reduces Reward-Driven Food Intake in Humans (2013) · cites this paper as [4]
Intranasal oxytocin administration reliably modulates neuropsychological functions in humans in the absence of relevant side effects.
“intranasal oxytocin administration has been shown to reliably modulate neuropsychological functions in a series of studies (2–5) in the absence of relevant side effects (16).”
From Oxytocin Reduces Reward-Driven Food Intake in Humans (2013) · cites this paper as [4]
Intranasal OT in humans increases time spent visually inspecting the eye region of faces compared to placebo.
“Following intranasal OT (Syntocinon spray, Novartis), humans spend more time visually inspecting the eye region of faces compared to placebo (i.e., all inactive ingredients except for the peptide) (Gamer et al., 2010; Guastella et al., 2008).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Gamer et al., 2010
OT inhalation reduces amygdala activation when viewing fearful faces but increases amygdala activation when viewing happy faces.
“Furthermore, OT inhalation reduces amygdala activation when viewing fearful faces but increases amygdala activation when viewing happy faces (Gamer et al., 2010).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Gamer et al., 2010
Activity of amygdala sub-regions is modulated by oxytocin.
“Importantly, the activity of amygdala sub-regions has been shown to be modulated by the neuropeptide oxytocin (OT; Gamer et al., 2010;Hurlemann et al., 2010), indicating that OT is a candidate hormone for modulating interpersonal distance.”
From OT promotes closer interpersonal distance among highly empathic individuals (2015) · cites this paper as Gamer et al., 2010
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“In addition, oxytocin suppresses amygdala activation for fearful faces but enhances activity for happy faces (Gamer et al. , 2010).”
The amygdala as a hub in brain networks that support social life
Bickart, K. C., Dickerson, B. C., & Feldman Barrett, L. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.08.013 · Cited by 344 · see citing works
“In response to fearful faces, OXT diminishes activity in the rostral amygdala in the vicinity of a nuclear group that includes the central nucleus (Gamer et al., 2010) and suppresses amygdala coupling with regions of the brainstem (Kirsch et al., 2005), suggesting a role for OXT in the amygdala…”
BackgroundVan IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.008 · Cited by 365 · see citing works
Rilling, J. K., DeMarco, A. C., Hackett, P. D., Chen, X., Gautam, P., Stair, S., Haroon, E., Thompson, R., Ditzen, B., Patel, R., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.022 · Cited by 343 · see citing works
“The left amygdala ROI was defined as a 10 mm-side cube centered on the coordinates of the activation peak reported in Gamer et al. (Gamer et al., 2010), after converting from MNI to Talairach coordinates, and then manually adjusting the ROI location to more closely match the anatomical features of the MNI template.”
MethodInfluentialA review of safety, side-effects and subjective reactions to intranasal oxytocin in human research
MacDonald, E., Dadds, M. R., Brennan, J. L., Williams, K., Levy, F., & Cauchi, A. J. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.02.015 · Cited by 352 · see citing works
Oxytocin enhances brain function in children with autism
Gordon, I., Vander Wyk, B. C., Bennett, R. H., Cordeaux, C., Lucas, M. V., Eilbott, J. A., Zagoory-Sharon, O., Leckman, J. F., Feldman, R., & Pelphrey, K. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312857110 · Cited by 336 · see citing works
“In animals, intranasal OT can excite neuronal populations in the amygdala (52), with different amygdala subregions mediating the variable impacts of OT on attention to affective social stimuli (53).”
BackgroundEmotion and cognition and the amygdala: From “what is it?” to “what's to be done?”
Pessoa, L. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.06.038 · Cited by 403 · see citing works
Rilling, J. K., DeMarco, A. C., Hackett, P. D., Thompson, R., Ditzen, B., Patel, R., & Pagnoni, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.013 · Cited by 303 · see citing works
“OT appears to reduce the salience of negative social stimuli and increase the salience of positive social stimuli (Heinrichs et al., 2003; Baumgartner et al., 2008; Guastella et al., 2008; Petrovic et al., 2008; Unkelbach et al., 2008; Heinrichs et al., 2009; Theodoridou et al., 2009; Gamer et al., 2010).”
