Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys
Open accessAbstract
Gaze following is a basic building block of social behavior that has been observed in multiple species, including primates. The absence of gaze following is associated with abnormal development of social cognition, such as in autism spectrum disorders (ASD). Some social deficits in ASD, including the failure to look at eyes and the inability to recognize facial expressions, are ameliorated by intranasal administration of oxytocin (IN-OT). Here we tested the hypothesis that IN-OT might enhance social processes that require active engagement with a social partner, such as gaze following. Alternatively, IN-OT may only enhance the perceptual salience of the eyes, and may not modify behavioral responses to social signals. To test this hypothesis, we presented four monkeys with videos of conspecifics displaying natural behaviors. Each video was viewed multiple times before and after the monkeys received intranasally either 50 IU of OT or saline. We found that despite a gradual decrease in attention to the repeated viewing of the same videos (habituation), IN-OT consistently increased the frequency of gaze following saccades. Further analysis confirmed that these behaviors did not occur randomly, but rather predictably in response to the same segments of the videos. These findings suggest that in response to more naturalistic social stimuli IN-OT enhances the propensity to interact with a social partner rather than merely elevating the perceptual salience of the eyes. In light of these findings, gaze following may serve as a metric for pro-social effects of oxytocin that target social action more than social perception.
AI snapshot
Written from the paper’s full text.
TL;DR
Intranasal oxytocin (IN-OT) increased gaze-following saccades in adult male rhesus monkeys viewing videos of natural conspecific social behavior, even though it did not increase time spent looking at the eyes during videos. The authors argue this supports an effect of oxytocin on active social engagement rather than merely on perceptual salience of the eyes.
Key findings
- Gaze following was rare but reliable: 465 gaze-following saccades occurred across 3924 video presentations, or 11.85% of presentations (min = 3.94%, max = 20.67%), and they clustered on the same video segments within and across viewers (permutation tests, both p < 0.001).
- IN-OT increased gaze-following frequency compared with saline: significant treatment effect, F(1,1) = 25.0, p < 0.001, ηp2 = 0.44, d = 1.77; saline produced a significant decrease interpreted as habituation, F(1,1) = 65.92, p < 0.001.
- OT also increased overall time viewing the videos, F(1,1) = 15.41, p < 0.001, but gaze following did not correlate with viewing time before treatment, post-saline, or post-OT (Spearman R = 0.204, 0.038, 0.037; all p > 0.05).
- OT increased time spent viewing eyes in static images, F(1,1) = 5.39, p < 0.05, ηp2 = 0.01, but not in videos, F(1,1) = 0.05, p > 0.05; OT had no effect on saccade peak velocities, F(1,1) = 3.15, p > 0.05.
Methods
- Four adult male rhesus macaques completed 10 sessions each: 5 with 50 IU nebulized oxytocin and 5 with saline, with treatment administered after the first 3 blocks of videos.
- Each session used 12 unique 10-s videos of unfamiliar conspecifics displaying threatening, neutral, or appeasing behaviors; videos were viewed 7 times in blocks, with eye position recorded at 240 Hz.
- Gaze-following saccades were scored manually under blind conditions using established criteria; analyses used two-way ANOVA with treatment and monkey factors, plus permutation tests for co-occurrence and treatment differences.
Limitations
- The paper states the primary limitation is the small number of subjects (N = 4), though each monkey viewed 840 videos; static images were shown only to 2 of 4 monkeys, and only male monkeys were used, so results may not extend to females.
- The paper also states that no control videos without social content were presented, so it cannot distinguish whether OT enhances attention to all videos or only social videos; peripheral effects of OT and possible vasopressin-1A receptor binding could not be ruled out.
- Evident from the text: the small sample limits generalizability, and the static-image eye-looking result is described as an additional control rather than the main result.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
0 of 31 cited sources checked · 0 supported · 0 flagged
- Findingcitation
Gaze following saccades occurred relatively infrequently, in response to 11.85% (min = 3.94%, max = 20.67%) of video presentations.
“Replicating previous reports, gaze following saccades occurred relatively infrequently, in response to 11.85% (min = 3.94%, max = 20.67%) of video presentations (Mosher et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
- Findingown data
There was no significant interaction between monkey and treatment on gaze following frequency (F(1,3) = 0.98, p = 0.41).
“No main effect of monkey (F(1,3) = 0.96, p = 0.42) and no significant interaction between monkey and treatment (F(1,3) = 0.98, p = 0.41) was observed.”
Quote in the paperNot a substantial claim - Findingown data
Inhalation of a nebulized solution of 50 IU OT increased the frequency of gaze following saccades compared to saline inhalation (F(1,1) = 25.0, p < 0.001, ηp2 = 0.44, d = 1.77).
“Confirming our hypothesis, inhalation of a nebulized solution of 50 UI OT increased the frequency of gaze following saccades (significant effect of treatment, F(1,1) = 25.0, p < 0.001, ηp2 = 0.44, d = 1.77) compared to saline inhalation.”
Quote in the paperSubstantial claim - Findingown data
Gaze following saccades were significantly more likely to occur in response to the same segment of the videos for repeated viewings by the same viewer (p < 0.001).
“We found that gaze following saccades were significantly more likely to occur in response to the same segment of the videos whether we considered repeated viewings by the same viewer (Permutation test, two-tailed, p < 0.001), or gaze follows from multiple viewers (Permutation test, two-tailed, p < 0.001).”
Quote in the paperSubstantial claim - Findingown data
There was no main effect of monkey on gaze following frequency (F(1,3) = 0.96, p = 0.42).
“No main effect of monkey (F(1,3) = 0.96, p = 0.42) and no significant interaction between monkey and treatment (F(1,3) = 0.98, p = 0.41) was observed.”
Quote in the paperNot a substantial claim
- Findingown data
Gaze following saccades were significantly more likely to occur in response to the same segment of the videos for multiple viewers (p < 0.001).
“We found that gaze following saccades were significantly more likely to occur in response to the same segment of the videos whether we considered repeated viewings by the same viewer (Permutation test, two-tailed, p < 0.001), or gaze follows from multiple viewers (Permutation test, two-tailed, p < 0.001).”
Quote in the paperSubstantial claim - Findingown data
For gaze following to occur, it was necessary for the head and eyes of the stimulus monkey to be turned from frontal view to semi-profile or full profile.
“For gaze following to occur it was necessary for the head and eyes of the stimulus monkey to be turned from frontal view to semi-profile or full profile.”
Quote in the paperNot a substantial claim - Findingown data
The observed difference between OT and saline treatments in gaze following frequency was significantly higher than chance (Permutation test, two-tailed, p < 0.001).
“We found that the observed difference between the two treatments was significantly higher than chance (Permutation test, two-tailed, p < 0.001).”
Quote in the paperSubstantial claim - Findingown data
Head rotations of this type were not sufficient to elicit gaze following.
“This was not sufficient, however, because head rotations of this type were abundant in the videos”
Quote in the paperSubstantial claim - Findingown data
The observed changes in viewing time after treatment were significantly different from randomly shuffled post-treatment/pre-treatment sessions (Permutation test, two-tailed, p < 0.001).
