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To mirror or not to mirror upon mutual gaze, oxytocin can pave the way: A cross-over randomized placebo-controlled trial
Abstract and Figures
The eyes constitute a highly salient cue to communicate social intent. Previous research showed that direct eye contact between two individuals can readily evoke an increased propensity to ‘mirror’ other peoples’ actions. Considering the implicated role of the ‘prosocial’ neuropeptide oxytocin (OXT) in enhancing the saliency of social cues and modulating approach/avoidance motivational tendencies, the current study adopted the non-invasive brain stimulation technique transcranial magnetic stimulation (TMS) to explore whether a single dose of intranasal OXT (24 IU) modulated (enhanced) a person’s propensity to show heightened ‘mirroring’ or ‘motor resonance’ upon salient social cues, such as eye contact. The study involved a double-blind, placebo-controlled, cross-over trial with twenty-seven healthy adult men (18-31y). By applying single-pulse TMS over the primary motor cortex during movement observation, it was shown that motor resonance was significantly higher when movement observation was accompanied by direct, compared to averted gaze, but that a single dose of OXT did not uniformly enhance this effect. Significant moderations of the treatment effect were noted however, indicating that participants with high self-reports of attachment avoidance displayed a stronger OXT-treatment effect (enhancement of motor resonance upon direct eye contact), compared to participants with low attachment avoidance. Particularly, while participants with high attachment avoidance initially displayed a reduced propensity to increase their motor resonance upon direct eye contact, a single dose of OXT was able to promote an otherwise avoidant individual’s propensity to engage in motor resonance upon a salient social cue such as eye contact.
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... Recently, a series of TMS studies assessing corticospinal excitability extended this behavioral work by showing that activity within the mirror system is indeed enhanced when observed movements are accompanied by the actor's direct compared to averted gaze (Prinsen et al., 2017(Prinsen et al., , 2018Prinsen & Alaerts, 2019, 2020, thereby providing important support to the assumption that the mirror system underlies the encountered gaze-related modulations of mimicry in the Wang experiments. However, direct neurophysiological evidence in favor of an inappropriate mirror system modulation upon eye-to-eye contact within ASD, that is, paralleling the behavioral results by Forbes et al. (2017), is at the moment still lacking. ...
... In contrast to previous studies addressing gaze-related modulations of TMS-assessed corticospinal excitability during action observation (Prinsen et al., 2017(Prinsen et al., , 2018Prinsen & Alaerts, 2019, 2020, the ANOVA showed no Muscle  Gaze interaction (F[1, 50] = 0.10, p = 0.75, η 2 p = 0.002). Inspection of the data by means of singlesample t-test against zero suggests the possibility of a less specific muscle activation pattern mainly in the ASD group, as they showed significant direct and averted gaze-related enhancements compared to rest in both the experimental FDI and control ADM muscle. ...
... ASD, autism spectrum disorder; FDI, first dorsal interosseous; MEP, motor evoked potentials et al., 2005). Results within control participants were largely consistent with this principle, indicating enhanced MEPs (compared to rest) and gaze-related effects in the index finger FDI muscle, but not the little finger ADM muscle, during the observation of index finger movements (in line with Prinsen et al., 2017Prinsen et al., , 2018Prinsen & Alaerts, 2019, 2020. For participants with ASD however, the pattern of results was overall less muscle-specific. ...
Individuals with an autism spectrum disorder (ASD) experience persistent difficulties during social interactions and communication. Previously, it has been suggested that deficits in the so‐called “mirror system,” active during both action execution and observation, may underlie these social difficulties. It is still a topic of debate however whether deficiencies in the simulation of others' actions (i.e., “broken” mirroring) forms a general feature of ASD, or whether these mostly reflect a lack of social attunement. The latter would suggest an overall intact mirror system, but an impaired modulation of mirror activity according to variable social contexts. In this study, 25 adults with ASD and 28 age‐ and IQ‐matched control participants underwent transcranial magnetic stimulation during the observation of hand movements under variable conditions. Hand movements were presented via a live interaction partner, either without social context to assess basic motor mirroring or in combination with direct and averted gaze from the actor to assess socially modulated mirroring. Overall, no significant group differences were revealed, indicating no generally diminished mirror activity in ASD. Interestingly however, regression analyses revealed that, among ASD participants, higher symptom severity was associated with both reduced basic motor mirroring and aberrant socially modulated mirroring (i.e., no enhancement of mirror system activity upon observation of the interaction partner's direct vs. averted gaze). These findings further challenge the notion that mirror system dysfunctions constitute a principal feature of ASD, but demonstrate that variations in mirroring may be related to differential expressions of ASD symptom severity. Our findings show similar activity levels in brain regions responsible for action simulation and understanding in adults with autism, compared to adults without autism. However, the presence of more severe autism symptoms was linked to reduced activity in these regions. This suggests lower levels of brain activity during action understanding in some, but not all, persons with autism, which may contribute to the social difficulties these persons experience in daily life.
... Also in terms of mirror system activity, several TMS studies have shown that under various experimental conditions, perceived communicative intent from the actor -as conveyed by different gaze cues -significantly modulates corticospinal excitability (i.e. MEPs) in the observer [29][30][31][32] . To date however it remains unexplored whether suppression of the EEG mu rhythm upon action observation is similarly modulated by social context or communicative intent, as conveyed by eye contact. ...
... Based on previous findings in our lab 31 and following recent recommendations 37,38 , a naturalistic two-person paradigm was adopted, incorporating a live stimulus person to convey the gaze and movement cues. In line with previous TMS studies demonstrating enhanced mirroring of others' actions during eye-to-eye contact [29][30][31] , it was hypothesized that mirror system activation is enhanced during observation of movements accompanied with direct gaze from the actor, compared to movements accompanied with averted gaze from the actor. ...
... indicative of eye-to-eye contact) and (ii) that participants equally attend the hand area in both gaze conditions (i.e. rendering it unlikely that a shift in attention away from the stimulus space during averted gaze trials underlie the encountered effects) [29][30][31] . Nevertheless, future studies could benefit from the inclusion of an online measure of visual attention to provide a multifaceted investigation of dyadic eye contact processing. ...
Previous research has demonstrated that eye contact between actor and observer specifically enhances the ‘mirroring’ of others’ actions, as measured by transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEPs). However, it remains unknown whether other markers of mirror system activation, such as suppression of the EEG mu rhythm (8–13 Hz) over the sensorimotor strip, are also susceptible to perceived eye contact. Here, both TMS-induced MEPs and EEG mu suppression indices were assessed (in separate sessions) while 32 participants (mean age: 24y; 8m) observed a simple hand movement combined with direct or averted gaze from the actor. Both measures were significantly modulated by perceived eye gaze during action observation; showing an increase in MEP amplitude and an attenuation of the mu rhythm during direct vs. averted gaze. Importantly, while absolute MEP and mu suppression scores were not related, a significant association was identified between gaze-related changes in MEPs and mu suppression, indicating that both measures are similarly affected by the modulatory impact of gaze cues. Our results suggest that although the neural substrates underlying TMS-induced MEPs and the EEG mu rhythm may differ, both are sensitive to the social relevance of the observed actions, which might reflect a similar neural gating mechanism.
... Accordingly, perceiving the gaze of others has been shown to influence several socio-cognitive processes and behavioral responses in the observer (for relevant reviews, see Conty, George, & Hietanen, 2016;Hietanen, 2018;Senju & Johnson, 2009). In terms of mirror system activity, several TMS studies have shown that under various experimental conditions, perceived communicative intent from the actor (conveyed by different gaze cues) significantly modulates M1 excitability (MEP responses) in the observer (Betti et al., 2019;Prinsen & Alaerts, 2019;Prinsen et al., 2017;Prinsen, Brams, & Alaerts, 2018). To date however it remains unexplored whether suppression of the EEG mu rhythm upon action observation is similarly modulated by social context or communicative intent (i.e. as conveyed by eye contact). ...
... Based on the findings of Prinsen and Alaerts (2019), and following the recommendations by Reader and Holmes (2016), a naturalistic two-person paradigm was adopted, incorporating a 'live' stimulus person to convey the gaze and movement cues. In line with previous TMS studies demonstrating an effect of observed eye contact on the mirroring of others' actions (Prinsen & Alaerts, 2019;Prinsen et al., 2017Prinsen et al., , 2018, it was hypothesized that TMS-induced MEPs are enhanced upon movement observation accompanied with direct eye gaze, compared to movement observation accompanied with averted gaze. A key question was to assess whether suppression of the mu rhythm is also susceptible to a top-down response modulation by perceived communicative intent (i.e. ...
