Elsevier

Cortex

Volume 70, September 2015, Pages 146-154
Cortex

Special issue: Research report
Is it me or is it you? Behavioral and electrophysiological effects of oxytocin administration on self-other integration during joint task performance

https://doi.org/10.1016/j.cortex.2015.04.017Get rights and content

Abstract

The neuropeptide oxytocin has been associated with promoting various social behaviors in humans including cooperation and trust. Surprisingly little, however, is known about the possible role of oxytocin in processes required for social interactive behavior such as joint task performance. The current study investigated whether intranasal administration of oxytocin leads to increased self-other integration using a social Simon task. A placebo-controlled double-blind between-subjects design was used. Behavioral and EEG measures were obtained from 63 healthy male volunteers who either received 24 intranasal units (IU) oxytocin or a placebo while they performed the social Simon task in an individual and a joint/social context. The behavioral results demonstrated an enhanced Simon effect in the social context after oxytocin administration. At the electrophysiological level, the stimulus-locked N2 component, reflecting response conflict, was increased in the social compared to the individual context for Go trials, but only after oxytocin administration. The P3 component, reflecting response inhibition, was increased for social compared to individual contexts, irrespective of condition. Both the behavioral and N2 findings suggest that oxytocin enhances self-other integration. While more inhibition is needed in the social context, this process seems less sensitive to changes in self-other integration. To conclude, the current study is the first to show oxytocin-induced modulations of processes that play a central role in joint task performance and thus importantly adds to our understanding of the neurocognitive mechanisms underlying the diverse social effects of oxytocin.

Introduction

The neuropeptide oxytocin, in popular science frequently referred to as “the love hormone”, is thought to modulate and promote various social cognitive behaviors (Bakermans-Kranenburg and van IJzendoorn, 2013, Bartz et al., 2011, Bos et al., 2012, Macdonald and Macdonald, 2010). This line of research on oxytocin-induced effects on social cognition followed from animal research showing that the hormone influences bonding and affiliative behavior in different species (Insel and Young, 2001, Uvnas-Moberg, 1998). More recently, an increasing number of studies have demonstrated comparable social effects of intranasal oxytocin in humans. For example, Kosfeld, Heinrichs, Zak, Fischbacher, and Fehr (2005) showed that males who received a nasal spray with oxytocin engaged in more trust behavior in a trust game than males who received a placebo spray. Similar, oxytocin made people more generous when instructed to divide an amount of money among oneself and an anonymous stranger (Zak, Stanton, & Ahmadi, 2007).

However, results regarding the social effects of oxytocin are not unambiguous. Decreased generosity was for example shown in a study using the dictator game (Radke & de Bruijn, 2012), illustrating the context-dependency of oxytocin effects (see also Olff et al., 2013). Similarly, oxytocin has been found to increase cooperative behavior, but only when participants were introduced to the other player prior to the task (Declerck, Boone, & Kiyonari, 2010). De Dreu et al. (2010) also emphasized the importance of the social relationship between people involved by showing in a series of studies that oxytocin promotes trust and cooperation towards individuals assigned to the in-group but defensive aggression towards individuals assigned to a competing out-group.

On a more basic cognitive level, studies have also shown effects of oxytocin on attention and perception of social cues (Domes et al., 2013, Ellenbogen et al., 2012). For instance, after oxytocin administration people look more and longer to the eye region of faces (Guastella, Mitchell, & Dadds, 2008) and people display improved recognition of emotions based on the eyes only (Domes, Heinrichs, Michel, Berger, & Herpertz, 2007). Moreover, administration of oxytocin results in faster recognition of slowly appearing sex and relationship related words while oxytocin has no effect on the recognition of neutral words (Unkelbach, Guastella, & Forgas, 2008). Taken together, these studies demonstrate oxytocin-induced modulations of both high level social behaviors such as trust, generosity and cooperation and more low-level cognitive processing of social cues. This line of research has thus given important input to the assumption that oxytocin plays a pivotal role in facilitating social behavior. However, surprisingly little research so far has focused on the effects of oxytocin on processes involved in actual interacting or jointly acting individuals even though interactive behavior or joint task performance is at the core of human's social nature.

Integration of one's own and other's actions or tasks is crucial for efficient social interactions. However, self-other integration may also lead to interference during joint task performance when knowledge of a co-actor's task or consequences of actions performed by a co-actor interfere with one's own behavior. An increasing number of studies have used a variant of the standard Simon task, known as the social Simon task (Sebanz, Knoblich, & Prinz, 2003) to investigate modulations of self-other integration processes during joint task performance. In the original Simon task (Simon, 1969), visual stimuli are presented left and right of a fixation cross. The participant is instructed to respond to the stimuli with a left or right located button depending on a feature of the stimulus (e.g., the color of the stimulus). Due to the task-irrelevant spatial location of the stimulus and the spatial location of the buttons a compatibility effect emerges: people are faster in responding to a stimulus when stimulus and response location are compatible and slower when stimulus and response location are incompatible. When participants are instructed to respond to only one color with one of the spatially located buttons –transforming the Simon task into a Go-NoGo task - this compatibility effect is no longer present: reaction times are similar for compatible and incompatible trials.