“To confirm this result was not due to the different videos seen under each treatment we performed a second statistical test which compared the observed changes in viewing after treatment to those randomly shuffled post-treatment pre-treatment session (Permutation test, two-tailed, p < 0.001).”
Quote in the paperSubstantial claim - Findingreasoning
Videos depicting neutral expressions triggered more gaze following saccades after IN-OT treatment than videos with appeasing or aggressive behaviors.
“Videos depicting neutral expressions triggered more gaze following saccades after IN-OT treatment than videos with appeasing or aggressive behaviors.”
Quote in the paperNot a substantial claim - Findingown data
The effect size for gaze following in this study was d = 1.6.
“the effect size for gaze following in our study is quite large (d = 1.6)”
Quote in the paperNot a substantial claim - Findingown data
The facial expression of the stimulus monkeys was not predictive of the number of gaze following saccades before IN-OT.
“Although the facial expression of the stimulus monkeys was not predictive of the number of gaze following saccades before IN-OT, we found that the increase in gaze following saccades after IN-OT was driven primarily by videos with neutral content (Supplemental Fig. S1).”
Quote in the paperNot a substantial claim - Findingown data
Of the 244 videos, only 27 elicited gaze following saccades in at least one of the 4 viewers.
“yet of the 244 videos only 27 elicited gaze following saccades in at least one of the 4 viewers.”
Quote in the paperNot a substantial claim - Findingown data
There was no correlation between the number of gaze following saccades and the time spent viewing the movie before treatment (Spearman rank correlation, R = 0.204, p > 0.05).
“This lack of correlation was true for videos shown before the treatment (Spearman rank correlation, R = 0.204, p > 0.05), post-saline inhalation (Spearman rank correlation, R = 0.038, p > 0.05) and post-oxytocin inhalation (Spearman rank correlation, R = 0.037, p > 0.05).”
Quote in the paperSubstantial claim - Findingown data
When viewing the videos, the time spent looking at the eyes was not significantly increased by OT (F(1,1) = 0.05, p > 0.05).
“Surprisingly, when viewing the videos the time spent looking at the eyes was not significantly increased (Fig. 3C, F(1,1) = 0.05, p > 0.05).”
Quote in the paperSubstantial claim - Findingown data
The effect size for the increase of global attention was rather small.
“In contrast, the effect size for the increase of global attention was rather small”
Quote in the paperSubstantial claim - Findingown data
After IN-OT, monkeys tended to respond with gaze-following saccades to segments of the video that did not elicit gaze following saccades prior to IN-OT.
“Interestingly, after IN-OT the monkeys tended to respond with gaze-following saccades to segments of the video that did not elicit gaze following saccades prior to IN-OT.”
Quote in the paperSubstantial claim - Findingown data
IN-OT produced an increase in gaze following frequency compared to the pre-treatment baseline (F(1,1) = 7.56, p < 0.05).
“IN-OT produced an increase in gaze following frequency compared to the pre-treatment baseline (F(1,1) = 7.56, p < 0.05), in contrast to saline inhalation, which produced a significant decrease in the frequency of gaze following saccades ANOVA, (F(1,1) = 65.92, p < 0.001), which we interpret to be due to habituation.”
Quote in the paperSubstantial claim - Findingown data
OT inhalation increased the time spent viewing the eyes in static images (F(1, 1) = 5.39, p < 0.05, ηp2 = 0.01).
“We found that OT inhalation increased the time spent viewing the eyes in static images (Fig. 3D, significant main effect of treatment F(1, 1) = 5.39, p < 0.05, ηp2 = 0.01) as reported by previous studies.”
Quote in the paperSubstantial claim - Findingown data
OT did not change the dynamics of gaze following saccades.
“The observation that OT did not change the dynamics of these saccades (despite the presence of OT receptors in the superior colliculus (Freeman et al., 2014))”
Quote in the paperSubstantial claim - Findingown data
There was no significant interaction between monkey and treatment on overall attention to videos (F(1,3) = 1.79, p = 0.15, ηp2 = 0.01).
“OT inhalation also increased the viewer’s overall attention to the videos as measured by the total time the monkeys spent viewing the videos (Fig. 3A/B) significant effect of treatment (F(1,1) = 15.41, p < 0.001) and no significant interaction between monkey and treatment (F(1,3) = 1.79, p = 0.15, with an effect size of ηp2 = 0.01).”
Quote in the paperNot a substantial claim - Findingown data
There was no correlation between the number of gaze following saccades and the time spent viewing the movie post-saline inhalation (Spearman rank correlation, R = 0.038, p > 0.05).
“This lack of correlation was true for videos shown before the treatment (Spearman rank correlation, R = 0.204, p > 0.05), post-saline inhalation (Spearman rank correlation, R = 0.038, p > 0.05) and post-oxytocin inhalation (Spearman rank correlation, R = 0.037, p > 0.05).”
Quote in the paperSubstantial claim - Findingown data
Only 17 of these 27 videos elicited gaze following in more than 1 viewer monkey.
“Only 17 videos of these 27 elicited gaze following in more than 1 viewer monkey.”
Quote in the paperNot a substantial claim - Findingown data
The increase in gaze following saccades after IN-OT was driven primarily by videos with neutral content.
“Although the facial expression of the stimulus monkeys was not predictive of the number of gaze following saccades before IN-OT, we found that the increase in gaze following saccades after IN-OT was driven primarily by videos with neutral content (Supplemental Fig. S1).”
Quote in the paperNot a substantial claim - Findingown data
OT did not significantly affect the duration of mutual gaze compared to saline inhalation (F(1,1) = 1.8, p > 0.05).
“Thus we determined whether OT affected the duration of mutual gaze (Supplemental Fig. S2A) and found no significant difference compared to saline inhalation (no significant main effect of treatment F(1,1) = 1.8, p > 0.05).”
Quote in the paperSubstantial claim - Findingown data
There was no difference between treatments for viewing the mouth (F(1,1) = 0.68, p > 0.05).
“Furthermore, no difference between treatments was found for viewing the mouth (Supplemental Fig. 3B, no significant main effect of treatment F(1,1) = 0.68, p > 0.05).”
Quote in the paperNot a substantial claim - Findingown data
OT inhalation increased the viewer's overall attention to the videos as measured by the total time the monkeys spent viewing the videos (F(1,1) = 15.41, p < 0.001).
“OT inhalation also increased the viewer’s overall attention to the videos as measured by the total time the monkeys spent viewing the videos (Fig. 3A/B) significant effect of treatment (F(1,1) = 15.41, p < 0.001) and no significant interaction between monkey and treatment (F(1,3) = 1.79, p = 0.15, with an effect size of ηp2 = 0.01).”
Quote in the paperNot a substantial claim - Findingown data
Gaze following saccades had a higher peak velocity (369.33 dva/s ± 19.96) than distance-matched saccades (304.16 dva/s ± 2.75) originating at the eye region and terminating elsewhere (main effect of saccade type F(1, 1) = 19.56, p < 0.001).
“Interestingly, gaze following saccades, also had a higher peak velocity (369.33 dva/s ± 19.96) than distance-matched saccades (304.16 dva/s ± 2.75) originating at the eye region and terminating elsewhere (ANOVA with factors saccade type and continuous factor of saccade distance, main effect of saccade type F(1, 1) = 19.56, p < 0.001).”