... was revealed. Thus, in accordance with previous TMS studies investigating the eye contact effect on M1 excitability (Prinsen & Alaerts, 2019;Prinsen et al., 2017Prinsen et al., , 2018, MEPs recorded from the FDI muscle were significantly higher when movement observation was accompanied with direct eye gaze from the stimulus person (mean: 0.231, SD: 0.356), compared to averted gaze (mean: 0.161, SD: 0.389). Note that no significant main or interaction effects were found for the categorical 'session' factor-of-no-interest (all p > .42). ...
Eye-to-eye contact is a salient cue for regulating everyday social interaction and communication. Previous research has demonstrated that direct eye contact between a live stimulus person and an observer specifically enhances the mirroring of others actions in the observer, as measured by transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEPs; an index of motor cortex excitability during action observation). However, it remains unknown whether other markers of mirror system activation, such as suppression of the EEG mu rhythm (i.e. attenuation of neural oscillations in the 8-13 Hz frequency band over the sensorimotor strip), are also susceptible to perceived eye contact. In the current study, a multimodal approach was adopted to assess both TMS-induced MEPs and EEG mu suppression (in separate sessions), while 32 participants (20 men; mean age: 24;8 years) observed a simple hand movement in combination with direct or averted gaze from the live stimulus person. Both indices of mirror system functioning were significantly modulated by perceived eye gaze; showing a significant increase in MEP amplitude and a significant attenuation of the mu rhythm when movement observation was accompanied with direct compared to averted gaze. Importantly, while inter-individual differences in absolute MEP and mu suppression scores were not significantly related, a significant association was identified between gaze-related changes in MEP responses and mu suppression. As such, it appears that while the neurophysiological substrates underlying mu suppression and TMS-induced MEP responses differ, both are similarly affected by the modulatory impact of gaze-related cues. In sum, our results suggest that both EEG mu rhythm and TMS-induced MEPs are sensitive to the social relevance of the observed actions, and that a similar neural substrate may drive gaze-related changes in these distinct markers of mirror system functioning.
... Several intranasal OT (IN-OT) administration studies have consistently shown that OT facilitates the recognition of emotional expressions from faces (Shahrestani, Kemp, & Guastella, 2013;van IJzendoorn & Bakermans-Kranenburg, 2012). Several studies also showed that OT increases the gaze time towards the eye region of faces both from static pictures (Guastella, Mitchell, & Dadds, 2008) (Eckstein et al., 2019) and during real-time interactions (Auyeung et al., 2015;Hall, Lightbody, McCarthy, Parker, & Reiss, 2012) (although see (Hubble et al., 2017;Lischke et al., 2012;Prinsen, Brams, & Alaerts, 2018) for contradictory results). With respect to OT's anxiolytic role, several studies have demonstrated decreases in subjective reports of anxiety and reductions in neuroendocrine stress responses (cortisol) after IN-OT (Heinrichs, Baumgartner, Kirschbaum, & Ehlert, 2003;Meinlschmidt & Heim, 2007;Riem, Kunst, Bekker, Fallon, & Kupper, 2019). ...
... securely attached individuals), the additional administration of IN-OT may not stimulate prosocial behavior further (Bartz et al., 2015). In line with the current observation of a modulatory impact of attachment avoidance, two prior studies of our lab also identified SAAM attachment avoidance to be a sensitive modulator of IN-OT treatment responses (Bernaerts et al., 2017;Prinsen et al., 2018). In one study, transcranial magnetic stimulation was adopted to assess automatic motor simulation (mirroring) of others actions and showed that, in avoidantly attached individuals -who otherwise show a low propensity to mirror -a single-dose of IN-OT was able to specifically enhance automatic motor . ...
... simulation (Prinsen et al., 2018). In the other study, young adult men were administered with a daily dose of OXT for a period of two weeks, and significant improvements in self-reports of attachment avoidance (SAAM) and attachment toward peers were revealed (Bernaerts et al., 2017). ...
The neuropeptide oxytocin (OT) is suggested to exert a pivotal role in a variety of complex human behaviors, including trust, attachment, social perception and fear-regulation. Previous studies have demonstrated that intranasal administration of OT reduces subjective and neuroendocrine stress responses and dampens amygdala reactivity. Moreover, OT has been proposed to modulate activity of the autonomic nervous system.
Here, we conducted a double-blind, placebo-controlled study with 56 men, to investigate whether a single-dose of OT (24 IU) modulates sympathetic autonomic arousal upon live dyadic gaze interactions. To do so, electro-dermal recordings of skin conductance were performed during the engagement of eye contact with a live model in a naturalistic two-person social context.
In accordance to prior research, direct eye gaze elicited a significant enhancement in skin conductance responses, but OT did not specifically enhance or dampen the overall magnitude (amplitude) of the autonomic arousal response. Administration of OT did facilitate the recovery of skin conductance responses back to baseline (increased steepness of recovery slope), indicating a role of OT in restoring homeostatic balance. Notably, the treatment-effect on autonomic recovery was most prominent in participants with low self-reported social responsiveness and high attachment avoidance, indicating that person-dependent factors play a pivotal role in determining OT treatment-responses. Behaviorally, OT significantly reduced self-reported feelings of tension and (at trend-level) worrying about how one presents oneself.
Together, these observations add further evidence to a role of OT in reducing subjective and autonomic stress responses, primarily by facilitating restoration of homeostatic balance after (social) stress-induced perturbation.
... These initial behavioral observations were recently extended by our laboratory by investigating the neurophysiological mechanism underlying the enhancing effect of eye gaze on automatic motor simulation, using transcranial magnetic stimulation (TMS) (Prinsen et al., 2017;Prinsen et al., 2018). Transcranial magnetic stimulation is a noninvasive method for stimulating cortical neurons via the administration of a brief magnetic pulse to the scalp. ...
... Importantly, Fadiga et al. (1995) demonstrated that when TMS is applied to M1 during the mere observation of others' actions, MEP amplitudes within the stimulated muscles are enhanced, indicating a muscle-specific and observation-induced facilitation of corticospinal excitability at the level of M1. Adopting this TMS technique, we have demonstrated that MEP amplitudes are significantly enhanced when participants observe actions accompanied with direct versus averted gaze from the model, indicating increased observation-induced M1 excitability upon mutual eye contact (Prinsen et al., 2017(Prinsen et al., , 2018. ...
... Furthermore, and in accordance to previous mirror system research adopting TMS (Fadiga et al., 1995;Strafella & Paus, 2000), the facilitatory effect of eye gaze on M1 excitability was shown to be specific to the muscle implicated in the observed movement. These findings extend results from previous behavioral studies (Wang & Hamilton, 2013;Wang, Newport, et al., 2011) and TMS studies from our laboratory (Prinsen et al., 2017(Prinsen et al., , 2018 showing Table 1. Means, standard deviations and Pearson correlations coefficients of self-report scores on the SRS (n = 22). ...
Previous research has shown a link between eye contact and interpersonal motor resonance, indicating that the mirroring of observed movements is enhanced when accompanied with mutual eye contact between actor and observer. Here, we further explored the role of eye contact within a naturalistic two-person action context. Twenty-two participants observed simple hand movements combined with direct or averted gaze presented via a live model in a two-person setting or via video recordings, while transcranial magnetic stimulation (TMS) was applied over the primary motor cortex (M1) to measure changes in M1 excitability. Skin conductance responses and gaze behavior were also measured to investigate the role of arousal and visual attention herein. Eye contact significantly enhanced excitability of the observer's M1 during movement observation within a two-person setting. Notably, participants with higher social responsiveness (Social Communication subscale of the SRS) displayed a more pronounced modulation of M1 excitability by eye gaze. Gaze-related modulations in M1 excitability were however not associated with differences in visual attention or autonomic arousal. In sum, the current study highlights the effectiveness and feasibility of adopting paradigms with high ecological validity for studying the modulation of mirror system processes by subtle social cues, such as eye gaze.
... Recently, a series of TMS studies extended this behavioral work by showing that activity within the MNS is enhanced when observed movements are accompanied by the actor's direct compared to averted gaze (Prinsen & Alaerts, 2019, 2020Prinsen et al., 2017;Prinsen, Brams, & Alaerts, 2018), thereby providing support to the notion that the MNS underlies the encountered gaze-related modulations of mimicry in the Wang experiments. ...
... Single-sample t-tests against zero showed that MEP amplitudes of the experimental FDI were significantly enhanced compared to rest ( (Prinsen & Alaerts, 2019, 2020Prinsen et al., 2017Prinsen et al., , 2018, there was no Muscle × Gaze interaction (F(1,50) = 0.10, p = .75, η²p = .002). ...
