ReviewA critical review of the influence of oxytocin nasal spray on social cognition in humans: Evidence and future directions
Highlights
► Oxytocin nasal spray impressively impacts on social cognition. ► It improves the early detection of affect from social cues, particularly positive social cues. ► It improves the accurate appraisal of affect from social cues at strategic levels of processing. ► Cognitive experimental methods may provide powerful tools to identify markers of response. ► These markers have value in predicting individual behavioral and therapeutic response.
Introduction
Translational neuroscience holds at its foundation the capacity to unravel complex biological systems through the conversion of basic science discoveries into clinical practice (Insel, 2009, Zerhouni, 2005). In the area of social neuroscience, the hormone and neuropeptide oxytocin holds center stage as one of the most important chemical modulators of social behavior (Donaldson and Young, 2008, Goodson and Thompson, 2010, MacDonald and Macdonald, 2010). In mice, rats, monkeys, and sheep, central administration of OT agonists enhances social recognition, memory for peers, development of partner preference and bonding, while reducing predatory aggression (for a review see Donaldson and Young, 2008; Goodson, 2008; Young and Wang, 2004). Studies using transgenic animals have also shown that OT knockout mice lose capacity for important social behaviors and develop into more aggressive social adults (Winslow and Insel, 2002). For instance, OT knockout mice show a near complete loss of social recognition which can be fully restored by an infusion of 1.0 mg OT into the medial amygdala prior to the social encounter (Ferguson, Aldag, Insel, & Young, 2001). Other work has illustrated how region specific-distributions of oxytocin receptors appear to regulate key social behaviors (Bale et al., 2001), and how OT receptor distribution and density within these regions seem to guide social behavior across species and throughout life (Insel, 1997). Various effects on physiology and cognition have been proposed to underlie these noted benefits of oxytocin to social behavior. These include observations of reductions in fear and anxiety within social situations, the facilitation of reward and the associated processing of rewarding cues during social contact, and the enhancement of social salience to enable more effective responses to social information (for a review see Lim and Young, 2006, James, 2008, MacDonald and Macdonald, 2010).
In extending these findings to humans, it is not possible to study the impact of oxytocin on the brain and behavior with the same degree of precision. One approach has been to correlate markers of oxytocin levels and responses in blood, urine, saliva, and cerebrospinal fluid with social behavior (e.g., parental behavior; Feldman et al., 2011). This approach is limited in capacity to manipulate and study causal influences of these markers on social behavior.
This aforementioned research base has, however, provided the necessary framework to establish a fast developing body of research in humans that has administered oxytocin nasal spray to study its impact on social cognition and behavior. Kosfeld et al. (2005) seminal study in ‘Nature’ explicitly paralleled this base by demonstrating a facilitation of trusting behavior following oxytocin nasal spray administration. Since then, a range of human studies has suggested that oxytocin nasal spray impacts on a range of social behavior and cognitive processes in humans in a manner that has not previously been observed from the administration of other medications (Bartz et al., 2011, Kemp and Graustella, 2011).
It is the aim of this review to illuminate how oxytocin nasal spray influences cognition in humans using an information-processing framework, and to comment on inconsistencies in reported findings that appear to produce confusion in the scientific community regarding the effect of the spray. We will 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. This review will also highlight some of the fundamental assumptions underpinning cognitive explanatory models, to progress future cognitive experimental investigations in the oxytocin field, and to develop more sophisticated explanatory models that can predict critical behavioral outcomes. Here, we will argue that sound cognitive experimental methods can provide powerful tools to identify critical markers of the moderating impact of oxytocin administration on behavior, and for subsequent integration into more complex bio-cognitive circuitry models (Insel, 2009). We will argue that it is these circuitry models that are now needed to substantially advance this research field
Section snippets
Cognitive and behavioral science in perspective
The scientific study of human cognition can be traced back to the initial work of William Wundt and William James (Blumenthal, 1975, Wundt, 1907). Wundt, for example, promoted the goal of psychological science as the construction of explanations for mental experience and the development of techniques for objectively assessing such experience. Wundt argued that the physical and psychological sciences could only be divided by separate methodologies, involving different types of observations.
The use of cognition as a predictive marker for change in oxytocin research
A number of studies have demonstrated an impact of oxytocin nasal spray on human social behavior using an identical placebo comparison condition containing all ingredients except the active OT (in either a within or between subject design; Bartz et al., 2011). We briefly summarize here the principal potential cognitive explanations for this effect, before going on to review experimental evidence1
Effects of oxytocin on selective attention to socially-relevant information
Visual search tasks rely on the presentation of pictorial arrays in which the participant is required to rapidly distinguish between perceptual features of differing stimuli, often used to assess early, perceptual stages of processing. When positive and negative faces are presented in such tasks, parallels can be drawn between performance on these tests and one's capacity to detect differentially valenced social information in the environment. Past research using visual search tasks has shown,
Registration of emotionally expressive faces
The capacity to swiftly and accurately register the emotional tone of information is of profound importance in many social situations and is likely to contribute to effective social functioning. For example, measures of one's ability to appreciate the emotional experiences of others have been shown to predict functional social capacity beyond more traditional neuropsychological assessments (Couture et al., 2006, Losh et al., 2009). Studies exploring the impact of oxytocin on the capacity to
Memory for emotionally-expressive faces
Two studies have examined the impact of oxytocin on the encoding of human memory for socially-relevant emotional information using facial stimuli. We conducted the first of these studies (Graustella et al., 2008b) exploring the effect of oxytocin on the encoding into memory of faces displaying emotional expressions. Sixty-nine males were randomly assigned to receive oxytocin or placebo. Forty-five minutes later participants were presented with a mixture of happy, neutral, and angry faces of
Effects of oxytocin on subjective appraisals of socially-relevant emotional information
A number of studies have explored how oxytocin influences subjective appraisals of socially relevant information. Theodoridou et al. (2009) administered 24 IU oxytocin or placebo nasal spray to 96 student participants, then 25 min later presented them with 30 images of neutral faces and asked them to rate how attractive and trustworthy each face was. Participants given oxytocin rated the faces as both more attractive and more trustworthy. In a second study, Norman et al. (2010) administered
A way forward: identification of individual differences and neural circuitry as markers of response to guide therapeutic practice
Most research conducted to date has evaluated the capacity of oxytocin nasal spray to alter social cognition by averaging results across participants. This group-based approach is necessary to determine whether oxytocin nasal spray exerts a consistent and general influence on behavior and cognition. It is quite impressive, for example, that oxytocin consistently improves the ability of people to process socially relevant information. The results of such work can inform the breadth of its likely
Acknowledgments
We thank Gail Alvares, Emma Thomas, and Chathuri Yatawara for comments on this manuscript. This manuscript was partially funded by an ARC Linkage project (LP110200562) and National Health and Medical Research Projects (623624; 623625).
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