Quote in the paperNot a substantial claim - Findingcitation
Gaze following can be reliably elicited by naturalistic, dynamic social stimuli.
“The results presented here confirm our previous findings that gaze following can be reliably elicited by naturalistic, dynamic social stimuli (Mosher et al., 2011)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
- Findingown data
Saline inhalation produced a significant decrease in the frequency of gaze following saccades compared to pre-treatment baseline (F(1,1) = 65.92, p < 0.001).
“IN-OT produced an increase in gaze following frequency compared to the pre-treatment baseline (F(1,1) = 7.56, p < 0.05), in contrast to saline inhalation, which produced a significant decrease in the frequency of gaze following saccades ANOVA, (F(1,1) = 65.92, p < 0.001), which we interpret to be due to habituation.”
Quote in the paperSubstantial claim - Findingown data
There was no correlation between the number of gaze following saccades and the time spent viewing the movie post-oxytocin inhalation (Spearman rank correlation, R = 0.037, p > 0.05).
“This lack of correlation was true for videos shown before the treatment (Spearman rank correlation, R = 0.204, p > 0.05), post-saline inhalation (Spearman rank correlation, R = 0.038, p > 0.05) and post-oxytocin inhalation (Spearman rank correlation, R = 0.037, p > 0.05).”
Quote in the paperSubstantial claim - Findingreasoning
OT increased the frequency of gaze following saccades independent of its effect on increasing global attention to the videos.
“Importantly, and regardless of the trigger, OT increased the frequency of gaze following saccades and this was independent of its effect on increasing global attention to the videos.”
Quote in the paperSubstantial claim - Premisecitation
The expected period of rise in OT levels is 20-45 min.
“This way the expected period of rise in OT levels (20–45 min) coincided with the post-treatment viewing period (Chang et al., 2012; Dal Monte et al., 2014b).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Chang et al., 2012 source
Not checked in the free run.
- cites Dal Monte et al., 2014b
Not checked in the free run.
- Premisecitation
Videos which depict the natural behaviors of monkeys reliably elicit gaze following from viewer monkeys.
“We have previously shown that videos which depict the natural behaviors of monkeys reliably elicit gaze following from viewer monkeys (Mosher et al., 2011).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
- Interpretationown data
While relatively rare, gaze following saccades occurred reliably in response to a specific stimulus, i.e., the behavior of the stimulus monkey.
“Thus, while relatively rare, gaze following saccades occurred reliably in response to a specific stimulus, i.e., the behavior of the stimulus monkey.”
Quote in the paperSubstantial claim - Interpretationown data
In response to more naturalistic social stimuli, IN-OT enhances the propensity to interact with a social partner rather than merely elevating the perceptual salience of the eyes.
“These findings suggest that in response to more naturalistic social stimuli IN-OT enhances the propensity to interact with a social partner rather than merely elevating the perceptual salience of the eyes.”
Quote in the paperSubstantial claim- Rests on an assumption: Gaze following saccades are a manifestation of active social engagement/propensity to interact with a social partner, rather than merely a perceptual response.
- Rests on an assumption: The gaze-following behavior of rhesus monkeys is a valid model for human social engagement and for pro-social effects of oxytocin.
- Interpretationreasoning
Gaze following may serve as a metric for pro-social effects of oxytocin that target social action more than social perception.
“In light of these findings, gaze following may serve as a metric for pro-social effects of oxytocin that target social action more than social perception.”
Quote in the paperSubstantial claim- Rests on an assumption: Gaze following saccades are a manifestation of active social engagement/propensity to interact with a social partner, rather than merely a perceptual response.
- Rests on an assumption: The gaze-following behavior of rhesus monkeys is a valid model for human social engagement and for pro-social effects of oxytocin.
- Interpretationcitation
The eyes represent an object of high interest or intrinsic value.
“The higher peak velocity of gaze following saccades and/or saccades targeting the eyes demonstrate that the eyes represent an object of high interest or intrinsic value (Xu-Wilson et al., 2009).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Xu-Wilson et al., 2009 source
Not checked in the free run.
- Interpretationown data
Inhaled OT does not appear to modify the mechanisms by which the eyes as a fixation target or as the origin of gaze following saccades may modify saccade velocities.
“The mechanism(s) by which the eyes as a fixation target or as the origin of gaze following saccades may modify saccade velocities are unknown; whatever these mechanism may be, inhaled OT does not appear to modify these mechanisms.”
Quote in the paperNot a substantial claim - Premisecitation
Typical IN-OT studies in humans examining effects on behavior have an effect size of d = 0.3.
“compared to the effect sizes of typical IN-OT studies in human examining effects on behavior (d = 0.3) (Walum et al., 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Walum et al., 2015
Not checked in the free run.
- Interpretationcitation
The decrease in gaze following frequency post-saline inhalation is likely due to habituation to the 7 successive presentations of the video sets.
“The reduction in gaze following frequency post-saline inhalation is likely due to habituation to the 7 successive presentations of the video sets. Indeed repeated presentation of the same videos in the current and in previous studies led to a gradual reduction in attention to the videos (Mosher et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
- Interpretationreasoning
The intrinsic value or saliency of eyes as a target of attention remained unchanged by OT inhalation.
“suggests that the intrinsic value or saliency of eyes as a target of attention remained unchanged by OT inhalation.”
Quote in the paperSubstantial claim - Study design and conductnone given
The primary limitation of this study is the small number of subjects (N = 4).
“The primary limitation of this study is the small number of subjects (N = 4).”
Quote in the paperSubstantial claim - Interpretationown data
The increase in the number of gaze following saccades did not result from a global enhancement of attention to the videos.
“Thus, the increase in the number of gaze following saccades did not result from a global enhancement of attention to the videos.”
Quote in the paperSubstantial claim - Premisecitation
In response to videos, viewers switch from simply staring at the most salient feature (the eyes) to attempting to engage the stimulus monkey in social interactions.
“Indeed, in response to videos, viewers switch from simply staring at the most salient feature (the eyes) to attempting to engage the stimulus monkey in social interactions.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
- Study design and conductnone given
No control videos without social content were presented to the animals during the experiment.
“No control videos without social content were presented to the animals during the experiment”
Quote in the paperSubstantial claim - Interpretationown data
These results support the hypothesis that saccade parameters might be related to the salience or value of fixation targets.
“These results support the hypothesis put forth by Xu-Wilson et al. (2009) that saccade parameters might be related to the salience or value of fixation targets.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Xu-Wilson et al. (2009) source
Not checked in the free run.
- Premisecitation
With repeated presentation of the same videos, the viewer's responses diminish as they learn that their social behaviors have no effect on the perceived social partner.
“With repeated presentation of the same videos the viewer’s responses diminish as they learn that their social behaviors have no effect on the perceived social partner.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
- Interpretationreasoning
This prevents us from distinguishing between the role of OT in enhancing attention to all videos or only to videos with social content.
“which prevent us from distinguishing between the role of OT in enhancing attention to all videos or only to videos with social content.”
Quote in the paperSubstantial claim - Interpretationown data
These videos most likely contain a more potent triggering signal for gaze following.
“These videos most likely contain a more potent triggering signal for gaze following.”