Individuals with an autism spectrum disorder (ASD) experience persistent difficulties during social interactions and communication. Previously, it has been suggested that deficits in the so-called ‘mirror neuron system’ (MNS), active during both action execution and observation, may underlie these social difficulties. It is still a topic of debate however whether deficiencies in the simulation of others’ actions (i.e. “broken” mirroring) forms a general feature of ASD, or whether these mostly reflect a lack of social attunement. The latter would suggest an overall intact MNS, but an impaired modulation of MNS activity according to variable social contexts. In this study, 25 adults with ASD and 28 age- and IQ-matched control participants underwent transcranial magnetic stimulation (TMS) during the observation of hand movements under variable conditions. Hand movements were presented via a live interaction partner, either without social context to assess basic motor mirroring, or in combination with direct and averted gaze from the acting model to assess socially modulated mirroring. Overall, no significant group differences were revealed, indicating no differential in MNS activity in ASD, compared to controls. Interestingly however, regression analyses revealed that, among ASD participants, higher social symptom severity was associated with both reduced basic motor mirroring and aberrant socially modulated mirroring (i.e. no enhancement of MNS activity upon direct vs. averted gaze). These findings further challenge the notion that MNS dysfunctions constitute a principal feature of ASD, but that variations in MNS function are related to differential expressions of (social) symptom severity.
... Authors argued that such an increase in motor simulation might be due to a direct impact of OT on the MNS. Another recent study, in which transcranial magnetic stimulation (TMS) of the primary motor cortex was used, supports the presence a direct link between the OT action in the brain and the MNS (Prinsen et al., 2018). Prinsen and colleagues showed that intranasal OT enhances individuals' motor resonance during the observation of hand movements when these are matched with salient social cues, corresponding to the direct gaze of the actor producing the movements. ...
... Future investigation would, therefore, benefit from an increase of the sample size and also from the use of a more powerful within-subject design, in which participants serve as their own control. Finally, as the majority of the behavioral and neurophysiological studies which have investigated the effects of OT so far (De Coster et al., 2014;Levy et al., 2016;Perry et al., 2010;Prinsen et al., 2018) our study targeted a population of young male adults. The rationale for targeting such population was mainly related to the intention of deliberately avoid the inclusion of confounding experimental variables such as age and sex, which may have included more variability in our data and consequently in the interpretation of the results. ...
Intranasal administration of oxytocin (OT) has been found to facilitate prosocial behaviors, emotion recognition and cooperation between individuals. Recent electroencephalography (EEG) investigations have reported enhanced mu rhythm (alpha: 8-13 Hz; beta: 15-25 Hz) desynchronization during the observation of biological motion and stimuli probing social synchrony after the administration of intranasal OT. This hormone may therefore target a network of cortical circuits involved in higher cognitive functions, including the mirror neuron system (MNS). Here, in a double-blind, placebo-controlled, between-subjects exploratory study, we investigated whether intranasal OT modulates the cortical activity from sensorimotor areas during the observation and the execution of social and non-social grasping actions. Participants underwent EEG testing after receiving a single dose (24 IU) of either intranasal OT or placebo. Results revealed an enhancement of alpha - but not beta - desynchronization during observation and execution of social grasps, especially over central and parietal electrodes, in participants who received OT (OT group). No differences between the social and non-social condition were found in the control group (CTRL group). Moreover, we found a significant difference over the cortical central-parietal region between the OT and CTRL group only within the social condition. These results suggest a possible action of intranasal OT on sensorimotor circuits involved in social perception and action understanding, which might contribute to facilitate the prosocial effects typically reported by behavioral studies.
... The association between the participants' self-evaluated level of social anxiety and the magnitude of the zygomatic and orbicular muscle responses was analyzed by correlating the social anxiety scores with the "direct gaze effect" of the EMG responses. A similar approach has been used in other previous studies investigating the association between participant-dependent factors and physiological responses to gaze direction (i.e., Prinsen et al., 2018;Prinsen & Alaerts, 2019). The "direct gaze effect" was quantified by calculating the difference between response magnitudes during the direct and averted gaze conditions (i.e., Δ direct gazeaverted gaze) separately for the model's gaze and participant's own gaze. ...
Eye contact often elicits a smiling response. We investigated whether an individual’s awareness that the recipient perceives their direct gaze during eye contact has an influence on this smiling response. Participants wore glasses with either clear or dark lenses (preventing the other person from seeing their eyes). Measurements of electromyographic activity from the zygomatic and periocular muscle regions showed that the smiling responses were greater to seeing the other’s direct versus averted gaze. The participants’ own gaze direction had also an effect, and this effect was modified by the visibility of their eyes. Zygomatic responses were greater when the participants were aware that their eyes were visible. Thus, awareness of sending a direct gaze to another plays a role in the smiling response. In addition, participants’ self-evaluated level of social anxiety was positively correlated with the magnitude of the zygomatic responses to the other person’s direct versus averted gaze.
... As implied by our EEG results, and in keeping with adult findings, this could involve a self-other matching mechanism. For example, in adults, intranasal OT enhances motor facilitation during manual action observation (Prinsen et al., 2018), and increases both facial and finger movement mimicry (De Coster et al., 2014;Korb et al., 2016). Our study demonstrates similar motor facilitation effects of OT in early infancy. ...
Although positive effects of oxytocin (OT) on social functioning are well-demonstrated, little is known about the mechanisms through which OT may drive early social development, or its therapeutic efficacy in infancy. To address these critical issues, we investigated the effects of exogenous OT on neural (EEG) and behavioral responses during observation of live facial gestures in infant macaques with limited social exposure (i.e. nursery-reared). Three key findings were revealed. First, OT increased alpha suppression over posterior scalp regions during observation of facial gestures but not non-biological movement, suggesting that OT targets self-other matching and attentional cortical networks involved in social perception from very early infancy. Second, OT increased infant production of matching facial gestures and attention towards the most socially-relevant facial stimuli, both behaviors typically silenced by early social deprivation. Third, infants with higher cortisol levels appeared to benefit the most from OT, displaying greater improvements in prosocial behaviors after OT administration. Altogether, these findings suggest that OT promotes prosocial behaviors and associated neural responses likely impacted by early social adversity, and demonstrate the potential of OT administration to ameliorate social difficulties in the context of neurodevelopmental and early-emerging psychiatric disorders, at a developmental stage when brain plasticity is greatest.
... Together, these previous studies and our study add to the growing body of evidence that inter-individual differences in (baseline) person-dependent factors may play a pivotal role in determining IN-OT treatment responses. In the current study, however, attachment style as assessed with the SAAM (State Adult Attachment Measure) was not shown to significantly modulate treatment responses, which is at odds with some prior studies identifying SAAM attachment to be a sensitive modulator of IN-OT treatment responses ( Bernaerts et al., 2017 ;Prinsen et al., 2018 ). For example, significant improvements in self-reports of attachment avoidance (SAAM) and attachment toward peers were shown after a two-week treatment with IN-OT, and these treatment-induced changes were found to be most pronounced for participants with less secure attachments ( Bernaerts et al., 2017 ). ...
The neuropeptide oxytocin (OT) is suggested to exert a pivotal role in a variety of complex human behaviors, including trust, attachment, social perception and fear regulation. Previous studies have demonstrated that intranasal administration of OT reduces subjective and neuroendocrine stress responses and dampens amygdala reactivity. OT has also been proposed to modulate activity of the autonomic nervous system.
Here, a randomized double-blind, placebo-controlled study (with parallel design) was conducted with 56 healthy adult men to investigate whether a single-dose of OT (24 IU) modulates sympathetic autonomic arousal upon live dyadic gaze interactions. To do so, electrodermal recordings of skin conductance were performed during the engagement of eye contact with a live model in a two-person social context.
In accordance to prior research, direct eye gaze elicited a significant enhancement in skin conductance responses, but OT did not specifically enhance or dampen the overall magnitude (amplitude) of the skin conductance response. Administration of OT did facilitate the recovery of skin conductance responses back to baseline (reduced recovery time), indicating a role of OT in restoring homeostatic balance. Notably, the treatment-effect on autonomic recovery was most prominent in participants with low self-reported social responsiveness, indicating that person-dependent factors play an important role in determining OT treatment-responses. Exploratory, it was shown that OT also significantly reduced self-reported feelings of tension and (at trend-level) worrying about how one presents oneself.
Together, these observations add further evidence to a role of OT in modulating activity of the autonomic nervous system, primarily by facilitating a restoration of homeostatic balance after stimulus-induced increases in sympathetically-driven autonomic arousal.
... However, including the present study, not all studies have found increases in visual attention towards the eye region of observed faces after administration of a single dose of intranasal oxytocin. In fact, studies directly testing the effect of oxytocin on different measures of social cognition while taking gaze behavior into account, have countered this notion, showing that oxytocin-related improvements can occur independently of oxytocin effects on eye-gaze patterns (Domes et al., 2010;Lischke et al., 2012;Hubble et al., 2017;Prinsen et al., 2018). ...
