Oxytocin enhances neural approach towards social and non-social stimuli of high personal relevance

Abstract

Oxytocin (OT) plays a pivotal role in a variety of complex social behaviors by modulating approach-avoidance motivational tendencies, but recently, its social specificity has been challenged. Here, a randomized, double-blind, placebo-controlled study was conducted with forty young adult men, investigating the effect of a single-dose of OT (24 IU) on behavioral and neural approach-avoidance. Frontal alpha asymmetry, indexing neurophysiological approach-avoidance, was obtained from electroencephalographic recordings while participants were presented with a series of pictures, individually rated in terms of personal relevance (i.e., high versus low positive/negative emotional evocativeness) and categorized as social or non-social. Additionally, participants could prolong (approach) or shorten (avoid) the viewing-time of each picture, providing a measure of behavioral approach-avoidance. Intranasal OT enhanced both behavioral and neural approach (increased viewing-time), particularly towards negatively valenced pictures of both social and non-social nature, thus challenging the notion that OT's effects are specific to social stimuli. Neurally, OT specifically amplified approach-related motivational salience of stimuli that were self-rated to have high personal relevance, but irrespective of their social nature or rated affective valence (positive/negative). Together, these findings provide support to the General Approach-Avoidance Hypothesis of OT, suggesting a role of OT in amplifying the motivational salience of environmental stimuli with high (personal) relevance, but irrespective of their social/non-social nature.Clinical Trial Number: The study design was registered at ClinicalTrials.gov (NCT04443647; 23/06/2020; https://clinicaltrials.gov/ct2/show/NCT04443647 ).

Figure 1

Example of differential picture ratings among two exemplary subjects. Participants individually rated the ‘sociality’ and ‘valence’ of a set of 36 stimulus pictures (here, only 8 exemplary pictures are shown; see Supplementary Fig. 1 for the full stimulus set) to obtain a person-dependent scoring of the perceived social/non-social nature of the presented stimuli, as well as the stimuli’s perceived emotional evocativeness (high, low) in terms of positive/negative valence. For example, a picture of a winning football team can be anticipated to be rated with high positive valence by a person who loves sports (exemplary subject X), whereas the same picture may be rated more neutral (low positive valence) by another subject (exemplary subject Y). Likewise, for a person who owns a cat, a picture of a dead cat may evoke stronger negative valence than the picture of the dirty toilet (exemplary subject X), whereas for others, this may be the other way around (exemplary subject Y). All pictures were selected from the publicly available Nencki Affective Picture System database (NAPS).

Figure 2

Effect of oxytocin on approach/avoidance as a function of self-rated stimulus characteristics. (A) visualizes pre-to-post changes in behavioral approach-avoidance (key press task, KPT) with positive scores indexing increased approach (prolongation of viewing time by pressing the ‘up’ key) and negative scores indexing increased avoidance (shortening of viewing time by pressing the ‘down’ key). (B) visualizes pre-to-post changes in EEG frontal alpha asymmetry scores, with positive scores indicating an increase in approach-related left-sided frontal alpha asymmetry. Pre-to-post change scores are visualized separately for each treatment group (oxytocin, placebo), as a function of self-rated sociality (social, non-social), affective valence (negative, positive) and valence intensity (high, low evocativeness). Vertical bars denote  ± standard errors.