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Theoretical Background: Appropriately decoding and recognizing facial expressions is a substantial ability that develops very early in infancy and is crucial for the understanding of and adaptation to social interactions (Thomas, De Bellis, Graham, & LaBar, 2007). Furthermore, in humans and other primates, facial expressions serve as important social cues to regulate behavior and for establishing and maintaining social relationships (Kringelbach & Rolls, 2003). Studies with normal adults showed that they direct most of their attention to the core features of the face (i.e. eyes, nose, and mouth) and spend less time on non-feature areas while exploring facial expressions (Pelphrey et al., 2002). Within the core features, the eyes are considered to provide humans with the most information in terms of emotion recognition. Numerous studies confirmed this bias towards inspecting the eyes from very early in ontogeny (Holmes, Richards, & Green, 2006; Walker-Smith, Gale, & Findlay, 1977). Deficits in emotion recognition and eye-to-eye gaze are core symptoms of various disorders with difficulties in social interactions (e.g. autism, schizophrenia, borderline personality disorder, social phobia, etc.). In addition, individuals with a personality trait called alexithymia have distinct difficulties in recognizing emotions. Alexithymia is a non-clinical, psychological concept defined by difficulties in understanding and regulating emotions. The neuropeptide oxytocin (OT) is well known for its physiological functions in milk ejection and during labour. Apart from these functions, OT receptors are distributed in various brain areas associated with social behavior (for a review, see Heinrichs & Domes, 2008). Given that oxytocin is believed to promote social attachment in non-human mammals and approach behavior – such as trust – in humans, we hypothesized that oxytocin might also promote the ability to infer the mental state of others from social cues of the eye region in subjects with particular deficits in recognizing emotions (RMET, Baron-Cohen, 1999; Domes et al., 2007). Moreover, oxytocin was expected to improve the performance in a task testing the ability to detect subtle changes in human facial expressions (emotion recognition task; Porges et al., in press) and to modulate eye gaze when viewing videos of facial expressions.
Methods: In a placebo-controlled, double-blind design, 65 healthy male participants were randomly assigned to receive a single dose of 24 IU oxytocin intranasally 40 minutes before the experiment. During the experimental phase, participants performed an emotion recognition task. For this task, pictures of the eye region of the six basic emotions (fear, sadness, disgust, happiness, anger, surprise and neutral) were chosen from the “Pictures of Facial Affect” (Ekman & Friesen, 1976). Pictures were presented to the participants on a computer screen with four alternative labels describing what the person displayed might be thinking or feeling at the moment. While we used static stimuli of only the eye region for the first experiment, the second study used the affect recognition test, (ART; Porges et al., in press), which presents videos of faces expressing different emotions. Participants were shown 48 neutral faces in a randomized sequence, which turned into one of the six primary emotions (anger, happiness, surprise, disgust, sadness and fear) over time. Within these experiments, eye movements were assessed during the viewing of the facial expressions.
Results: Results of the first study investigating the effects of oxytocin in persons with selective difficulties in recognizing emotions showed that the single administration of 24 IU oxytocin led to an increased ability to recognize emotions in the high-alexithymic group (t30 = 2.23; p = .033), while no such effect occurred in the low-alexithymic group (t31 = -.594; p = .557). Furthermore, in the group with high alexithymia, oxytocin administration induced an improvement of emotion recognition particularly in emotions that are difficult to recognize (t30 = 2.218; p =.034). The results of the second study revealed that over the whole time sequence, subjects with oxytocin made more fixations towards the eyes (F1;59 = 3.23; p = 0.077) and spent significantly more time fixating the eye region (F1;59 = 4.42; p = 0.04) than the placebo group for happy facial expressions. In terms of the time sequence of the videos of facial expressions, we found that particularly in the early time phase during face exploration, subjects with oxytocin spent significantly more time on the eyes (F1;60 = 6.37; p = .014) and made significantly more fixations to the eyes (F1;60 = 6.73; p = .012). Moreover, subjects of the oxytocin group looked less at (F1;60 = 3.94; p = .052) and spent less time fixating on the nose (F1;60 = 3.67; p = .06) in the early detection phase.
Conclusion: This is the first study to show that a single dose of intranasal oxytocin is sufficient to improve performance in an emotion recognition task in healthy men with difficulties in identifying and describing emotions. Although alexithymia is a subclinical phenomenon, it is associated with general psychological distress, especially with depression and anxiety, and has been observed in numerous psychiatric and somatic disorders (Bankier, Aigner, & Bach, 2001; Gil et al., 2007; Le, Ramos, & Munoz, 2007; Marchesi, Bertoni, & Maggini, 2008; Saarijärvi, Salminen, Taylor, & Toikka, 2006; Taylor, Bagby, & Parker, 1997). Further, our results show that a single dose of oxytocin enhances the gaze toward the eye region for all basic emotions, and in particular in happy faces. These findings may therefore have several important clinical implications. People with impaired ability to process or regulate emotions have been shown to be at risk of developing mental disorders such as major depression, anxiety disorder, eating disorders, and substance abuse. Moreover, the inability to focus the attention toward the eyes seems to be responsible for emotion recognition deficits, for example in autism or social anxiety disorder, and thus, oxytocin may provide substantial support in the treatment of disorders with social deficits.