The neuropeptide oxytocin is suggested to play a major role in a variety of complex human behaviors, including interpersonal bonding, trust, and attachment. Recent theories have suggested that the role oxytocin plays in these complex social behaviors involves a modulation of motivational tendencies of approach/avoidance-related behaviors. However, to date, direct neurophysiological evidence supporting this notion is limited. In this double-blind, randomized, placebo-controlled study with parallel design, we assessed the effects of administered intranasal oxytocin in 40 adult men on gaze behavior and a neural marker of approach/avoidance motivational tendencies. Specifically, electroencephalography recordings were performed during the engagement of eye contact with a live model in a naturalistic two-person social context and electroencephalographic frontal alpha asymmetry, an established neurophysiological index of motivational tendencies for approach/avoidance-related behaviors, was assessed. Compared to placebo, a single dose of oxytocin (24 international units) was shown to increase relative left-sided frontal asymmetry upon direct eye contact with a live model, which is indicative of an increase in approach-related motivational tendencies towards the presented eye contact stimulus. Notably, the treatment effect was most prominently observed in participants with lower self-reported social motivation (higher Motivation subscale scores on the Social Responsiveness Scale), indicating that participants with lower social motivation benefitted the most from the administered oxytocin. No treatment-specific changes were identified in terms of gaze behavior towards the eye region of the live model. Together, these observations add neurophysiological evidence to the hypothesized role of oxytocin in modulating approach/avoidance related tendencies and suggest that inter-subject variability in person-dependent factors need to be considered in order to evaluate the potential benefit of intranasal oxytocin as a treatment. This notion is of particular relevance to the variety of neuropsychiatric populations such as autism spectrum disorder, social anxiety disorder and depression, for which intranasal oxytocin is increasingly considered a potential treatment.
... However, including the present study, not all studies have found increases in visual attention towards the eye region of observed faces after administration of a single dose of intranasal oxytocin. In fact, studies directly testing the effect of oxytocin on different measures of social cognition while taking gaze behavior into account, have countered this notion, showing that oxytocin-related improvements can occur independently of oxytocin effects on eye-gaze patterns (Domes et al., 2010;Lischke et al., 2012;Hubble et al., 2017;Prinsen et al., 2018). ...
The neuropeptide oxytocin is suggested to exert a pivotal role in a variety of complex human behaviors, including interpersonal bonding, trust, and attachment. Recent theories have suggested that the role oxytocin plays in these complex social behaviors involves a modulation of motivational tendencies of approach/avoidance-related behaviors. However, to date, direct neurophysiological evidence supporting this notion is limited. In this double-blind, randomized, placebo-controlled study with parallel design, we assessed the effects of administered intranasal oxytocin in 40 adult men on gaze behavior and a neural marker of approach/avoidance motivational tendencies. Specifically, electroencephalography recordings were performed during the engagement of eye contact with a live model in a naturalistic two-person social context and electroencephalographic frontal alpha asymmetry, an established neurophysiological index of motivational tendencies for approach/avoidance-related behaviors, was assessed. Compared to placebo, a single dose of oxytocin (24 international units) was shown to increase relative left-sided frontal asymmetry upon direct eye contact with a live model, which is indicative of an increase in approach-related motivational tendencies toward the presented eye contact stimulus. Notably, the treatment effect was most prominently observed in participants with lower self-reported social motivation (higher Motivation subscale scores on the Social Responsiveness Scale), indicating that participants with lower social motivation benefitted the most from the administered oxytocin. No treatment-specific changes were identified in terms of gaze behavior toward the eye region of the live model. Together, these observations add neurophysiological evidence to the hypothesized role of oxytocin in modulating approach/avoidance related tendencies and suggest that inter-individual variance in person-dependent factors need to be considered in order to evaluate the potential benefit of intranasal oxytocin as a treatment. This notion is of particular relevance to the variety of neuropsychiatric populations such as autism spectrum disorder, social anxiety disorder and depression, for which intranasal oxytocin is increasingly considered a potential treatment.
Background:
Current neuroimaging perspectives on a variety of mental disorders emphasize dysfunction of the amygdala. The neuropeptide oxytocin (OXT), a key mediator in the regulation of social cognition and behavior, accumulates in cerebrospinal fluid after intranasal administration in macaques and humans and modulates amygdala reactivity in both species. However, the translation of neuromodulatory OXT effects to novel treatment approaches is hampered by the absence of studies defining the most effective dose and dose-response latency for targeting the amygdala.
Methods:
To address this highly relevant issue, a total of 116 healthy men underwent functional magnetic resonance imaging using a randomized, double-blind, placebo-controlled crossover study design. The experimental rationale was to systematically vary dose-test latencies (15-40, 45-70, and 75-100 minutes) and doses of OXT (12, 24, and 48 international units) in order to identify the most robust effects on amygdala reactivity. During functional magnetic resonance imaging, subjects completed an emotional face recognition task including stimuli with varying intensities ranging from low (highly ambiguous) to high (less ambiguous).
Results:
Our results indicate that the OXT-induced inhibition of amygdala responses to fear was most effective in a time window between 45 and 70 minutes after administration of a dose of 24 international units. Furthermore, the observed effect was most evident in subjects scoring high on measures of autistic-like traits. Behavioral response patterns suggest that OXT specifically reduced an emotional bias in the perception of ambiguous faces.
Conclusions:
These findings provide initial evidence of the most effective dose and dose-test interval for future experimental or therapeutic regimens aimed at targeting amygdala functioning using intranasal OXT administration.
The neuropeptide ‘oxytocin’ (OT) is known to play a pivotal role in a variety of complex social behaviors by promoting a prosocial attitude and interpersonal bonding. One mechanism by which OT is hypothesized to promote prosocial behavior is by enhancing the processing of socially relevant information from the environment. With the present study, we explored to what extent OT can alter the ‘reading’ of emotional body language as presented by impoverished biological motion point light displays (PLDs). To do so, a double-blind between-subjects randomized placebo-controlled trial was conducted, assessing performance on a bodily emotion recognition task in healthy adult males before and after a single-dose of intranasal OT (24 IU). Overall, a single-dose of OT administration had a significant effect of medium size on emotion recognition from body language. OT-induced improvements in emotion recognition were not differentially modulated by the emotional valence of the presented stimuli (positive versus negative) and also, the overall tendency to label an observed emotional state as ‘happy’ (positive) or ‘angry’ (negative) was not modified by the administration of OT. Albeit moderate, the present findings of OT-induced improvements in bodily emotion recognition from whole-body PLD provide further support for a link between OT and the processing of socio-communicative cues originating from the body of others.
The use of intranasal oxytocin (OT) in research has become increasingly important over the past decade. Although researchers have acknowledged a need for further investigation of the physiological effects of intranasal administration, few studies have actually done so. In the present double-blind cross-over study we investigated the longevity of a single 24 IU dose of intranasal OT measured in saliva in 40 healthy adult males. Salivary OT concentrations were significantly higher in the OT condition, compared to placebo. This significant difference lasted until the end of testing, approximately 108 minutes after administration, and peaked at 30 minutes. Results showed significant individual differences in response to intranasal OT administration. To our knowledge this is the largest and first all-male within-subjects design study to demonstrate the impact of intranasal OT on salivary OT concentrations. The results are consistent with previous research in suggesting that salivary OT is a valid matrix for OT measurement. The results also suggest that the post-administration 'wait-time' prior to starting experimental tasks could be reduced to 30 minutes, from the 45 minutes typically used, thereby enabling testing during peak OT concentrations. Further research is needed to ascertain whether OT concentrations after intranasal administration follow similar patterns in females, and different age groups.
Oxytocin promotes prosocial behavior, especially in those individuals who are low in affiliation (e.g., avoidantly attached individuals), but can exacerbate interpersonal insecurities in those preoccupied with closeness (e.g., anxiously attached individuals). One explanation for these opposing observations is that oxytocin induces a communal, other-orientation. Becoming more other oriented should help those people who focus on the self to the exclusion of others, but could be detrimental to those who are other focused but have little sense of an agentic self. Using a within-subjects design, we administered intranasal oxytocin and placebo to 40 males and measured their agency (self-orientation) and communion (other-orientation). Oxytocin produced a slight increase in communion for the average participant; however, as predicted, avoidantly attached individuals were especially likely to perceive themselves as more communal ("kind," "warm," "gentle," etc.) after receiving oxytocin than after receiving the placebo. There was no main effect of oxytocin on agency for the average participant; however, anxiously attached individuals showed a selective decrease in agency ("independent," "self-confident," etc.) following administration of oxytocin. These data help explain the complex social effects of oxytocin.
© The Author(s) 2015.