InfluentialOxytocin Modulates Social Distance between Males and Females
Scheele, D., Striepens, N., Güntürkün, O., Deutschländer, S., Maier, W., Kendrick, K. M., & Hurlemann, R. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2755-12.2012 · Cited by 298 · see citing works
“, 2009) and the activity of amygdala subregions is also modulated by OXT (Gamer et al., 2010).”
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
“More recent studies suggest a difference in the effect of OT on amygdala activation that is related to the valence of emotional stimuli (Gamer et al., 2010).”
BackgroundResultInfluentialProsocial 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
“[64] reported attenuated activation in lateral and dorsal regions of the anterior amygdala for fearful faces but enhanced activity for happy expressions, an effect interpreted as a shift of the processing focus toward positive social stimuli.”
BackgroundThe animal and human neuroendocrinology of social cognition, motivation and behavior
McCall, C., & Singer, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3084 · Cited by 273 · see citing works
Nasal oxytocin for social deficits in childhood autism: A randomized controlled trial
Dadds, M. R., MacDonald, E., Cauchi, A., Williams, K., Levy, F., & Brennan, J. (2014) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-013-1899-3 · Cited by 250 · 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
Effects of intranasal oxytocin on the neural basis of face processing in autism spectrum disorder
Domes, G., Heinrichs, M., Kumbier, E., Grossmann, A., Hauenstein, K., & Herpertz, S. C. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.02.007 · Cited by 255 · see citing works
“Initial studies in healthy humans show that oxytocin, a nine– amino acid neuropeptide, reduces anxiety and endocrine responses to social stress (18,19), modulates social memory (20–22), promotes trust in social interactions (23), improves the ability to infer the emotional or mental states of others from subtle facial…”
BackgroundAuyeung, 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
Nonapeptide mechanisms of social cognition, behavior and species-specific social systems
Goodson, J. L., & Thompson, R. R. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.08.020 · Cited by 261 · see citing works
“Figure adapted with permission from [50].”
Prefrontal–amygdala circuits in social decision-making
Gangopadhyay, P., Chawla, M., Monte, O. D., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00738-9 · Cited by 247 · see citing works
The 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
Kinetics and dose dependency of intranasal oxytocin effects on amygdala reactivity
Spengler, F. B., Schultz, J., Scheele, D., Essel, M., Maier, W., Heinrichs, M., & Hurlemann, R. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.04.015 · Cited by 229 · see citing works
“It is noteworthy that the modulatory effect of OXT on responses to fearful faces in the left amygdala found here is consistent with observations in previous studies (8,12), while other studies (7) pinpointed the OXT effect in the right amygdala.”
ResultChen, F. S., Kumsta, R., von Dawans, B., Monakhov, M., Ebstein, R. P., & Heinrichs, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113079108 · Cited by 268 · see citing works
Lischke, A., Berger, C., Prehn, K., Heinrichs, M., Herpertz, S. C., & Domes, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.015 · Cited by 221 · see citing works
“…by the finding that OT increases gaze to the eye region of neutral (Guastella et al., 2008a; Andari et al., 2010) and emotional expressions (Gamer et al., 2010) and that OT enhances the ability to infer an opponent’s mental state from subtle cues around the eye region (Domes et al., 2007;…”
BackgroundMethodResultInfluentialOxytocin Reduces Reward-Driven Food Intake in Humans
Ott, V., Finlayson, G., Lehnert, H., Heitmann, B., Heinrichs, M., Born, J., & Hallschmid, M. (2013) · Diabetes · doi:10.2337/db13-0663 · Cited by 226 · see citing works
“intranasal oxytocin administration has been shown to reliably modulate neuropsychological functions in a series of studies (2-5) in the absence of relevant side effects (16).”