In the social version of the Simon task, two participants sitting next to each other perform a complementary Go/NoGo version of the task together, i.e., each participant responds to only one color with one button. Interestingly, Sebanz et al. (2003) showed that the compatibility effect re-emerges in this situation. The effect has since then been referred to as the social Simon effect (SSE; for a recent review see Dolk et al., 2014). The SSE is thought to reflect the formation of shared action or task representations during joint task performance (Sebanz et al., 2006, Sebanz et al., 2003). Because people incorporate the action representation of their co-actor into their own action repertoire, the situation becomes similar as to when the (standard) Simon task is performed individually. Thus, the SSE emerges as a result of the social situation in which the task is performed and the fact that people are social in nature and automatically share each other's action representations (Sebanz et al., 2006). More recently, the SSE has also been suggested to reflect a discrimination problem resulting from perceived similarity between the action consequences of one's own responses and those of a co-actor (the so-called referential coding account; Dolk et al., 2013, Dolk et al., 2014). Please note that the aim of the current study is not to clarify the exact nature of the SSE, but to investigate whether oxytocin may modulate self-other integration irrespective of whether this is associated with shared representations or referential-coding processes.

Along with behavioral indices self-other integration processes can also be studied using electrophysiological measures. The added value of this approach is that it enables detailed investigation of stimulus-induced response conflict or inhibition processes that go unnoticed when looking at behavioral measures alone. Previous event-related potential (ERP) studies using (variants of) the social Simon task have mainly focused on the stimulus-locked P3 component following NoGo trials (de Bruijn et al., 2008, Sebanz et al., 2006, Tsai et al., 2006). The NoGo P3 ERP component is thought to reflect response inhibition (Bokura et al., 2001, Falkenstein et al., 1995, Tekok-Kilic et al., 2001) and studies have demonstrated larger P3 amplitudes in the social compared to the individual version of the social Simon task. This finding has been interpreted as reflecting an increased need for inhibition when the task is performed together with a co-actor (see e.g., Sebanz et al., 2006). Importantly, a NoGo trial requires a Go response from the co-actor and when the task of the co-actor is shared or integrated, one may need more inhibition or a different and more selective inhibition process (Cavallo, Catmur, Sowden, Ianì, & Becchio, 2014) to overcome the activation associated with the co-actor's Go response (de Bruijn et al., 2008).

Another ERP component of interest in this paradigm is the stimulus-locked N2. The N2 is thought to reflect response conflict elicited by simultaneously activated, but conflicting, response tendencies (see e.g., Yeung, Botvinick, & Cohen, 2004). In general, the N2 is enlarged for trials that elicit a response conflict, e.g., infrequent trials (Nieuwenhuis et al., 2003) or incongruent compared to congruent stimuli in a Flankers task (see e.g., de Bruijn et al., 2004, de Bruijn et al., 2006, Yeung et al., 2004). In the social Simon task, response conflict arises from the different task rules for the two actors as, for example, a Go trial for the participant requires a NoGo response from the co-actor. Hence, when co-representation of the co-actor's task takes place, a conflict occurs since the to be executed response is associated with an inhibition by the co-actor. Increased response conflict as reflected in larger N2 amplitudes are thus expected in the social compared to the individual setting.

Although the SSE has been the focus of a rapidly growing number of studies, no one has to our knowledge investigated the effects of oxytocin on self-other integration and its electrophysiological correlates. The aim of the current study is to bridge this gap by nasally administering oxytocin or placebo to two groups of male participants before they perform both the individual and the social version of the social Simon task. Because of the known pro-social effects of oxytocin on both high and low-level processes such as trust and attention to social cues, an oxytocin-induced increase in self-other integration, as reflected in a larger SSE, is expected. A similar pattern is expected for the electrophysiological measures, with increased P3 and N2 effects for the social setting in the oxytocin condition compared to placebo.

Section snippets

Participants

Seventy healthy heterosexual male volunteers participated in the study. Exclusion criteria were use of medication, medical or physical illness, excessive drug or alcohol use and excessive smoking (>15 cigarettes per day). Three participants were excluded because they did not follow the instructions and four participants were excluded because of missing ERP data due to technical problems. Data of the remaining 63 participants (Mean Age: 22.8 yrs, SD: 3.8, Range: 18–35) were included in the

Behavioral results

The reaction-time analyses revealed a significant main effect of Compatibility [F(1,61) = 4.49, p = .038] with faster RTs on compatible (338 msec) than on incompatible trials (341 msec). Neither the main effect of Condition [F < 1] nor the main effect of Context [F(1,61) = 3.07, p = .085] was significant. As expected, a significant Context × Compatibility interaction effect [F(1,61) = 16.97, p < .001] was found, demonstrating a larger compatibility effect in the social (7 msec; the so-called

Discussion

The aim of the present study was to investigate the role of oxytocin in self-other integration during joint task performance using the social Simon task. Participants who received oxytocin showed a larger SSE than participants in the placebo group. Also, N2 amplitudes on Go trials were larger in the social compared to the individual context, but only for participants receiving oxytocin. P3 amplitudes were larger in the social than in the individual context, but this effect of context was not

Acknowledgments

This study was supported by a personal grant to EdB by the Netherlands Organization for Scientific Research (NWO; VIDI Grant no. 452-12-005).

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