The neuropeptide oxytocin (OXT) has been revealed as a profound anxiolytic and antistress factor of the brain, besides its many prosocial and reproductive effects. Therefore, there is substantial scientific and medical interest in its potential therapeutic use for the treatment of psychopathologies associated with anxiety, fear, and social dysfunctions, such as generalized anxiety disorder, posttraumatic stress disorder, and social anxiety disorder, as well as autism and schizophrenia, among others. Focusing on preclinical studies, we review the existing evidence for the regulatory capacity of OXT to fine-tune general and social anxiety-related behaviors, as well as cued and social fear conditioning from a translational perspective. The available evidence from animal and human studies substantiates the hypothesis of an imbalance of the endogenous brain OXT system in the etiology of anxiety disorders, particularly those with a social component such as social anxiety disorder. In addition, such an imbalance of the OXT system is also likely to be the consequence of chronic OXT treatment resulting in a dose-dependent reduction in OXT receptor availability and increased anxiety.
Copyright © 2015 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
Autism spectrum conditions (autism) affect ~1% of the population and are characterized by deficits in social communication. Oxytocin has been widely reported to affect social-communicative function and its neural underpinnings. Here we report the first evidence that intranasal oxytocin administration improves a core problem that individuals with autism have in using eye contact appropriately in real-world social settings. A randomized double-blind, placebo-controlled, within-subjects design is used to examine how intranasal administration of 24 IU of oxytocin affects gaze behavior for 32 adult males with autism and 34 controls in a real-time interaction with a researcher. This interactive paradigm bypasses many of the limitations encountered with conventional static or computer-based stimuli. Eye movements are recorded using eye tracking, providing an objective measurement of looking patterns. The measure is shown to be sensitive to the reduced eye contact commonly reported in autism, with the autism group spending less time looking to the eye region of the face than controls. Oxytocin administration selectively enhanced gaze to the eyes in both the autism and control groups (transformed mean eye-fixation difference per second=0.082; 95% CI:0.025–0.14, P=0.006). Within the autism group, oxytocin has the most effect on fixation duration in individuals with impaired levels of eye contact at baseline (Cohen’s d=0.86). These findings demonstrate that the potential benefits of oxytocin in autism extend to a real-time interaction, providing evidence of a therapeutic effect in a key aspect of social communication.
There has been an unprecedented interest in the modulatory effects of intranasal oxytocin on human social cognition and behaviour, however as yet no study has actually demonstrated that this modality of administration increases concentrations of the peptide in the brain as well as blood in humans. Here using combined blood and cerebrospinal fluid (CSF) sampling in subjects receiving either 24 IU of oxytocin (n = 11) or placebo (n = 4) we have shown that oxytocin levels significantly increased in both plasma and CSF. However, whereas oxytocin plasma concentrations peaked at 15 min after intranasal administration and decreased after 75 min, CSF concentrations took up to 75 min to reach a significant level. Moreover, there was no correlation (r = <0.10) between oxytocin plasma and CSF concentrations. Together, these data provide crucial insights into the plasma and CSF kinetics of intranasally administered oxytocin.
The results of two studies are reported. Study I involved the development of the Inventory of Parent and Peer Attachment (IPPA), a self-report instrument for use with adolescents. Subject were 179 college students aged 16-20 years. Item content of the instrument was suggested by attachment theory's formulations concerning the nature of feelings toward attachment figures. In Study II, the convergent validity of the IPPA was examined. Also, a hierarchial regression model was employed to investigate the association between quality of attachment and self-esteem, life-satisfaction, and affective status. Respondents were 86 adolescents from the Study I sample. As hypothesized, perceived quality of both parent and peer attachments was significantly related to psychological well-being. Results of the development of a theoretically focused, exploratory classification scheme indicated that adolescents classified as highly securely attached reported greater satisfaction with themselves, a higher likelihood of seeking social support, and less symptomatic response to stressful life events.
The popularity of oxytocin (OT) has grown exponentially during the past decade, and so has the number of OT trials in healthy and clinical groups. We take stock of the evidence from these studies to explore potentials and limitations of pharmacotherapeutic applications. In healthy participants, intranasally administered OT leads to better emotion recognition and more trust in conspecifics, but the effects appear to be moderated by context (perceived threat of the 'out-group'), personality and childhood experiences. In individuals with untoward childhood experiences, positive behavioral or neurobiological effects seem lowered or absent. In 19 clinical trials, covering autism, social anxiety, postnatal depression, obsessive-compulsive problems, schizophrenia, borderline personality disorder and post-traumatic stress, the effects of OT administration were tested, with doses ranging from 15 IU to more than 7000 IU. The combined effect size was d=0.32 (N=304; 95% confidence interval (CI): 0.18-0.47; P<0.01). However, of all disorders, only studies on autism spectrum disorder showed a significant combined effect size (d=0.57; N=68; 95% CI: 0.15-0.99; P<0.01). We hypothesize that for some of the other disorders, etiological factors rooted in negative childhood experiences may also have a role in the diminished effectiveness of treatment with OT.
As a distinct feature of human social interactions, spontaneous mimicry has been widely investigated in the past decade. Research suggests that mimicry is a subtle and flexible social behavior which plays an important role for communication and affiliation. However, fundamental questions like why and how people mimic still remain unclear. In this paper, we evaluate past theories of why people mimic and the brain systems that implement mimicry in social psychology and cognitive neuroscience. By reviewing recent behavioral and neuroimaging studies on the control of mimicry by social signals, we conclude that the subtlety and sophistication of mimicry in social contexts reflect a social top-down response modulation (STORM) which increases one's social advantage and this mechanism is most likely implemented by medial prefrontal cortex (mPFC). We suggest that this STORM account of mimicry is important for our understanding of social behavior and social cognition, and provides implications for future research in autism.
For over two decades, individual differences in adult attachment style have been conceptualized and measured in terms of anxiety, avoidance, and security. During this time, the prevailing assumption has been that an adult’s attachment style is a relatively stable disposition, rooted in internal working models of self and relationship partners. These models are based on previous experiences in close relationships. Recent research, however, suggests that levels of attachment anxiety, avoidance, and security are also affected by situational factors. To capture temporary fluctuations in the sense of attachment security and insecurity we developed a state adult attachment measure (SAAM). Exploratory and confirmatory factor analyses yielded three reliable subscales measuring state levels of attachment-related anxiety, avoidance, and security. Additional studies demonstrated both convergent and discriminant validity of the new measure, and its sensitivity to a variety of experimental manipulations. Our discussion focuses on potential uses for the SAAM for both researchers and clinicians.
People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms.
Spontaneous mimicry of other people's actions serves an important social function, enhancing affiliation and social interaction. This mimicry can be subtly modulated by different social contexts. We recently found behavioral evidence that direct eye gaze rapidly and specifically enhances mimicry of intransitive hand movements (Wang et al., 2011). Based on past findings linking medial prefrontal cortex (mPFC) to both eye contact and the control of mimicry, we hypothesized that mPFC might be the neural origin of this behavioral effect. The present study aimed to test this hypothesis. During functional magnetic resonance imaging (fMRI) scanning, 20 human participants performed a simple mimicry or no-mimicry task, as previously described (Wang et al., 2011), with direct gaze present on half of the trials. As predicted, fMRI results showed that performing the task activated mirror systems, while direct gaze and inhibition of the natural tendency to mimic both engaged mPFC. Critically, we found an interaction between mimicry and eye contact in mPFC, superior temporal sulcus (STS) and inferior frontal gyrus. We then used dynamic causal modeling to contrast 12 possible models of information processing in this network. Results supported a model in which eye contact controls mimicry by modulating the connection strength from mPFC to STS. This suggests that mPFC is the originator of the gaze-mimicry interaction and that it modulates sensory input to the mirror system. Thus, our results demonstrate how different components of the social brain work together to on-line control mimicry according to the social context.
Building on animal research, the past decade has witnessed a surge of interest in the effects of oxytocin on social cognition and prosocial behavior in humans. This work has generated considerable excitement about identifying the neurochemical underpinnings of sociality in humans, and discovering compounds to treat social functioning deficits. Inspection of the literature, however, reveals that the effects of oxytocin in the social domain are often weak and/or inconsistent. We propose that this literature can be informed by an interactionist approach in which the effects of oxytocin are constrained by features of situations and/or individuals. We show how this approach can improve understanding of extant research, suggest novel mechanisms through which oxytocin might operate, and refine predictions about oxytocin pharmacotherapy.
We investigated the effects of intranasal oxytocin (OXT) on trust and cooperation in borderline personality disorder (BPD), a disorder marked by interpersonal instability and difficulties with cooperation. Although studies in healthy adults show that intranasal OXT increases trust, individuals with BPD may show an altered response to exogenous OXT because the effects of OXT on trust and pro-social behavior may vary depending on the relationship representations and expectations people possess and/or altered OXT system functioning in BPD. BPD and control participants received intranasal OXT and played a social dilemma game with a partner. Results showed that OXT produced divergent effects in BPD participants, decreasing trust and the likelihood of cooperative responses. Additional analyses focusing on individual differences in attachment anxiety and avoidance across BPD and control participants indicate that these divergent effects were driven by the anxiously attached, rejection-sensitive participants. These data suggest that OXT does not uniformly facilitate trust and pro-social behavior in humans; indeed, OXT may impede trust and pro-social behavior depending on chronic interpersonal insecurities, and/or possible neurochemical differences in the OXT system. Although popularly dubbed the 'hormone of love', these data suggest a more circumspect answer to the question of who will benefit from OXT.