Quote in the paperNot a substantial claim - Interpretationown data
The effect of OT on looking at the eyes depends on the static or dynamic nature of the social stimuli.
“We conclude, therefore, that the effect of OT on looking at the eyes depends on the static or dynamic nature of the social stimuli.”
Quote in the paperSubstantial claim - Interpretationown data
The increase in overall attention to videos was less prominent than the increase in the number of gaze following saccades.
“As the small effect sizes indicate, this outcome, albeit statistically significant, was less prominent than the large increase in the number of the gaze following saccades.”
Quote in the paperSubstantial claim - Interpretationown data
The stimulus monkeys emitted a, yet insufficiently characterized, signal that compelled the viewers to follow their gaze.
“The observation that gaze following saccades occurred reliably in response to the same video segments suggests that the stimulus monkeys emitted a, yet insufficiently characterized, signal that compelled the viewers to follow their gaze (Fig. 1).”
Quote in the paperNot a substantial claim
- May combine two claims. 10
- Classified as probably not a substantial claim. 29
May combine two claims.
Findingown dataGaze following saccades tended to occur in response to the same segment of a video during successive presentations to a given viewer monkey, and also across different viewers.
“Gaze following saccades tended to occur in response to the same segment of a video during successive presentations of the video to a given viewer monkey, and also across different viewers (Fig. 1).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown data465 gaze following saccades were extracted from scanpaths made during the viewing of 3924 videos.
“We extracted 465 gaze following saccades from scanpaths made during the viewing of 3924 videos.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe perception of these signals is subject to individual differences, as rarely a video segment elicited gaze following reliably in all four subjects.
“the perception of these signals is subject to individual differences as we rarely identified a video segment that elicited reliably gaze following in all four subjects.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingnone givenThe results are consistent across subjects.
“While it is encouraging that the results are consistent across subjects”
Quote in the paperNot a substantial claimMay combine two claims.
FindingreasoningIN-OT enhances the frequency of gaze following saccades without increasing looking time at the eyes.
“and report the effect of IN-OT in enhancing the frequency of gaze following saccades without increasing looking time at the eyes.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S4 (based).
Findingnone givenThe parameters of eye movements in monkeys (including saccade velocity) and humans are highly similar.
“As we have shown here the parameters of eye movements in monkeys (including saccade velocity) and humans are highly similar.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe dose of 50 IU oxytocin has been used previously for rhesus monkeys.
“This dose has been used previously used for rhesus monkeys (Dal Monte et al., 2014b; Parr et al., 2013).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Dal Monte et al., 2014b
Not checked in the free run.
- cites Parr et al., 2013 source
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductnone givenSets of 12 videos were randomly allocated to OT and saline sessions.
“Sets of 12 videos were randomly allocated to OT and saline sessions.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationOT increases reward allocation to a partner monkey.
“OT also enhances socially reinforced learning (Parr, 2014), and increases reward allocation to a partner monkey (Chang et al., 2012).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Chang et al., 2012 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe neuromodulator oxytocin (OT) improves social deficits in ASD and other disorders accompanied by social deficits.
“The neuromodulator oxytocin (OT) has been shown to improve social deficits in both ASD and other disorders accompanied by social deficits (Guastella et al., 2010, 2010; Hollander et al., 2002, 2007; Yatawara et al., 2015; Young and Barrett, 2015).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationGaze following is not unique to humans; it has been described in multiple social species, ranging from birds to humans.
“Gaze following is not unique to humans; it has been described in multiple social species, ranging from birds to humans as reviewed by Shepherd (2010).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Shepherd (2010)
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductnone givenAll experimenters were blind to the treatment.
“All experimenters were blind to the treatment.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationOT enhances socially reinforced learning.
“OT also enhances socially reinforced learning (Parr, 2014), and increases reward allocation to a partner monkey (Chang et al., 2012).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Parr, 2014 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationWhen administered intranasally, OT increases the time that rhesus monkeys spend viewing the eyes of conspecifics in static images.
“When administered intranasally, OT increases the time that rhesus monkeys spend viewing the eyes of conspecifics in static images (Dal Monte et al., 2014a; Ebitz et al., 2013) and communicative gesturing in rhesus infants (Simpson et al., 2014).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Dal Monte et al., 2014a
Not checked in the free run.
- cites Ebitz et al., 2013 source
Not checked in the free run.
Classified as probably not a substantial claim.
PremisecitationDeficits of gaze following are among the symptoms of autism spectrum disorders (ASD).
“Deficits of gaze following are among the symptoms of autism spectrum disorders (ASD) (Dawson et al., 1998).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Dawson et al., 1998 source
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductcitationGaze follows were scored manually using previously established criteria.
“Gaze follows were scored manually using previously established criteria (Mosher et al., 2011).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductnone givenManual scoring of gaze following saccades was done blindly, with the scorer unaware of treatment, session, or order of video viewing.
“Manual scoring of gaze following saccades was done blindly, where the scorer was unaware of the treatment, session, or the order in which the videos were viewed in a session.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationWhen administered intranasally, OT increases communicative gesturing in rhesus infants.
“When administered intranasally, OT increases the time that rhesus monkeys spend viewing the eyes of conspecifics in static images (Dal Monte et al., 2014a; Ebitz et al., 2013) and communicative gesturing in rhesus infants (Simpson et al., 2014).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Simpson et al., 2014 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenGaze following saccade velocities were calculated for a subset (n = 202) of randomly selected gaze following saccades, which were manually verified.
“Gaze following saccade velocities were calculated individually for a subset (n = 202) of randomly selected of gaze following saccades, which were manually verified.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataThe OT-induced increase in gaze following cannot be explained by an increased attention to the eyes because OT did not increase eye looking in response to the videos.
“Finally, the OT-induced increase in gaze following cannot be explained by an increased attention to the eyes because OT did not increase eye looking in response to the videos.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationreasoningNeutral faces with averted gaze, possibly being more ambiguous, prompt both greater arousal and more frequent gaze following saccades due to the viewer's interest in where another monkey is looking.
“it appears that neutral faces with averted gaze, possibly being more ambiguous, prompt both greater arousal and more frequent gaze following saccades due to the viewer’s interest in the where another monkey is looking.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenOnly male monkeys were used.
“Finally, only male monkeys were used”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationIncreased engagement of the viewer is manifested in the production and reciprocation of facial expressions and, more rarely, in the production of social calls (coos).
“This increased engagement of the viewer is manifested in the production and reciprocation of facial expressions and, more rarely, in the production of social calls (coos) (Mosher et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mosher et al., 2011 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenStatic images were shown only to two of the four monkeys.
“Static images were shown only to two of the four monkeys.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe effect size can be improved by high number of trials for each subject even if the number of subjects is low.
“As suggested by Walum et al. (2015), the effect size can be improved by high number of trials for each subject even if the number of subjects is low.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Walum et al., 2015
Not checked in the free run.
May combine two claims.
Interpretationown dataOur results appear to lend support to the idea that OT increases social motivation and/or decreases social inhibition.
“our results appear to lend support to the idea that OT increases social motivation and/or decreases social inhibition.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationIn our paradigm, IN-OT also increases viewing the eyes of conspecifics.