BackgroundGroppe, S. E., Gossen, A., Rademacher, L., Hahn, A., Westphal, L., Gründer, G., & Spreckelmeyer, K. N. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.12.023 · Cited by 218 · see citing works
“Although discordant with studies in male participants suggesting that oxytocin reduces arousal in response to threatening social stimuli [(5,10,11) but see (44) for an alternative account], our finding is well in line with a recent study suggesting enhanced arousal toward threatening social cues under oxytocin in null…”
BackgroundResultBaribeau, D. A., & Anagnostou, E. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00335 · Cited by 229 · see citing works
“For example, more than one study has shown that oxytocin increased amygdala activation in response to positive social information (Gamer et al., 2010; Rilling et al., 2012).”
BackgroundPuglia, 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
“(43) found that after oxytocin administration, amygdala response decreased in response to angry faces but increased when viewing happy faces.”
BackgroundGenetic 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
“fMRI studies have shown that oxytocin exerts influence on important neural circuits for a wide range of social–cognitive abilities such as eye gaze, mentalizing, emotion recognition, and learning [18, 46, 47, 57, 83, 89, 110, 117].”
BackgroundOxytocin 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
Bertsch, K., Gamer, M., Schmidt, B., Schmidinger, I., Walther, S., Kästel, T., Schnell, K., Büchel, C., Domes, G., & Herpertz, S. C. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.13020263 · Cited by 214 · see citing works
Self-citationOxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice
Ferretti, V., Maltese, F., Contarini, G., Nigro, M., Bonavia, A., Huang, H., Gigliucci, V., Morelli, G., Scheggia, D., Managò, F., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.04.070 · Cited by 212 · see citing works
“In humans, alterations in amygdala responses to positive and negative emotions have been reported in neuropsychiatric conditions, such as autism and schizophrenia [72, 73], in association with OXTR genetic variants [41, 102] or following intranasal OXT [33, 36, 38, 103].”
BackgroundOxytocin, the peptide that bonds the sexes also divides them
Gao, S., Becker, B., Luo, L., Geng, Y., Zhao, W., Yin, Y., Hu, J., Gao, Z., Gong, Q., Hurlemann, R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602620113 · Cited by 186 · see citing works
“The amygdala has a sexually dimorphic distribution and expression of OXT receptors in nonprimate mammals (12, 13), and separate OXT-application studies in humans have indicated that there may be differential amygdala reactivity to fearful faces and fearful/threatening scenes in men (14, 15) and women (16, 17).”
BackgroundChronic and acute intranasal oxytocin produce divergent social effects in mice
Huang, H., Michetti, C., Busnelli, M., Managò, F., Sannino, S., Scheggia, D., Giancardo, L., Sona, D., Murino, V., Chini, B., et al. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.310 · Cited by 199 · see citing works
“…of OXT in healthy subjects (Baumgartner et al, 2008; Buchheim et al, 2009; Ditzen et al, 2009; Domes et al, 2007a; Domes et al, 2007b; Gamer et al, 2010; Guastella et al, 2010; Heinrichs et al, 2003; Kirsch et al, 2005; MacDonald et al, 2011; Rimmele et al, 2009), whereas prolonged…”
BackgroundSocial “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications
Kohls, G., Chevallier, C., Troiani, V., & Schultz, R. T. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-10 · Cited by 197 · see citing works
“[157-163].”
Oxytocin increases amygdala reactivity to threatening scenes in females
Lischke, A., Gamer, M., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., Herpertz, S. C., & Domes, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.01.011 · Cited by 194 · see citing works
“…OT decreases amygdala reactivity to aversive, threat-related scenes (Kirsch et al., 2005) and fearful, threat-related faces (Domes et al., 2007a; Gamer et al., 2010; Kirsch et al., 2005; Petrovic et al., 2008) in males, but increases amygdala reactivity to similar faces in females (Domes et…”
BackgroundInfluentialSelf-citationAtypical Reflexive Gaze Patterns on Emotional Faces in Autism Spectrum Disorders
Kliemann, D., Dziobek, I., Hatri, A., Steimke, R., & Heekeren, H. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0688-10.2010 · Cited by 194 · see citing works
“In typically developed controls, the amygdala seems to be not only involved in orienting toward socially salient stimuli (Gamer and Büchel, 2009; Gamer et al., 2010), but also in fear and aversion processing (LeDoux et al.”