One possible reason for the continued neglect of statistical power analysis in research in the behavioral sciences is the inaccessibility of or difficulty with the standard material. A convenient, although not comprehensive, presentation of required sample sizes is provided. Effect-size indexes and conventional values for these are given for operationally defined small, medium, and large effects. The sample sizes necessary for .80 power to detect effects at these levels are tabled for 8 standard statistical tests: (1) the difference between independent means, (2) the significance of a product-moment correlation, (3) the difference between independent rs, (4) the sign test, (5) the difference between independent proportions, (6) chi-square tests for goodness of fit and contingency tables, (7) 1-way analysis of variance (ANOVA), and (8) the significance of a multiple or multiple partial correlation.
When two people meet in a bar, a subtle interplay of social behaviours, including eye contact and unconscious mimicry of actions play an important role in how much the individuals like each other by the end of the evening. However, it is not known how these different social signals interact. Here, we adopt a rapid mimicry paradigm, to test if eye contact can modulate mimicry on a second by second time scale. Our results show that direct eye contact rapidly and specifically enhances mimicry of hand actions. These findings have implications for understanding the role of eye contact as a controlling signal in human non-verbal social behaviour.
Repeated interactions between infant and caregiver result in either secure or insecure relationship attachment patterns, and insecure attachment may affect individual emotion-regulation and health. Given that oxytocin enhances social approach behavior in animals and humans, we hypothesized that oxytocin might also promote the subjective experience of attachment security in humans. Within a 3-week interval, 26 healthy male students classified with an insecure attachment pattern were invited twice to an experimental session. At the beginning of each experiment, a single dose of oxytocin or placebo was administered intranasally, using a double-blind, placebo-controlled within-subject design. In both conditions, subjects completed an attachment task based on the Adult Attachment Projective Picture System (AAP). Thirty-two AAP picture system presentations depicted attachment-related events (e.g. illness, solitude, separation, and loss), and were each accompanied by four prototypical phrases representing one secure and three insecure attachment categories. In the oxytocin condition, a significant proportion of these insecure subjects (N=18; 69%) increased in their rankings of the AAP prototypical "secure attachment" phrases and decreased in overall ranking of the "insecure attachment" phrases. In particular, there was a significant decrease in the number of subjects ranking the pictures with "insecure-preoccupied" phrases from the placebo to the oxytocin condition. We find that a single dose of intranasally administered oxytocin is sufficient to induce a significant increase in the experience of attachment security in insecurely attached adults.
1. We stimulated the motor cortex of normal subjects (transcranial magnetic stimulation) while they 1) observed an experimenter grasping 3D-objects, 2) looked at the same 3D-objects, 3) observed an experimenter tracing geometrical figures in the air with his arm, and 4) detected the dimming of a light. Motor evoked potentials (MEPs) were recorded from hand muscles. 2. We found that MEPs significantly increased during the conditions in which subjects observed movements. The MEP pattern reflected the pattern of muscle activity recorded when the subjects executed the observed actions. 3. We conclude that in humans there is a system matching action observation and execution. This system resembles the one recently described in the monkey.
In this paper, we describe the development of and our preliminary work to empirically validate the Adult Attachment Projective (AAP), a new adult attachment classification system that is based on the analysis of individuals' responses to a set of seven attachment-related drawings. The AAP classification system uses evaluations of three dimensions (Discourse, Content and Defensive Processing) to designate four major adult classification groups: Secure, Dismissing, Preoccupied, and Unresolved. Preliminary validation of the AAP is based on 75 participants drawn from three separate samples. The results indicate strong interjudge reliability and convergent agreement between the AAP and Adult Attachment Interview (AAI) classifications. The AAP, thus, appears to be a promising developmental measure for assessing the representation of attachment in adults. Contributions of the AAP to attachment theory and research are discussed. The similarities and differences between AAP stories and other child and adult representational measures are also discussed.
A category of stimuli of great importance for primates, humans in particular, is that formed by actions done by other individuals. If we want to survive, we must understand the actions of others. Furthermore, without action understanding, social organization is impossible. In the case of humans, there is another faculty that depends on the observation of others' actions: imitation learning. Unlike most species, we are able to learn by imitation, and this faculty is at the basis of human culture. In this review we present data on a neurophysiological mechanism--the mirror-neuron mechanism--that appears to play a fundamental role in both action understanding and imitation. We describe first the functional properties of mirror neurons in monkeys. We review next the characteristics of the mirror-neuron system in humans. We stress, in particular, those properties specific to the human mirror-neuron system that might explain the human capacity to learn by imitation. We conclude by discussing the relationship between the mirror-neuron system and language.
The neuropeptide ‘oxytocin’ (OT) is known to play a pivotal role in a variety of complex social behaviors by promoting a prosocial attitude and interpersonal bonding. Previous studies showed that a single-dose of exogenously administered OT can affect trust and feelings of attachment insecurity. With the present study, we explored the effects of two weeks of daily OT administration on measures of state and trait attachment using a double-blind between-subjects randomized placebo-controlled design. In 40 healthy young adult men state and trait attachment were assessed before and after two weeks of daily intranasal OT (24 IU) or placebo using the State Adult Attachment Scale and the Inventory of Parent and Peer Attachment. Mood, social responsiveness and quality of life were additionally assessed as secondary outcome measures. Reductions in attachment avoidance and increases in reports of attachment toward peers were reported after two weeks of OT treatment. Further, treatment-induced changes were most pronounced for participants with less secure attachment towards their peers. indicating that normal variance at baseline modulated treatment response. OT treatment was additionally associated with changes in mood, indicating decreases in feelings of tension and (tentatively) anger in the OT group, not in the placebo group. Further, at the end of the two-week trial, both treatment groups (OT, placebo) reported to experience an increase in social responsiveness and quality of life, but the effects were only specific to the OT-treatment in terms of reports on ‘social motivation’. In summary, the observed improvements on state and trait dimensions of attachment after a multiple-dose treatment with OT provide further evidence in support of a pivotal role of OT in promoting the experience of attachment.
Attachment bonds are a defining feature of mammals. A conceptual framework on human attachments is presented, integrating insights from animal research with neuroimaging studies. Four mammalian bonds are described, including parent-infant, pair-bonds, peers, and conspecifics, all built upon systems shaped by maternal provisions during sensitive periods, and evolution from rodents to humans is detailed. Bonding is underpinned by crosstalk of oxytocin and dopamine in striatum, combining motivation and vigor with social focus, and their time sensitivity/pulsatility enables reorganization of neural networks. Humans' representation-based attachments are characterized by biobehavioral synchrony and integrate subcortical with cortical networks implicated in reward/motivation, embodied simulation, and mentalization. The neurobiology of love may open perspectives on the 'situated' brain and initiate dialog between science and humanities, arts, and clinical wisdom.
Direct eye contact is a powerful social cue to regulate interpersonal interactions. Previous behavioral studies showed a link between eye contact and motor mimicry, indicating that the automatic mimicry of observed hand movements is significantly enhanced when direct eye contact exists between the observer and the observed model. In the present study, we aim to investigate the neurophysiological basis of the previously reported behavioral enhancements. Here, transcranial magnetic stimulation (TMS) was applied to assess changes in cortico-motor excitability at the level of the primary motor cortex (M1) to explore whether and how the motor system is facilitated from observing others’ hand movements and, in particular, how this process is modulated by eye contact. To do so, motor evoked potentials (MEPs) were collected from two hand muscles while participants received single-pulse TMS and naturally observed video clips of an actor showing hand opening movements or static hands. During the observation, either direct or averted eye gaze was established between the subject and the observed actor. Our findings show a clear effect of eye gaze on observation-induced motor facilitation. This indicates that the mapping or ‘mirroring’ of others' movements is significantly enhanced when movement observation is accompanied by direct eye gaze compared to averted eye gaze. Our results support the notion that eye contact is a powerful social signal with the ability to direct human non-verbal social behavior. Furthermore, our findings are important for understanding the role of the mirror motor system in the mapping of socially relevant actions.
Objectives:
Previous studies have found that oxytocin (OXT) can improve the recognition of emotional facial expressions; it has been proposed that this effect is mediated by an increase in attention to the eye-region of faces. Nevertheless, evidence in support of this claim is inconsistent, and few studies have directly tested the effect of oxytocin on emotion recognition via altered eye-gaze Methods: In a double-blind, within-subjects, randomized control experiment, 40 healthy male participants received 24 IU intranasal OXT and placebo in two identical experimental sessions separated by a 2-week interval. Visual attention to the eye-region was assessed on both occasions while participants completed a static facial emotion recognition task using medium intensity facial expressions.