“a previously published finding that in our paradigm IN-OT also increases viewing the eyes of conspecifics (Dal Monte et al., 2014a).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Dal Monte et al., 2014a
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductreasoningWe compensated for the small cohort of subjects by recording large numbers of observations from each subject.
“We compensated for the small cohort of subjects by recording large numbers of observations from each subject.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Study design and conductreasoningThe small sample size is justified by the difficulties to carry out these studies in large cohorts of non-human primates.
“This sample size does not compare favorably to well-powered human studies, but is justified by the difficulties to carry out these studies in large cohorts of non-human primates.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataOT influences the interactive aspect of social behavior rather than modifying some aspect of social perception.
“further substantiating the claim that OT influences the interactive aspect of social behavior rather than modify some aspect of social perception.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
PremisecitationThe effects of IN-OT are oftentimes subtle and many studies reporting behavioral effects of IN-OT are indeed underpowered.
“The effects of IN-OT are oftentimes subtle and many studies reporting behavioral effects of IN-OT are indeed underpowered (Walum et al., 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Walum et al., 2015
Not checked in the free run.
May combine two claims.
InterpretationcitationThese results may not extend to female monkeys, as there may be a sex-dependent expression of OXTR in the brain.
“thus these results may not extend to female monkeys, as there may be a sex-dependent expression of OXTR in the brain (Insel et al., 1993).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Insel et al., 1993 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationNeutral images with averted gaze induce more reliably skin conductance responses than appeasing or aggressive facial expressions.
“an earlier finding indicating that neutral images with averted gaze induce more reliably skin conductance responses than appeasing or aggressive facial expressions (Hollander et al., 2007).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hollander et al., 2007 source
Not checked in the free run.
Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).
InterpretationreasoningA larger sample size would clearly lead to stronger conclusions.
“a larger sample size would clearly lead to stronger conclusions.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
PremisecitationPrevious reports indicate changes in saccade parameters induced by social stimuli.
“This analysis was justified by previous reports on changes in saccade parameters induced by social stimuli (Xu-Wilson et al., 2009).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Xu-Wilson et al., 2009 source
Not checked in the free run.
Probably not a substantial claim: may not pass S2 (checkable).
Interpretationnone givenThe use of videos as social stimuli added to the growing evidence that natural stimuli, albeit more difficult to control, elicit natural behaviors that are quantifiable and robust.
“the use of videos as social stimuli added to the growing evidence that natural stimuli, albeit more difficult to control, elicit natural behaviors that are quantifiable and robust.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).
InterpretationreasoningGaze following is one step closer to spontaneous, natural social behavior than looking at the eyes.
“Gaze following is a basic form of social interaction and a fundamental building block of theory of mind, and as such is one step closer to spontaneous, natural social behavior than looking at the eyes.”
Quote in the paperNot a substantial claim- Rests on an assumption: Gaze following is a basic form of social interaction and a fundamental building block of theory of mind.
Classified as probably not a substantial claim.
InterpretationreasoningThis behavior can be readily elicited and studied in the laboratory because eye movements are relatively easy to record and quantify.
“This behavior can be readily elicited and studied in the laboratory because eye movements are relatively easy to record and quantify.”
Quote in the paperSubstantial claim
The paper relies on this without support.
Gaze following saccades are a manifestation of active social engagement/propensity to interact with a social partner, rather than merely a perceptual response.
“Gaze following is an expression of social engagement, a behavior that indicates an explicit interest in where others are looking.”
The paper relies on this without support.
The four adult male rhesus monkeys studied are representative of adult male rhesus monkeys generally.
“Behavioral data was collected from four adult male rhesus macaques (Macaca mulatta): G, Z, U, and R.”
The paper relies on this without support.
The gaze-following behavior of rhesus monkeys is a valid model for human social engagement and for pro-social effects of oxytocin.
“The absence of gaze following is associated with abnormal development of social cognition, such as in autism spectrum disorders (ASD).”
The paper relies on this without support.
Gaze following is a basic form of social interaction and a fundamental building block of theory of mind.
“Gaze following is a basic form of social interaction and a fundamental building block of theory of mind”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
IN-OXT treatment increases gaze following, increases socially oriented gaze, and alters social attention in a wide variety of contexts in macaques.
“This work provides anatomical support for other findings in macaques, which indicate that IN-OXT treatment increases gaze following67, increases socially oriented gaze68, and alters social attention in a wide variety of contexts69–74.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [67]
Statistics that don’t add up
Each reported p-value recomputed from its test statistic and degrees of freedom.
Inconsistent p-value across alpha = .05: F(1,1) = 7.56, p < .05
MajorThe paper reports p < .05 here; recomputing from the test statistic and its degrees of freedom gives p = .222. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p < .05 · recomputed p = .222
“F(1,1) = 7.56, p < 0.05”
Inconsistent p-value across alpha = .05: F(1, 1) = 5.39, p < .05
MajorThe paper reports p < .05 here; recomputing from the test statistic and its degrees of freedom gives p = .259. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p < .05 · recomputed p = .259
“F(1, 1) = 5.39, p < 0.05”
Inconsistent p-value across alpha = .05: F(1, 1) = 19.56, p < .001
MajorThe paper reports p < .001 here; recomputing from the test statistic and its degrees of freedom gives p = .142. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p < .001 · recomputed p = .142
“F(1, 1) = 19.56, p < 0.001”
Inconsistent p-value across alpha = .05: F(1,1) = 65.92, p < .001
MajorThe paper reports p < .001 here; recomputing from the test statistic and its degrees of freedom gives p = .078. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p < .001 · recomputed p = .078
“F(1,1) = 65.92, p < 0.001”
Inconsistent p-value across alpha = .05: F(1,1) = 15.41, p < .001
MajorThe paper reports p < .001 here; recomputing from the test statistic and its degrees of freedom gives p = .159. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p < .001 · recomputed p = .159
“F(1,1) = 15.41, p < 0.001”
Inconsistent p-value: F(1,3) = 1.79, p = .15
MinorThe paper reports p = .15 here; recomputing from the test statistic and its degrees of freedom gives p = .273. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p = .15 · recomputed p = .273
“F(1,3) = 1.79, p = 0.15”
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Doesn’t add upF(1, 1) = 7.56reported p < .05 · recomputed p = .222The two fall on opposite sides of .05
“F(1,1) = 7.56, p < .05”
- Doesn’t add upF(1, 1) = 65.92reported p < .001 · recomputed p = .078The two fall on opposite sides of .05
“F(1,1) = 65.92, p < .001”
- Doesn’t add upF(1, 1) = 15.41reported p < .001 · recomputed p = .159The two fall on opposite sides of .05
“F(1,1) = 15.41, p < .001”
- Doesn’t add upF(1, 1) = 5.39reported p < .05 · recomputed p = .259The two fall on opposite sides of .05
“F(1, 1) = 5.39, p < .05”
- Doesn’t add upF(1, 1) = 19.56reported p < .001 · recomputed p = .142The two fall on opposite sides of .05
“F(1, 1) = 19.56, p < .001”
- Doesn’t add upF(1, 3) = 1.79reported p = .15 · recomputed p = .273
“F(1,3) = 1.79, p = .15”
- ConsistentF(1, 1) = 25reported p < .001 · recomputed p = .126
“F(1,1) = 25.0, p < .001”
The paper states an exact test
- ConsistentF(1, 3) = 0.96reported p = .42 · recomputed p = .399
“F(1,3) = 0.96, p = .42”
The paper states an exact test
- ConsistentF(1, 3) = 0.98reported p = .41 · recomputed p = .395
“F(1,3) = 0.98, p = .41”
The paper states an exact test
- ConsistentF(1, 1) = 0.05reported p > .05 · recomputed p = .860
“F(1,1) = 0.05, p > .05”
- ConsistentF(1, 1) = 1.8reported p > .05 · recomputed p = .408
“F(1,1) = 1.8, p > .05”
- ConsistentF(1, 1) = 0.68reported p > .05 · recomputed p = .561
“F(1,1) = 0.68, p > .05”
- ConsistentF(1, 3) = 173.5reported p < .001 · recomputed p < .001
“F(1, 3) = 173.5, p < .001”
- ConsistentF(1, 1) = 3.15reported p > .05 · recomputed p = .327
“F(1, 1) = 3.15, p > .05”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Two different effect sizes are reported for gaze following
MinorThe results report d = 1.77 for the treatment effect, while the discussion describes the study's gaze-following effect size as d = 1.6. Rounding 1.77 to one decimal place would give 1.8, not 1.6.