BackgroundRiem, M. M. E., van IJzendoorn, M. H., Tops, M., Boksem, M. A. S., Rombouts, S. A. R. B., & Bakermans-Kranenburg, M. J. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.313 · Cited by 191 · see citing works
“This is supported by a study of Gamer et al (2010), who showed that oxytocin increased functional coupling between the amygdala and the superior colliculus as well as gaze changes towards the eyes of an emotional stranger in order to facilitate the classification of the emotion.”
BackgroundResultFreeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.023 · Cited by 185 · see citing works
“Indirect support for this idea comes from an IN-OT study in humans that reported increased functional coupling between the SC and the amygdala during a face viewing task (Gamer et al., 2010).”
ResultThe role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders
Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., & Heekeren, H. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5294-11.2012 · Cited by 183 · see citing works
“Within normal functioning, an increase in amygdala activation seems to be associated with immediate orientation toward the eyes (Gamer and Büchel, 2009; Gamer et al., 2010).”
BackgroundResultInfluentialWatanabe, T., Abe, O., Kuwabara, H., Yahata, N., Takano, Y., Iwashiro, N., Natsubori, T., Aoki, Y., Takao, H., Kawakubo, Y., et al. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.3181 · Cited by 183 · see citing works
CSF and blood oxytocin concentration changes following intranasal delivery in macaque
Dal Monte, O., Noble, P. L., Turchi, J., Cummins, A., & Averbeck, B. B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103677 · Cited by 177 · see citing works
“From neuroimaging studies, OT has been shown to modulate amygdala activity in response to threatening social stimuli [14], pain [15], and emotional faces [16].”
BackgroundOxytocin increases recognition of masked emotional faces
Schulze, L., Lischke, A., Greif, J., Herpertz, S. C., Heinrichs, M., & Domes, G. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.011 · Cited by 180 · see citing works
“However, enhanced activity for dorsal and lateral subregions of the amygdala for happy faces presented for 150 ms was reported recently (Gamer et al., 2010), which might be associated with enhanced emotion recognition performance as shown in the present study.”
InfluentialWigton, 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
“001 1182 Left BA 13 (222) Left BA 22 (219) Left BA 38 (174) Left BA 6 (165) Left BA 21 (120) Left BA 43 (70) Left BA 44 (39) Left BA 4 (37) Left BA 47 (31) Left BA 42 (26) Left BA 9 (19) Left BA 20 (12)”
Barrett, J., Wonch, K. E., Gonzalez, A., Ali, N., Steiner, M., Hall, G. B., & Fleming, A. S. (2012) · Social Neuroscience · doi:10.1080/17470919.2011.609907 · Cited by 177 · see citing works
“Interestingly, a recent study by Gamer, Zurowski, and Büchel (2010) found that the administration of oxytocin, a neuropeptide important in attachment and bonding, enhanced the response of the lateral amygdala to happy adult facial expressions (Gamer et al., 2010).”
BackgroundHuman 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
“On the other hand, oxytocin enhanced activity in a posterior amygdala subregion (likely corresponding to the basal nucleus) when face stimuli triggered a redirection of social attention to the eyes, irrespective of the emotional valence (Gamer et al., 2010).”
BackgroundResultInfluentialOxytocin, testosterone, and human social cognition
Crespi, B. J. (2015) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12175 · Cited by 175 · see citing works
Intranasal 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
“(2010) showed that a differential pattern of amygdala activation occurs: a decrease in the lateral and dorsal regions of the anterior amygdala (after fearful faces) concurred with an increase in the posterior amygdala related to gazing shifts and an enhanced coupling to the superior colliculus.”
