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Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans
Open accessAbstract
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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In the citing paper
“Functioning as both a neurotransmitter and a hormone, oxytocin's targets are widespread and include the hippocampus and the amygdala (10–12).”
From Oxytocin promotes human ethnocentrism (2011) · cites this paper as [12]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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
The cited source says what the claim attributes to it.
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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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Citations
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BackgroundInfluential
Cited by
Sorted by citations
Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
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“Indeed, it has been suggested that OT elevates both the number of saccades towards the eye region (33, 74), enhances stimulus-induced pupil dilation (22), increases orienting of attention in response to emotional gaze cues (75), as well as attentional shifts towards happy facial expressions presented for 100 ms (76).”
Oxytocin promotes human ethnocentrism
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Oxytocin Attenuates Amygdala Reactivity to Fear in Generalized Social Anxiety Disorder
Labuschagne, I., Phan, K. L., Wood, A., Angstadt, M., Chua, P., Heinrichs, M., Stout, J. C., & Nathan, P. J. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.123 · Cited by 549
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“Notably, the neuropeptides oxytocin (OXT) and arginine vasopressin as well as melatonin and insulin were shown to efficiently alter neuronal, behavioral and physiological parameters after intranasal delivery in humans (Thompson et al., 2004; Kirsch et al., 2005; Benedict et al., 2006; Reger et al., 2008; Shamay-Tsoory…”
BackgroundSurvival of the Friendliest: Homo sapiens Evolved via Selection for Prosociality
Hare, B. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-010416-044201 · Cited by 444
“In particular, oxytocin is known to modulate mutual gaze and increase attention to the eyes of others in humans (Gamer et al. 2010, Guastella et al. 2008).”
BackgroundBos, 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
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“…OT administration has been shown to affect many aspects of human sociability ranging from social perception, increased gazing toward the eye region (Gamer et al, 2010; Guastella et al, 2008), and improved recognition of emotional facial expressions (Domes et al, 2007; Savaskan et al, 2008) to…”
BackgroundBakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.34 · Cited by 383
“Participants were instructed to classify briefly presented negative (fearful), positive (happy) or neutral facial expressions as quickly and accurately as possible.(46) OT decreased activity in lateral and dorsal regions of the anterior amygdala when viewing fearful faces, and stimulated activity in these parts in res…”
BackgroundGraustella, A. J., & MacLeod, C. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.002 · Cited by 379
Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M., van IJzendoorn, M. H., & Rombouts, S. A. R. B. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.006 · Cited by 366
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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
“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
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“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
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“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
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“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 301
“, 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
“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
“[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
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Oxytocin facilitates protective responses to aversive social stimuli in males
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“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
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“Figure adapted with permission from [50].”
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“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
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“…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
“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
“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 241
“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
“(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
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“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
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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
“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
“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
“…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
“[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
“…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 212
“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
“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
“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
“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
Oxytocin 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
“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
“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
“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).”
BackgroundCSF 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
“From neuroimaging studies, OT has been shown to modulate amygdala activity in response to threatening social stimuli [14], pain [15], and emotional faces [16].”
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
“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 183
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
“(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.”
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
Domes, G., Kumbier, E., Heinrichs, M., & Herpertz, S. C. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.254 · Cited by 160
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
“Intranasal OT reliably modulates hemodynamic activity in the amygdala in healthy humans (28, 29, 31), children with autism (32), and rhesus macaques (30).”
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
“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].”
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
“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 168
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
“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 158
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
“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
Gur, R., Tendler, A., & Wagner, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.022 · Cited by 144
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 148
“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
“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 144
“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 143
Herpertz, S. C., & Bertsch, K. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15020216 · Cited by 147
“(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 142
“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
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
“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 136
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
“, 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
“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
“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
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
“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
“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
“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
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 126
“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
“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 122
“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
“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
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
“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
“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 127
“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.”
BackgroundA Little Anthropomorphism Goes a Long Way
de Visser, E. J., Monfort, S. S., Goodyear, K., Lu, L., O’Hara, M., Lee, M. R., Parasuraman, R., & Krüeger, F. (2017) · Human Factors The Journal of the Human Factors and Ergonomics Society · doi:10.1177/0018720816687205 · Cited by 118
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 117
Metadata
- 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
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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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