“significant effect of treatment, F(1,1) = 25.0, p < 0.001, ηp2 = 0.44, d = 1.77”
“the effect size for gaze following in our study is quite large (d = 1.6)”
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Oxytocin, vasopressin, and the neurogenetics of sociality
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“Deficits of gaze following are among the symptoms of autism spectrum disorders (ASD) (Dawson et al., 1998).”
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
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Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders.
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“A large portion of the human studies focused on the effect of OT on allocating attention to salient social stimuli, such as the eyes (Andari et al., 2010; Auyeung et al., 2015; Guastella et al., 2008), but these studies address only one component of social interactions, that of social perception.”
The Social Salience Hypothesis of Oxytocin
Shamay-Tsoory, S. G., & Abu-Akel, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.020 · Cited by 904 · cited 1× · see citing works
“This hormone might (1) increase the saliency of social cues (Shamay-Tsoory and Abu-Akel, 2016; Young, 2015), (2) reduce vigilance to facilitate social interactions (Ebitz et al.”
What does the amygdala contribute to social cognition
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“, 1987), a structure heavily implicated in social cognition (Adolphs, 2010).”
Oxytocin increases gaze to the eye region of human faces
Guastella, A. J., Mitchell, P. B., & Dadds, M. R. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.06.026 · Cited by 798 · see citing works
Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans
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“These results in non-human primates replicate similar findings in humans (Guastella et al., 2008; Hurlemann et al., 2010).”
Oxytocin-gaze positive loop and the coevolution of human-dog bonds
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Oxytocin Increases Retention of Social Cognition in Autism
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Oxytocin-dependent consolation behavior in rodents
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Oxytocin Infusion Reduces Repetitive Behaviors in Adults with Autistic and Asperger's Disorders
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Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain
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“The NBM also provides cholinergic innervation to many cortical regions of the social brain, including the superior temporal sulcus (STS) (Selden et al., 1998), a region involved in face processing, the detection of gaze direction, and gaze following.”
Faces and objects in macaque cerebral cortex
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“It is likely, therefore, that gaze following behaviors rely on neural connections between face- and gaze-selective regions in the STS and the amygdala (Iidaka et al., 2012; Kliemann et al., 2012; Tsao et al., 2003) which might be modulated by OT through the NBM.”
Intranasal Oxytocin: Myths and Delusions
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“, 2014) we also cannot rule out the possibility that the observed results are due, at least in part, to the peripheral effects of OT (Leng and Ludwig, 2015).”
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Following gaze: gaze-following behavior as a window into social cognition
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Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies
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“The neuromodulator oxytocin (OT) has been shown to improve social deficits in both ASD and other disorders accompanied by social deficits (Guastella et al., 2010, 2010; Hollander et al., 2002, 2007; Yatawara et al., 2015; Young and Barrett, 2015).”
Gaze following and joint attention in rhesus monkeys (Macaca mulatta).
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“One individual might direct the attention of a social partner to that object (pointing with the eyes), but ultimately it is the object that captures the gaze of both partners (Emery et al., 1997).”
Chang, S. W. C., Barter, J. W., Ebitz, R. B., Watson, K. K., & Platt, M. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114621109 · Cited by 252 · cited 2× · see citing works
“OT also enhances socially reinforced learning (Parr, 2014), and increases reward allocation to a partner monkey (Chang et al., 2012).”
Auyeung, B., Lombardo, M. V., Heinrichs, M., Chakrabarti, B., Sule, A., Deakin, J. B., Bethlehem, R. A. I., Dickens, L., Mooney, N., Sipple, J. A. N., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2014.146 · Cited by 234 · cited 1× · see citing works
“A large portion of the human studies focused on the effect of OT on allocating attention to salient social stimuli, such as the eyes (Andari et al., 2010; Auyeung et al., 2015; Guastella et al., 2008), but these studies address only one component of social interactions, that of social perception.”
Skuse, D. H., Lori, A., Cubells, J. F., Lee, I., Conneely, K. N., Puura, K., Lehtimäki, T., Binder, E. B., & Young, L. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302985111 · Cited by 207 · see citing works
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Oxytocin-Induced Analgesia and Scratching Are Mediated by the Vasopressin-1A Receptor in the Mouse
Schorscher-Petcu, A., Sotocinal, S., Ciura, S., Dupre, A., Ritchie, J., Sorge, R. E., Crawley, J. N., Hu, S.-B., Nishimori, K., Young, L. J., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1594-10.2010 · Cited by 189 · cited 1× · see citing works
“, 1999), implying that the behavioral effects seen in this study might be explained independently of OXTR activation (Schorscher-Petcu et al., 2010).”
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“including the nucleus basalis of Meynert (NBM) (Freeman et al., 2014).”
The 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 · cited 1× · see citing works
“It is likely, therefore, that gaze following behaviors rely on neural connections between face- and gaze-selective regions in the STS and the amygdala (Iidaka et al., 2012; Kliemann et al., 2012; Tsao et al., 2003) which might be modulated by OT through the NBM.”
CSF and blood oxytocin concentration changes following intranasal delivery in macaque
Dal Monte, O., Noble, P. L., Turchi, J., Cummins, A., & Averbeck, B. B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103677 · Cited by 177 · see citing works
Mirroring of attention by neurons in macaque parietal cortex
Shepherd, S. V., Klein, J. T., Deaner, R. O., & Platt, M. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900419106 · Cited by 172 · cited 1× · see citing works
“Finally, neurons in the lateral intraparietal area track the gaze directions of both viewer and stimulus monkeys, which likely contributes to gaze following behaviors (Shepherd et al., 2009).”
Neurobiological mechanisms of social attachment and pair bonding
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The intrinsic value of visual information affects saccade velocities
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“This analysis was justified by previous reports on changes in saccade parameters induced by social stimuli (Xu-Wilson et al., 2009).”