BackgroundKemp, A. H., Quintana, D. S., Kuhnert, R.-L., Griffiths, K., Hickie, I. B., & Guastella, A. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044014 · Cited by 158 · see citing works
“Neuroimaging research has demonstrated that the effects of OT are dependent on the nature of the stimulus, such that OT attenuates amygdala activation for fearful faces, but enhances activity for happy faces [8].”
BackgroundA model of differential amygdala activation in psychopathy
Moul, C., Killcross, S., & Dadds, M. R. (2012) · Psychological Review · doi:10.1037/a0029342 · Cited by 159 · see citing works
Domes, G., Kumbier, E., Heinrichs, M., & Herpertz, S. C. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.254 · Cited by 160 · 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
“Intranasal OT reliably modulates hemodynamic activity in the amygdala in healthy humans (28, 29, 31), children with autism (32), and rhesus macaques (30).”
BackgroundEllingsen, D.-M., Wessberg, J., Chelnokova, O., Olausson, H., Laeng, B., & Leknes, S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.017 · Cited by 153 · see citing works
“Intranasally administered oxytocin improves the ability to ‘‘read’’ others emotions (Domes et al., 2007; Bartz et al., 2010; Leknes et al., 2012; Van IJzendoorn and Bakermans-Kranenburg, 2012) and enhances social attention (Gamer et al., 2010; Ellenbogen et al., 2012).”
Face processing in autism spectrum disorders: From brain regions to brain networks
Nomi, J. S., & Uddin, L. Q. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.03.029 · Cited by 155 · see citing works
Oxytocin enhances pupil dilation and sensitivity to 'hidden' emotional expressions
Leknes, S., Wessberg, J., Ellingsen, D.-M., Chelnokova, O., Olausson, H., & Laeng, B. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss062 · Cited by 151 · see citing works
“Related studies have demonstrated effects of centrally enhanced oxytocin on social memory, behaviour in economic games, social attention and the focus of eye gaze (e.g. Kosfeld et al., 2005; Guastella et al., 2008; Unkelbach et al., 2008; Gamer et al., 2010; Ellenbogen et al., 2012).”
BackgroundLonstein, J. S., Lévy, F., & Fleming, A. S. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.011 · Cited by 151 · 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
“Higher-resolution imaging studies have now begun to elucidate the specific amygdala subregions responsible for these effects (Gamer et al., 2010).”
BackgroundOxytocin׳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
Gur, R., Tendler, A., & Wagner, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.022 · Cited by 144 · see citing works
Emotion recognition and oxytocin in patients with schizophrenia
Averbeck, B. B., Bobin, T., Evans, S., & Shergill, S. S. (2011) · Psychological Medicine · doi:10.1017/s0033291711001413 · Cited by 144 · see citing works
“2008a), an effect mediated by interactions between the amygdala and brain stem regions involved in saccade generation (Gamer et al. 2010).”
BackgroundOxytocin differentially modulates eye gaze to naturalistic social signals of happiness and anger
Domes, G., Steiner, A., Porges, S. W., & Heinrichs, M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.10.002 · Cited by 139 · see citing works
“Whereas a previous study showed that OT can enhance reflexive saccades toward the eye region of very briefly presented emotional faces regardless of valence (Gamer et al., 2010), our results seem to reflect a modulation of visual attention depending on the social signal communicated by the presented expression when th…”
InfluentialLabuschagne, 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
“2007), although valence-dependent modulation has been observed in subregions within the amygdala (Gamer et al. 2010).”
BackgroundHarari-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
“(83) suggest that oxytocin exerts different effects on subregionsof the amygdala.”