Results:
Although OXT had no effect on emotion recognition accuracy, recognition performance was improved because face processing was faster across emotions under the influence of OXT. This effect was marginally significant (p<.06). Consistent with a previous study using dynamic stimuli, OXT had no effect on eye-gaze patterns when viewing static emotional faces and this was not related to recognition accuracy or face processing time.
Conclusions:
These findings suggest that OXT-induced enhanced facial emotion recognition is not necessarily mediated by an increase in attention to the eye-region of faces, as previously assumed. We discuss several methodological issues which may explain discrepant findings and suggest the effect of OXT on visual attention may differ depending on task requirements. (JINS, 2016, 22, 1-11).
Eyes have been shown to play a key role during human social interactions. However, to date, no comprehensive cross-discipline model has provided a framework that can account for uniquely human responses to eye cues. In this review, I present a framework that brings together work on the phylogenetic, ontogenetic, and neural bases of perceiving and responding to eyes. Specifically, I argue for a two-process model: a first process that ensures privileged attention to information encoded in the eyes and is important for the detection of other minds and a second process that permits the decoding of information contained in the eyes concerning another person’s emotional and mental states. To some degree, these processes are unique to humans, emerge during different times in infant development, can be mapped onto distinct but interconnected brain regions, and likely serve critical functions in facilitating cooperative interactions in humans. I also present evidence to show that oxytocin is a key modulator of sensitive responding to eye cues. Viewing eyes as windows into other minds can therefore be considered a hallmark feature of human social functioning deeply rooted in our biology.
Popularly hailed as the “love hormone,” oxytocin has emerged as a key variable in the regulation of human social cognition and behavior. In particular, research using intranasal oxytocin to pharmacologically manipulate the availability of oxytocin shows that oxytocin augmentation can promote a wide range of affiliative processes; however, evidence also shows null and even antisocial effects. Rather than random error to be eliminated, such variability may offer clues about the mechanisms by which oxytocin modulates human sociality. Three potential mechanisms—anxiety reduction, social salience, and affiliative motivation—are discussed, along with recent work showing how the affiliative-motivation hypothesis can simultaneously account for oxytocin’s pro- and antisocial effects. Appreciating oxytocin’s nuanced social effects is important for advancing our understanding of the neuroscience and psychology of affiliation.
Oxytocin is a nonapeptide that also serves as a neuromodulator in the human central nervous system. Over the last decade, a sizeable body of literature has examined its effects on social behavior in humans. These studies show that oxytocin modulates various aspects of social behaviors such as empathy, trust, in-group preference, and memory of socially relevant cues. Several theoretical formulations have attempted to explain the effects of oxytocin. The prosocial account argues that oxytocin mainly enhances affiliative prosocial behaviors; the fear/stress theory suggests that oxytocin affects social performance by attenuating stress; and the in-/out-group approach proposes that oxytocin regulates cooperation and conflict among humans in the context of intergroup relations. Nonetheless, accumulating evidence reveals that the effects of oxytocin are dependent on a variety of contextual aspects and the individual's characteristics and can induce antisocial effects including aggression and envy. In an attempt to reconcile these accounts, we suggest a theoretical framework that focuses on the overarching role of oxytocin in regulating the salience of social cues through its interaction with the dopaminergic system. Crucially, the salience effect modulates attention orienting responses to external contextual social cues (e.g., competitive vs. cooperative environment) but is dependent on baseline individual differences such as gender, personality traits, and degree of psychopathology. This view could have important implications for the therapeutic applications of oxytocin in conditions characterized with aberrant social behavior.
Copyright © 2015 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
Recent studies have shown enhanced brain and autonomic responses to seeing a face with a direct gaze. Interestingly, greater responses to eye contact vs. averted gaze have been observed when showing “live” faces as stimuli but not when showing pictures of faces on a computer screen. In this study, we provide unequivocal evidence that the differential responses observed in the “live” condition are dependent on the observer’s mental attributions. Results from two experiments showed that eye contact resulted in greater autonomic and brain responses compared to averted gaze if a participant believed that the stimulus person sitting on the other side of an electronic shutter was able to see him or her through the shutter. Gaze direction had no effects if participants believed that the transparency from their side was blocked. The results suggest that mental attributions exert a powerful modulation on the processing of socially relevant sensory information.
The possibility to improve socio-emotional behaviors in humans by intranasal administration of synthetic oxytocin (OXT) attracts increasing attention, but its uptake into the brain has never been demonstrated so far. Here we used simultaneous microdialysis in both the dorsal hippocampus and amygdala of rats and mice in combination with concomitant blood sampling from the jugular vein to study the dynamics of the neuropeptide in brain extracellular fluid and plasma after its nasal administration. OXT was found to be increased in microdialysates from both the hippocampus and amygdala with peak levels occurring 30-60min after nasal administration. Despite a similar temporal profile of OXT concentrations in plasma, peripheral OXT is unlikely to contribute to dialysate OXT as calculated from in vitro recovery data, indicating a central route of transport. Moreover, intraperitoneal administration of synthetic OXT in identical amounts caused rapid peak levels in brain dialysates and plasma during the first 30min after treatment and a subsequent return toward baseline. While the precise route(s) of central transport remain to be elucidated, our data provide the first evidence that nasally applied OXT indeed reaches behaviorally relevant brain areas, and this uptake is paralleled by changes in plasma OXT.
A series of studies have reported on the salubrious effects of oxytocin nasal spray on social cognition and behavior in humans, across physiology (e.g., eye gaze, heart rate variability), social cognition (e.g., attention, memory, and appraisal), and behavior (e.g., trust, generosity). Findings suggest the potential of oxytocin nasal spray as a treatment for various psychopathologies, including autism and schizophrenia. There are, however, increasing reports of variability of response to oxytocin nasal spray between experiments and individuals. In this review, we provide a summary of factors that influence transmucosal nasal drug delivery, deposition, and their impact on bioavailability. These include variations in anatomy and resultant airflow dynamic, vascularisation, status of blood vessels, mode of spray application, gallenic formulation (including presence of uptake enhancers, control release formulation), and amount and method of administration. These key variables are generally poorly described and controlled in scientific reports, in spite of their potential to alter the course of treatment outcome studies. Based on this review, it should be of no surprise that differences emerge across individuals and experiments when nasal drug delivery methods are employed. We present recommendations for researchers to use when developing and administering the spray, and guidelines for reporting on peptide nasal spray studies in humans. We hope that these recommendations assist in establishing a scientific standard that can improve the rigor and subsequent reliability of reported effects of oxytocin nasal spray in humans.
Discusses a shortened version of the Dutch translation of the POMS, based on the results of a previous empirical study. Item and factor analyses of the results were used to produce the shortened version. The test scores correlated to sex differences but not to age differences. The available data are insufficient to validate the test, but they do not contradict the test's validity and thus justify further investigation. (English abstract) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
The neuropeptide oxytocin has become a subject of great interest in studies investigating human social cognition. Single intranasal administration of the hormone has been reported to have positive behavioral effects, such as increasing trust or facilitating social approach, 45-80min after administration. However, little is still known about the long-term pharmacokinetics of oxytocin nasal spray application in humans. This study addressed the question how long oxytocin plasma levels remain elevated following nasal spray administration. Another goal was to examine the influence of oxytocin administration on endogenous steroid hormones since such alterations might modulate social behavior via an indirect way. Eight healthy Caucasian men were challenged with a single intranasal application of 26 international units of oxytocin. Changes in oxytocin blood plasma levels, as well as steroid hormone levels of progesterone, testosterone and estradiol were assessed at 5 consecutive time points over a period of 3.5h (-5, +30, +90, +150, +210min relative to oxytocin administration). Results gave evidence for a substantial rise of oxytocin plasma levels 30min after intranasal administration, observed in 7 of 8 participants. Group mean oxytocin plasma level was found to have returned to baseline already 90min post administration, though in some individuals the plasma levels was still elevated relative to sampling at post 150min. Steroid hormone analyses yielded a slight augmentation of endogenous testosterone levels 210min after oxytocin administration. Our data confirms previous findings that oxytocin administered as a nasal spray enters the blood circulation, elevating oxytocin plasma levels for a limited time. Our findings suggest that this time window differs between individuals, but that, for the used dose, it does not extend beyond 150min post administration. The data further provides preliminary evidence that intranasal oxytocin has an enhancing effect on testosterone in healthy men.