Localization of Vasopressin (V<sub>1a</sub>) Receptor Binding and mRNA in the Rhesus Monkey Brain
Young, Toloczko, & Insel (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00332.x · Cited by 139 · cited 1× · see citing works
“OT is known to also bind to vasopressin-1A receptors (AVPR1A), which are amply expressed in the amygdala and the cortex (Young et al., 1999), implying that the behavioral effects seen in this study might be explained independently of OXTR activation (Schorscher-Petcu et al.”
Oxytocin blunts social vigilance in the rhesus macaque
Ebitz, R. B., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305230110 · Cited by 132 · see citing works
Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques
Modi, M. E., Connor-Stroud, F., Landgraf, R., Young, L. J., & Parr, L. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.02.011 · Cited by 129 · cited 1× · see citing works
“Although IN-OT does increase the CSF levels of OT (Dal Monte et al., 2014b; Modi et al., 2014) we also cannot rule out the possibility that the observed results are due, at least in part, to the peripheral effects of OT (Leng and Ludwig, 2015).”
Impact of Basal Forebrain Cholinergic Inputs on Basolateral Amygdala Neurons
Ünal, Ç. T., Paré, D., & Záborszky, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2706-14.2015 · Cited by 124 · cited 1× · see citing works
“In the amygdala, neural responses to incoming signals are strongly enhanced by cholinergic inputs (Unal et al., 2015).”
Intranasal 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 · cited 2× · see citing works
“This dose has been used previously used for rhesus monkeys (Dal Monte et al., 2014b; Parr et al., 2013).”
Materna, S., Dicke, P. W., & Thier, P. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2008.20.1.108 · Cited by 121 · see citing works
Gonadal steroids have paradoxical effects on brain oxytocin receptors
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Fiber pathways of basal forebrain cholinergic neurons in monkeys
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Inhaled oxytocin increases positive social behaviors in newborn macaques
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Oxytocin enhances attention to the eye region in rhesus monkeys
Dal Monte, O., Noble, P. L., Costa, V. D., & Averbeck, B. B. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00041 · Cited by 80 · see citing works
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Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys
Mosher, C. P., Zimmerman, P. E., & Gothard, K. M. (2011) · Behavioral Neuroscience · doi:10.1037/a0024264 · Cited by 67 · see citing works
Self-citationOxytocin, social cognition and psychiatry
Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.186 · Cited by 64 · see citing works
Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta)
Roy, A., Shepherd, S. V., & Platt, M. L. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss123 · Cited by 42 · see citing works
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Neuronal substrates of gaze following in monkeys
Kamphuis, S., Dicke, P. W., & Thier, P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06730.x · Cited by 30 · cited 1× · see citing works
“The STS shows increased BOLD signals during gaze following in both monkeys (Kamphuis et al., 2009) and humans (Materna et al.”
Intranasal oxytocin enhances socially-reinforced learning in rhesus monkeys
Parr, L. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00278 · Cited by 23 · see citing works
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4 of the 57 references couldn’t be matched to a known paper.
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Loth, E., Charman, T., Mason, L., Tillmann, J., Jones, E. J. H., Wooldridge, C., Ahmad, J., Auyeung, B., Brogna, C., Ambrosino, S., et al. (2017) · Molecular Autism · doi:10.1186/s13229-017-0146-8 · Cited by 299 · see citing works
“This behavioural marker of social impairment has been linked to either reduced social reward sensitivity or increased (social) anxiety, which may in turn be mediated by the neuropeptides oxytocin [62] and vasopressin [63], or serotonin [64].”
Prefrontal–amygdala circuits in social decision-making
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BackgroundOxytocin regulates reunion affiliation with a pairmate following social separation in marmosets
Cavanaugh, J., Mustoe, A. C., & French, J. A. (2018) · American Journal of Primatology · doi:10.1002/ajp.22750 · Cited by 41 · see citing works
An integrated framework for the role of oxytocin in multistage social decision‐making
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“There is accumulated research on the role of IN-OT in promoting social exploration, enhancing social motivation and attenuating social vigilance in nonhuman primate models (Chang et al. 2012; Chang and Platt 2014; Ebitz and Platt 2013; Parr et al. 2013; Putnam et al. 2016).”
BackgroundIntranasal oxytocin modulates neural functional connectivity during human social interaction
Rilling, J. K., Chen, X., Chen, X., & Haroon, E. (2018) · American Journal of Primatology · doi:10.1002/ajp.22740 · Cited by 40 · see citing works
Gothard, K. M., Mosher, C. P., Zimmerman, P. E., Putnam, P. T., Morrow, J. K., & Fuglevand, A. J. (2017) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1449 · Cited by 36 · see citing works
“45,46 Static images rarely induce such spontaneous and interactive behaviors.”
BackgroundSelf-citationSimpson, E. A., Paukner, A., Sclafani, V., Kaburu, S., Suomi, S. J., & Ferrari, P. F. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4480-x · Cited by 36 · see citing works
“For example, a recent study in male rhesus macaque adults reported that OT improved gaze-following responses to video stimuli (Putnam et al. 2016).”
BackgroundGaze following: A socio-cognitive skill rooted in deep time
Zeiträg, C., Jensen, T. R., & Osvath, M. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.950935 · Cited by 34 · see citing works
From Oxytocin to Compassion: The Saliency of Distress
Kucerova, B., Levit‐Binnun, N., Gordon, I., & Golland, Y. (2023) · Biology · doi:10.3390/biology12020183 · Cited by 35 · see citing works
Non-invasive Eye Tracking Methods for New World and Old World Monkeys
Ryan, A. M., Freeman, S. M., Murai, T., Lau, A. R., Palumbo, M., Hogrefe, C. E., Bales, K. L., & Bauman, M. D. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00039 · Cited by 32 · see citing works
Le, J., Kou, J., Zhao, W., Fu, M., Zhang, Y., Becker, B., & Kendrick, K. M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0830-x · Cited by 28 · see citing works
Interplay between the oxytocin and opioid systems in regulating social behaviour
Putnam, P. T., & Chang, S. W. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0050 · Cited by 33 · see citing works
“In non-human primates, oxytocin increases time spent looking at faces [35,36], improves socially reinforced learning [37], increases the frequency of gaze following behaviours [38] and promotes the donation of rewards to social partners [39,40].”
BackgroundSelf-citationDivergent effects of oxytocin on eye contact in bonobos and chimpanzees
Brooks, J., Kano, F., Sato, Y., Yeow, H., Morimura, N., Nagasawa, M., Kikusui, T., & Yamamoto, S. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.105119 · Cited by 27 · see citing works
Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research
Putnam, P. T., Young, L. J., & Gothard, K. M. (2018) · American Journal of Primatology · doi:10.1002/ajp.22756 · Cited by 28 · see citing works
“Rhesus monkeys that received AE OT before they freely viewed videos of conspecifics, showed a robust increase in the frequency of gaze following saccades, abehaviorthatindicatesanexplicitinterestinwhereothersarelooking (Putnam, Roman, Zimmerman, & Gothard, 2016) (Figure 4).”