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
“Following a standardized protocol used in previous studies [Domes et al., 2013; Gamer and Buchel, 2012; Gamer et al., 2010; Hurlemann et al., 2010; Labuschagne et al., 2010], participants selfadministered a single intranasal dose of 24 IU OXT/PLA (three puffs per nostril, each puff with 4 IU, or 6.”
MethodRiem, M. M. E., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Out, D., & Rombouts, S. A. R. B. (2012) · Attachment & Human Development · doi:10.1080/14616734.2012.727252 · Cited by 134 · see citing works
Oxytocin blunts social vigilance in the rhesus macaque
Ebitz, R. B., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305230110 · Cited by 132 · see citing works
“OT thus promotes gaze to the eye region in rhesus macaques, replicating previous reports in humans (8, 10, 11).”
BackgroundResultInfluentialLukas, M., & Neumann, I. D. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.016 · Cited by 133 · see citing works
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
“, happy face [42,70] or partner's or own child's images [75,76]), anticipating social reward [74], and engaging in positive social interactions (e.”
BackgroundInfluentialIntranasal oxytocin increases covert attention to positive social cues
Domes, G., Sibold, M., Schulze, L., Lischke, A., Herpertz, S. C., & Heinrichs, M. (2013) · Psychological Medicine · doi:10.1017/s0033291712002565 · Cited by 130 · see citing works
“For instance, previous studies on OT and face processing have reported an increased number of saccades towards the eye region (Guastella et al. 2008 ; Gamer et al. 2010), suggesting that OT modulates overt visual attention during the processing of social cues.”
ResultIntranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions
Parr, L. A., Modi, M., Siebert, E., & Young, L. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.011 · Cited by 124 · see citing works
“Human studies have reported a wide range of effects of IN-OT on socio-emotional behavior and social cognition, including increased salience of the eyes in faces, more accurate emotion recognition (Domes et al., 2007a; Fischer-Shofty et al., 2010; Gamer et al., 2010; Guastella et al., 2008; Savaskan et al., 2008), impr…”
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
Dai, L., Carter, C. S., Ying, J., Bellugi, U., Pournajafi-Nazarloo, H., & Korenberg, J. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038513 · Cited by 119 · see citing works
“Nonetheless, with the caveats above, our findings combine with recent work [43,88] employing intranasal OT and fMRI, to suggest not-unreasonal hypotheses indicating the neural networks that may modulate social behavior in WS.”
BackgroundResultInfluentialGrace, 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
“When broken down into task type: 14 studies used tasks that included facial emotion or aversive stimuli (Domes et al., 2013; Domes et al., 2014; Domes et al., 2010; Frijling et al., 2016; Gamer et al., 2010; Gordon et al., 2016; Grimm et al., 2014; Koch et al., 2016a; Lischke et al., 2012; Petrovic et al., 2008; Pincu…”
InfluentialOxytocin 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
“In order to address potential confounding effects of OT on social attention, eye movements can be assessed as a physiological correlate of visual attention processes during MRI scanning (Domes et al., 2013b; Gamer et al., 2010; Guastella et al., 2008).”
BackgroundMethodResultInfluentialOverview of human oxytocin research
Kendrick, K. M., Guastella, A. J., & Becker, B. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_19 · Cited by 121 · see citing works
The Associations Between Oxytocin and Trauma in Humans: A Systematic Review
Donadon, M. F., Martín‐Santos, R., & Osório, F. D. L. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00154 · Cited by 119 · see citing works
“According to their findings and the previous literature (Kirsch et al., 2005; Domes et al., 2007; Gamer et al., 2010), the effects of OXT on amygdala reactivity might differ not only because of inter-individual factors such as gender and level of psychopathology but also because of the context…”
Diagnostic Features of Emotional Expressions Are Processed Preferentially
Scheller, E., Büchel, C., & Gamer, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041792 · Cited by 116 · see citing works
“Any ‘‘reflexive’’ saccade that is related to the stimulus presentation would start when the picture already disappeared from the screen (for a similar procedure see [11,18]).”