The past eight years of research has demonstrated that oxytocin nasal spray has a significant impact on human social cognition. The aim of this review is to provide critical comment on the literature using an information-processing framework. We provide a summary of fundamental assumptions of information-processing models and highlight an impressive range of consistent findings that demonstrate the impact of oxytocin nasal spray on social information processing. These findings include that oxytocin nasal spray improves the early conceptual detection of affect from social cues and improves the accurate appraisal of affect from social cues at elaborate and strategic levels of processing. There is some evidence that these effects may be particularly powerful for positive social cues. This review comments on inconsistent results that have been reported. We argue that such inconsistencies can, in part, be explained by variability across experiments in the degree to which potential extraneous confounds have been controlled, the different methods upon which studies assessed cognition, and the extent to which the focus of investigation has been on group-based outcomes. Finally, we argue that sound cognitive experimental methods can provide powerful tools to identify markers of response to oxytocin nasal spray that can be integrated into more complex circuitry models. The identification of robust markers has particular value in predicting behavioral and therapeutic response to intervention. This should now be a major focus for future research. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.
Among its many roles in body and brain, oxytocin influences social behavior. Understanding the precise nature of this influence is crucial, both within the broader theoretical context of neurobiology, social neuroscience and brain evolution, but also within a clinical context of disorders such as anxiety, schizophrenia, and autism. Research exploring oxytocin's role in human social behavior is difficult owing to its release in both body and brain and its interactive effects with other hormones and neuromodulators. Additional difficulties are due to the intricacies of the blood-brain barrier and oxytocin's instability, which creates measurement issues. Questions concerning how to interpret behavioral results of human experiments manipulating oxytocin are thus made all the more pressing. The current paper discusses several such questions. We highlight unresolved fundamental issues about what exactly happens when oxytocin is administered intranasally, whether such oxytocin does in fact reach appropriate receptors in brain, and whether central or peripheral influences account for the observed behavioral effects. We also highlight the deeper conceptual issue of whether the human data should be narrowly interpreted as implicating a specific role for oxytocin in complex social cognition, such a generosity, trust, or mentalizing, or more broadly interpreted as implicating a lower-level general effect on general states and dispositions, such as anxiety and social motivation. Using several influential studies, we show how seemingly specific, higher-level social-cognitive effects can emerge via a process by which oxytocin's broad influence is channeled into a specific social behavior in a context of an appropriate social and research setting. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.
Humans regulate intergroup conflict through parochial altruism; they self-sacrifice to contribute to in-group welfare and
to aggress against competing out-groups. Parochial altruism has distinct survival functions, and the brain may have evolved
to sustain and promote in-group cohesion and effectiveness and to ward off threatening out-groups. Here, we have linked oxytocin,
a neuropeptide produced in the hypothalamus, to the regulation of intergroup conflict. In three experiments using double-blind
placebo-controlled designs, male participants self-administered oxytocin or placebo and made decisions with financial consequences
to themselves, their in-group, and a competing out-group. Results showed that oxytocin drives a “tend and defend” response
in that it promoted in-group trust and cooperation, and defensive, but not offensive, aggression toward competing out-groups.
Oxytocin (OT) plays a determining role in social and pair bonding in many vertebrates and increasing evidence suggests it is a social hormone also in humans. Indeed, intranasal administration of OT modulates several social cognitive processes in humans. Electrophysiological studies in humans associated the suppression of EEG in the mu/alpha and beta bands with perception of biological motion and social stimuli. It has been suggested that mu and beta suppression over sensory-motor regions reflects a resonance system in the human brain analogous to mirror neurons in the monkey. We therefore hypothesized that OT, a social hormone, would enhance this suppression, hence, for the first time, link the action of this neuropeptide with a human correlate of mirror neuron activity. Twenty-four students were administered 24 IU of OT or placebo intranasally in a robust, double-blind within-subject design. 45 min later participants were shown a point-light display of continuous biological motion of a human figure's walk. In the 8-10 Hz (low alpha/mu band) and in the 15-25 Hz beta band, a significant main effect of treatment showed that suppression was significantly enhanced in the OT versus the placebo conditions and that this suppression was widespread across the scalp. These results are a first step linking OT to the modulation of EEG rhythms in humans, suggesting that OT may have a role in allocating cortical resources to social tasks partly mediated by mirror neuron activity.
Evidence suggests that intranasally administered oxytocin modulates several social cognitive and emotional processes in humans. In this study, we investigated the effect of oxytocin on the perception of biological motion (a walking character) and nonbiological motion (a rotating shape). The participants were 20 healthy volunteers who observed moving dots embedded among a cloud of noise (mask) dots. Sensitivity (d
’) for motion detection was determined after the administration of oxytocin and placebo. The results showed that oxytocin (relative to placebo) administration increased sensitivity to biological motion but not to nonbiological motion. These results suggest that oxytocin specifically modulates the perception of socially relevant stimuli.
The neuropeptide oxytocin (OXT) has previously been found to reduce amygdala reactivity to social and emotional stimuli in healthy men. The present study aimed to investigate the effect of intranasally administered OXT on brain activity in response to social emotional stimuli of varying valence in women. In a functional magnetic-resonance imaging study, sixteen women were presented with fearful, angry, happy and neutral facial expressions after a single dose of 24IU OXT or a placebo administration in a within-subject design. Group analysis revealed that the blood-oxygen-level-dependent (BOLD) signal was enhanced in the left amygdala, the fusiform gyrus and the superior temporal gyrus in response to fearful faces and in the inferior frontal gyrus in response to angry and happy faces following OXT treatment. This effect was independent of fixation pattern to specific sections of the facial stimuli as revealed by eye tracking and independent of basal plasma levels of OXT, estradiol, and progesterone. The results are at odds with the previously reported effects found in men. Future studies should include both sexes to determine a possible sexual dimorphism in the neural effects of OXT, considering gonadal steroids and OXT receptor affinity.
The 'eye contact effect' is the phenomenon that perceived eye contact with another human face modulates certain aspects of the concurrent and/or immediately following cognitive processing. In addition, functional imaging studies in adults have revealed that eye contact can modulate activity in structures in the social brain network, and developmental studies show evidence for preferential orienting towards, and processing of, faces with direct gaze from early in life. We review different theories of the eye contact effect and advance a 'fast-track modulator' model. Specifically, we hypothesize that perceived eye contact is initially detected by a subcortical route, which then modulates the activation of the social brain as it processes the accompanying detailed sensory information.
Experiments in monkeys have shown that coding the goal of the motor acts is a fundamental property of the cortical motor system. In area F5, goal-coding motor neurons are also activated by observing motor acts done by others (the 'classical' mirror mechanism); in area F2 and area F1, some motor neurons are activated by the mere observation of goal-directed movements of a cursor displayed on a computer screen (a 'mirror-like' mechanism). Experiments in humans and monkeys have shown that the mirror mechanism enables the observer to understand the intention behind an observed motor act, in addition to the goal of it. Growing evidence shows that a deficit in the mirror mechanism underlies some aspects of autism.
Autistic disorder (AD) is a disabling oligogenic condition characterized by severe social impairment. Subthreshold autistic social impairments are known to aggregate in the family members of autistic probands; therefore, we conducted this study to examine the intergenerational transmission of such traits in the general population.
The Social Responsiveness Scale (SRS), a quantitative measure of autistic traits, was completed on 285 pairs of twins (by maternal report) and on their parents (by spouse report).
Correlation for social impairment or competence between parents and their children and between spouses was on the order of .4. In families in which both parents scored in the upper quartile for social impairment on the SRS, mean SRS score of offspring was significantly elevated (effect size 1.5). Estimated assortative mating explained approximately 30% of the variation in parent SRS scores.
Children from families in which both parents manifest subthreshold autistic traits exhibit a substantial shift in the distribution of their scores for impairment in reciprocal social behavior, toward the pathological end. As has been previously demonstrated in children, heritable subthreshold autistic impairments are measurable in adults and appear continuously distributed in the general population.
Neuroscience research during the past ten years has fundamentally changed the traditional view of the motor system. In monkeys, the finding that premotor neurons also discharge during visual stimulation (visuomotor neurons) raises new hypotheses about the putative role played by motor representations in perceptual functions. Among visuomotor neurons, mirror neurons might be involved in understanding the actions of others and might, therefore, be crucial in interindividual communication. Functional brain imaging studies enabled us to localize the human mirror system, but the demonstration that the motor cortex dynamically replicates the observed actions, as if they were executed by the observer, can only be given by fast and focal measurements of cortical activity. Transcranial magnetic stimulation enables us to instantaneously estimate corticospinal excitability, and has been used to study the human mirror system at work during the perception of actions performed by other individuals. In the past ten years several TMS experiments have been performed investigating the involvement of motor system during others' action observation. Results suggest that when we observe another individual acting we strongly 'resonate' with his or her action. In other words, our motor system simulates underthreshold the observed action in a strictly congruent fashion. The involved muscles are the same as those used in the observed action and their activation is temporally strictly coupled with the dynamics of the observed action.