BackgroundSelf-citationOpportunities and challenges for intranasal oxytocin treatment studies in nonhuman primates
Bauman, M. D., Murai, T., Hogrefe, C. E., & Platt, M. L. (2018) · American Journal of Primatology · doi:10.1002/ajp.22913 · Cited by 25 · see citing works
Social determinants of eyeblinks in adult male macaques
Ballesta, S., Mosher, C. P., Szep, J., Fischl, K. D., & Gothard, K. M. (2016) · Scientific Reports · doi:10.1038/srep38686 · Cited by 24 · see citing works
Self-citationBridging the species gap in translational research for neurodevelopmental disorders
Ryan, A. M., Berman, R. F., & Bauman, M. D. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.10.006 · Cited by 24 · see citing works
Effects of chronic oxytocin on attention to dynamic facial expressions in infant macaques
Parr, L. A., Brooks, J. M., Jonesteller, T., Moss, S., Jordano, J. O., & Heitz, T. R. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.08.028 · Cited by 23 · see citing works
“Numerous studies have utilized these videos in other experiments (Gothard et al., 2007; Mosher et al., 2011; Putnam et al., 2016).”
MethodOxytocin increases eye gaze in schizophrenia
Bradley, E. R., Seitz, A., Niles, A. N., Rankin, K. P., Mathalon, D. H., O'Donovan, A., & Woolley, J. D. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.07.039 · Cited by 22 · see citing works
“Administration of oxytocin enhances eye gaze in non-human primates (Kotani et al., 2017; Putnam et al., 2016), neurotypical humans (Domes et al.”
BackgroundClinical potential of oxytocin in autism spectrum disorder: current issues and future perspectives
Benner, S., & Yamasue, H. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000341 · Cited by 19 · see citing works
“Increased attention to faces and gaze following oxytocin administration has also been observed in non-human primates (Ebitz et al., 2013; Putnam et al., 2016) and dogs (Kovacs et al., 2016).”
InfluentialDevelopment of social systems neuroscience using macaques
Isoda, M., Noritake, A., & Ninomiya, T. (2018) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.94.020 · Cited by 19 · see citing works
Testing the effect of oxytocin on social grooming in bonobos
Brooks, J., Kano, F., Yeow, H., Morimura, N., & Yamamoto, S. (2022) · American Journal of Primatology · doi:10.1002/ajp.23444 · Cited by 19 · see citing works
“negative and fearful facial expressions [10] as well as social threats [11], and more gaze following 56 [12].”
BackgroundDifferences in how macaques monitor others: Does serotonin play a central role?
Weinberg‐Wolf, H., & Chang, S. W. C. (2019) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1494 · Cited by 14 · see citing works
“, 2017), and to also increase gaze following (Putnam et al., 2016; Tollenaar, Chatzimanoli, van der Wee, & Putman, 2013).”
Oxytocin facilitates socially directed attention
Le, J., Zhao, W., Kou, J., Fu, M., Zhang, Y., Becker, B., & Kendrick, K. M. (2021) · Psychophysiology · doi:10.1111/psyp.13852 · Cited by 13 · see citing works
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Oxytocin modulates mate-guarding behavior in marmoset monkeys
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Territorial blueprint in the hippocampal system
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Behavioral screening tools for identifying autism in macaques: existing and promising tests
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Social engagement revealed by gaze following in third-party observers of simulated social conflict
Champ, T. M., Lee, S., Martin, A. B., Bolles, C. M., Kim, S. W., & Gothard, K. M. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.952390 · Cited by 8 · see citing works
“Similar studies in macaques have shown that the scanpaths elicited by videos with ethologically valid social content contain information about social knowledge of the viewers (Mosher et al., 2011; Putnam et al., 2016).”
ResultSelf-citationIntranasal oxytocin enhances the perception of ambiguous averted gaze in women but not in men
Zheng, Y., Shi, Y., Jia, H., Gao, S., & Hu, Z. (2021) · Psychopharmacology · doi:10.1007/s00213-021-05828-5 · Cited by 8 · see citing works
Oxytocin and cardiometabolic interoception: Knowing oneself affects ingestive and social behaviors
Smith, J. A., Eikenberry, S. A., Scott, K. A., Baumer-Harrison, C., de Lartigue, G., de Kloet, A. D., & Krause, E. G. (2022) · Appetite · doi:10.1016/j.appet.2022.106054 · Cited by 8 · see citing works
Mulholland, M. M., Webb, S. J. N., Mareno, M. C., Schweller, K., Schapiro, S. J., & Hopkins, W. D. (2021) · PLoS ONE · doi:10.1371/journal.pone.0259941 · Cited by 6 · see citing works
“On the other hand, Putnam, Roman, Zimmerman, and Gothard [13] showed that male rhesus monkeys attempt to interact with conspecifics in videos by gaze following, and that intranasal oxytocin increases this behavior.”
BackgroundDensten, I. L. (2020) · Emerald Group Publishing Limited eBooks · doi:10.1108/s1535-120320200000013002 · Cited by 3 · see citing works
Multi-dimensional social relationships shape social attention in monkeysPreprint
Liu, S., Huang, J., Chen, S., Platt, M. L., & Yang, Y. T. (2025) · eLife · doi:10.7554/elife.104460 · Cited by 3 · see citing works
“This peptide hormone also plays a crucial role in shaping social development and promoting prosocial behavior ( Bauman et al., 2018 ; Putnam et al., 2016 ).”
Oxytocin and opioid antagonists: A dual approach to improving social behavior
Monte, O. D., Gangopadhyay, P., Putnam, P. T., & Chang, S. W. C. (2025) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15376 · Cited by 3 · see citing works
“91 In macaques, OT enhances social attention by increasing the time spent looking at conspecifics’ eyes, 92,93 promoting gaze-following behaviors, 94 and reducing attention to negative facial expressions 95 and social threats.”
Self-citationNeural Bases of Collective Social Behavior and Group Interactions across Species
Williams, Z. M., Jurgensen, J., Williams, L., & Lee, S. G. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0023-25.2025 · Cited by 2 · see citing works
Hormonal and behavioural responses to visual social cues in common marmosets (Callithrix jacchus)
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Natural variation in the oxytocin receptor gene predicts social observation in female prairie volesPreprint
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Multi-dimensional social relationships shape social attention in monkeys
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Multi-dimensional social relationships shape social attention in monkeysPreprint
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Multi-dimensional social relationships shape social attention in monkeysPreprint
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“11–17 Monkeys also exhibit gaze-following behavior, 8,18–22 a behavior closely related to shared or joint attention.”
InfluentialSelf-citation
- Authors
- Putnam, P. T., Roman, J. M., Zimmerman, P. E., & Gothard, K. M.
- Affiliations
- University of Arizona (US)
- Corresponding author
- Putnam, P.T.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 72
- Pages
- 47-53
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC5226068
- OpenAlex
- W2413350634
- Cited by
- 53
- References
- 57
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 2 · 2023: 1 · 2022: 5 · 2021: 6 · 2020: 5 · 2019: 4 · 2018: 11 · 2017: 6 · 2016: 3
- FWCI
- 12.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Psychoneuroendocrinology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- Funders
- University of Arizona
- National Institutes of Health
- National Institute of Mental Health (P50MH100023)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- oxytocin, gaze following, rhesus monkeys, social cognition, autism spectrum disorder, intranasal administration, social behavior, gaze, habituation, prosocial behavior
- MeSH terms
- Animals, Eye Movements, Macaca mulatta, Male, Neuropeptides, Oxytocin, Social Perception, Visual Perception
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