Social cognition under stress: Differential effects of stress-induced cortisol elevations in healthy young men and women

Abstract

Humans as social beings often have to perform complex social cognitive tasks while under stress (e.g., during a social conflict). Previous research has established that the brain regions responsible for social cognitive tasks are target regions for stress hormones. However, little experimental research has been done testing the acute effects of stress on social cognition. Here, we investigated whether stress exposure and the ensuing glucocorticoid (i.e., cortisol) elevations affect social cognition. Thirty-two men and 32 women were exposed to either a psychosocial stress or a non-stressful control test before assessing their social cognition using the Reading the Mind in the Eyes Test (RMET) and the Movie for the Assessment of Social Cognition (MASC). Results showed differential effects of stress-induced cortisol responses among men and women for the MASC, but not the RMET. Among men, high cortisol responders displayed elevated MASC scores compared with low cortisol responders. Moreover, for stressed men a positive association between the magnitude of the cortisol responses to the stressor and MASC scores emerged. Among women, enhanced MASC scores were found for low cortisol responders relative to high cortisol responders and non-stressed controls. A strong negative association between cortisol reactivity and MASC scores was found among women. These results imply sex specific effects of glucocorticoids on social cognition and partially support the idea of sex differences in biobehavioral stress responses, with men engaging in fight-or-flight responses while women may react to stress with tending and befriending behavior.

Introduction

The ability to form enduring social relationships permeates human society and in large part is dependent on individuals' social cognition. Social cognition refers to the mental operations that underlie social interactions and includes the ability to attribute mental states (e.g., emotions, thoughts, intentions) to oneself and others. A key brain structure implicated in successful social cognition is the prefrontal cortex (PFC) (for review, see Gallagher and Frith, 2003, Olsson and Ochsner, 2008, Singer, 2006). Aside from being implicated in social cognition, the PFC is also concerned with the feedback regulation of the stress responsive hypothalamic-pituitary-adrenal (HPA) axis (e.g., de Kloet et al., 1998). Of course, there is abundant evidence that the secretion of glucocorticoid (GC) stress hormones (e.g., cortisol; CORT) may modulate memory functioning (e.g., de Kloet et al., 1999, McGaugh and Roozendaal, 2002, Wolf, 2008). However, despite vigorous research of the past decades, only very few studies have focused on social aspects of information processing.

Meanwhile, there is considerable evidence suggesting that the effects of stress-induced CORT elevations on memory performance may be moderated by sex differences (e.g., Andreano and Cahill, 2006, Wolf et al., 2001). For example, Wolf et al. (2001) found that within a group of young adults exposed to the Trier Social Stress Test (TSST; Kirschbaum et al., 1993), CORT increases displayed a strong and negative correlation with memory retrieval performance in men, while no such correlation was found among women. Similarly, Andreano and Cahill (2006) demonstrated that low, but not high, CORT responses to stress enhanced memory consolidation and that this effect was restricted to male participants. In line with the results of Andreano and Cahill (2006), a number of studies (e.g., Buchanan and Tranel, 2008, Nater et al., 2007) have shown that memory modulation following stress exposure may depend on the magnitude of the CORT response.

In relation to this, it has been proposed that the biobehavioral response to stress differs between men and women (Taylor et al., 2000). Traditionally, the primary human stress response has been characterized as a “fight-or-flight” response. According to Taylor and colleagues, men and women share this fight-or-flight response on the physiological level, yet they differ in their behavioral stress response. Specifically, Taylor et al. (2000) suggest that, depending on the nature of the stressor, men either fight or flee. Women, on the other hand, engage in a so-called “tend-and-befriend” behavioral stress response. Here, tending refers to nurturing activities that are adaptive when the offspring is nearby, while befriending refers to the construction and maintenance of social relationships to alleviate stress. This latter issue points to the distinct possibility that in times of stress, women might show enhanced social cognition.

With this in mind, the current study was set out to determine whether stress-induced CORT elevations would yield sex-specific effects on one of the most important types of human social cognition, namely the ability to attribute internal states to oneself or others based on external cues (e.g., facial expressions, speech).