BackgroundNeural, cognitive, and evolutionary foundations of human altruism
Marsh, A. A. (2015) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1377 · Cited by 119 · see citing works
“Together, these findings suggest that when indications of vulnerability and distress are paired— whether in the form of actual infant distress cries or infantile-looking fearful expressions—the information converges in the amygdala, perhaps in the lateral division of the central nucleus, stimulating oxytocinmediated i…”
BackgroundOxytocin and vasopressin support distinct configurations of social synchrony
Apter-Levi, Y., Zagoory-Sharon, O., & Feldman, R. (2014) · Brain Research · doi:10.1016/j.brainres.2013.10.052 · Cited by 116 · see citing works
“Regions characterized as part of the AVP circuitry are implicated in socio-cognitive processes in both humans and rodents (Goodson and Thompson, 2010).”
Gordon, I., Jack, A., Pretzsch, C. M., Vander Wyk, B., Leckman, J. F., Feldman, R., & Pelphrey, K. A. (2016) · Scientific Reports · doi:10.1038/srep35054 · Cited by 114 · see citing works
Riem, M. M. E., Bakermans‐Kranenburg, M. J., Huffmeijer, R., & van IJzendoorn, M. H. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.12.023 · Cited by 114 · see citing works
“These anxiolytic effects may be mediated by the inhibitory influence of oxytocin on the amygdala (Kirsch et al., 2005; Gamer et al., 2010; Riem et al., 2011), a brain region involved in fear processing (MacLean, 1990).”
BackgroundGoldman, M. B., Gomes, A. M., Carter, C. S., & Lee, R. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2193-8 · Cited by 112 · see citing works
“Intranasal oxytocin enhances facial affect discrimination (Marsh et al. 2007) and specifically reduces detection of fear in nonfearful faces (Fischer-Shofty et al. 2010) perhaps by diminishing amygdala activity (Kirsch et al. 2005; Domes et al. 2007a; Gamer et al. 2010).”
BackgroundThe Eyes as Windows Into Other Minds
Großmann, T. (2017) · Perspectives on Psychological Science · doi:10.1177/1745691616654457 · Cited by 116 · see citing works
“Findings by Gamer, Zurowski, and Büchel (2010) seemed to indicate that at the brain level, the amygdala plays a mediating role in driving these effects of oxytocin on eye-cue detection.”
Backgroundde Visser, E., Monfort, S. S., Goodyear, K., Lu, L., O'Hara, M., Lee, M. R., Parasuraman, R., & Krueger, F. (2017) · Hum. Factors · doi:10.1177/0018720816687205 · Cited by 104 · see citing works
Oxytocin in schizophrenia: a review of evidence for its therapeutic effects
MacDonald, K. S., & Feifel, D. (2011) · Acta Neuropsychiatrica · doi:10.1111/j.1601-5215.2011.00634.x · Cited by 111 · see citing works
- Authors
- Gamer, M., Zurowski, B., & Büchel, C.
- Affiliations
- University Medical Center Hamburg-Eppendorf (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-04-26
- Volume
- 107
- Issue
- 20
- Pages
- 9400-9405
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2889107
- OpenAlex
- W2077718235
- Cited by
- 487
- References
- 53
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 14 · 2023: 16 · 2022: 18 · 2021: 25 · 2020: 38 · 2019: 16 · 2018: 31 · 2017: 40 · 2016: 30 · 2015: 38 · 2014: 43 · 2013: 59 · 2012: 46
- FWCI
- 68.76
- Type
- journal article
- Language
- en
- Update notices
- correction (2011-01-18)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Bundesministerium für Bildung und Forschung
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin, amygdala subregions, emotional face processing, valence, attentional bias, gaze shifts, eye movements, superior colliculus, social cognition
- MeSH terms
- Adult, Amygdala, Attention, Double-Blind Method, Emotions, Eye Movements, Face, Germany, Humans, Magnetic Resonance Imaging, Male, Oxytocin, Photic Stimulation
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