Oxytocin sharpens self-other perceptual boundary
Introduction
The recognition of self-other dissimilarities and a positive perception of others are crucial for initiating social approach and developing social bonds. Beginning in the first months of life, before the development of conceptual self-knowledge, human infants are capable of distinguishing whether certain stimuli pertain to the self or to someone else (Rochat and Striano, 2000, Rochat and Striano, 2002). The ability to recognize that the other is distinct from the self is considered an early marker of typical development, and it is central to the ability to form social bonds and engage in successful social interactions (Lewis and Brooks-Gunn, 1979, Rochat and Striano, 2000, Keenan et al., 2003). Conversely, a diminished ability to discriminate whether stimuli are related to the self or to others is associated with deficits in interpersonal interactions often seen in various psychopathologies. For instance, individuals with schizophrenia exhibit both social deficits and impairment in self-recognition processes (Irani et al., 2006).
Social transactions are based on the interplay between self-other relatedness and self-other differentiation processes. As self-other perceptual differentiation and recognition are rooted in brain and mind development, based on various poorly understood neural functions, it is critical to explore the neurobiological mechanisms that regulate perceptual boundaries between the “self” and “others”.
In recent years, cross-species research has demonstrated that several evolutionarily conserved neuropeptides play a key role in diverse social behaviors (Nelson and Panksepp, 1998, Ferguson et al., 2000, Insel and Young, 2001, Panksepp, 2009, Bos et al., 2012). Among them, the neuropeptide oxytocin appears to regulate fundamental aspects of mammalian social affiliative behaviors and social cognition (Carter, 1998, Insel and Young, 2001, Donaldson and Young, 2008, Heinrichs et al., 2009, Meyer-Lindenberg et al., 2011). The oxytocinergic system also plays a critical role in diverse social behaviors, including mother–infant attachment and pair bonding (Panksepp, 1992, Carter, 1998, Pedersen et al., 2006, Donaldson and Young, 2008). In humans, oxytocin is also crucial for social interactions (Heinrichs and Domes, 2008, Heinrichs et al., 2009, Meyer-Lindenberg et al., 2011, Van IJzendoorn and Bakermans-Kranenburg, 2012). After receiving a single dose of intranasally administered oxytocin, healthy adults show decreased reactivity to social stress (Heinrichs et al., 2003) and increased approach, trust, empathy, and attachment (Kosfeld et al., 2005, Baumgartner et al., 2008, Ditzen et al., 2008, Buchheim et al., 2009, Hurlemann et al., 2010), although these effects are strongly modulated by the social context. For example, stronger oxytocin effects have been found toward in-group than out-group members (Chen et al., 2011, De Dreu, 2012, De Dreu et al., 2012). Oxytocin also dampens amygdala reactivity to threatening faces (Kirsch et al., 2005, Domes et al., 2007, Petrovic et al., 2008, Gamer et al., 2010) and modulates social memory (Heinrichs et al., 2004, Rimmele et al., 2009). In addition, oxytocin administration improves emotion recognition (Lischke et al., 2012b), responsiveness to others (Kosfeld et al., 2005), and social behavior in individuals with autism (Andari et al., 2010, Guastella et al., 2010).
Several studies from social neuroscience have found that self-other differentiation is crucial for social approach and the formation of social bonds (Rochat and Striano, 2000, Keenan et al., 2003). While several studies have demonstrated that oxytocin administration facilitates the differentiation and recognition of unfamiliar facial features, we are unaware of any studies that have specifically targeted the potential role of oxytocin in modulating recognition of self-other perceptual differences in a controlled laboratory setting. Hence, we set out to study whether oxytocin might modulate the ability to differentiate the self from others. Since in humans one's own face is considered among the most salient self-related stimuli (Brédart et al., 2006), we used a face morphing paradigm, wherein participants viewed a photo of themselves morphing into the photo of an initially unfamiliar face during a self-other differentiation task (Keenan et al., 2000, Tsakiris, 2008). As the interactions between oxytocin administration and hormonal fluctuation in women have been not systematically investigated, only men were tested.
We predicted that an increased central nervous system availability of oxytocin would increase the speed of self-other perceptual differentiation and would decrease the self-serving bias regarding the pleasantness of the own face as compared to an unfamiliar one.
Section snippets
Participants
A total of 44 male participants, aged 22–31 (SD = 2) years, were recruited from the University of Freiburg, Germany, and randomly assigned to receive oxytocin (n = 22) or placebo (n = 22) intranasally in a placebo-controlled, double-blind, between-subject design. An additional male subject was recruited and asked to provide his picture for the preparation of the “unfamiliar other” social stimulus. The participants and the unfamiliar “other” had comparable demographic characteristics (e.g., age, sex,
Results
During the self-other differentiation task, participants who received oxytocin exhibited a significantly shorter latency to discriminate between “self” and “other” (main effect of substance: F(1,42) = 4.7, p = 0.03, ηp2 = 0.5, mean ± SE % of frames, placebo: 69 ± 1.7, oxytocin: 63 ± 1.9), without any differences between groups in relation to the video morphing directions (substance × direction interaction: F(1,42)= 0.5, p > 0.05) (Fig. 1a). Overall, the reaction time was shorter when the subject's own face was
Discussion
Our study demonstrates for the first time that oxytocin administration sharpens self-other perception. In particular, during the self-other face differentiation task, oxytocin reduced the threshold to distinguish between one's own and an unfamiliar face. This finding complements previous studies showing that oxytocin increases awareness for briefly presented facial stimuli (Schulze et al., 2011), the ability to identify facial dissimilarities between unknown individuals and subtle changes of
Role of the funding source
This study is supported by the Deutsche Forschungsgemeinschaft (DFG He5310/1-1; to M.H. and F.S.C.). V.C. is supported by a research grant from the Neuropsychoanalysis Foundation; V.C. and F.S.C. gratefully acknowledge support from research fellowships of the Alexander von Humboldt Foundation.
Conflict of interest statement
None declared.
Acknowledgments
We thank Laura Huber and Anna Mauz for assistance during data collection.
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2021, Neuroscience and Biobehavioral ReviewsEffect of intranasal oxytocin administration on self-other distinction: Modulations by psychological distance and gender
2020, PsychoneuroendocrinologyCitation Excerpt :Second, previous inconsistent findings have been observed in two distinct categories of tasks. On the one hand, OT sharpens the self-other boundary in the face-morphing task (Colonnello et al., 2013), the perspective task (Tomova et al., 2019) and the perceptual task employed in the current study. The self-other distinction measured in these tasks is thought to be critical in developing and maintaining social bonds by decreasing self-centeredness (Steinbeis, 2016).
Oxytocin modulation of self-referential processing is partly replicable and sensitive to oxytocin receptor genotype
2020, Progress in Neuro-Psychopharmacology and Biological PsychiatryThe Other and Me: Effects of oxytocin on self-other distinction
2019, International Journal of PsychophysiologyCitation Excerpt :Future replication studies should therefore consider randomized task ordering. In addition, while our sample size is comparable to those of other oxytocin administration studies addressing similar research questions (e.g., Colonnello et al., 2013; De Coster et al., 2014; Abu-Akel et al., 2015; Ruissen and de Bruijn, 2015), replication studies should employ larger sample sizes in order to verify the reliability of our results. Furthermore, the visual complexity between the three tasks was different and might have contributed to the reported effects.