Sex Differences in the Neural Correlates of Affective Experience

Yoshiya Moriguchi; Alexandra Touroutoglou; Bradford C. Dickerson; Lisa Feldman Barrett

Disclosures

Soc Cogn Affect Neurosci. 2014;9(5):591-600. 

In This Article

Abstract and Introduction

Abstract

People believe that women are more emotionally intense than men, but the scientific evidence is equivocal. In this study, we tested the novel hypothesis that men and women differ in the neural correlates of affective experience, rather than in the intensity of neural activity, with women being more internally (interoceptively) focused and men being more externally (visually) focused. Adult men (n = 17) and women (n = 17) completed a functional magnetic resonance imaging study while viewing affectively potent images and rating their moment-to-moment feelings of subjective arousal. We found that men and women do not differ overall in their intensity of moment-to-moment affective experiences when viewing evocative images, but instead, as predicted, women showed a greater association between the momentary arousal ratings and neural responses in the anterior insula cortex, which represents bodily sensations, whereas men showed stronger correlations between their momentary arousal ratings and neural responses in the visual cortex. Men also showed enhanced functional connectivity between the dorsal anterior insula cortex and the dorsal anterior cingulate cortex, which constitutes the circuitry involved with regulating shifts of attention to the world. These results demonstrate that the same affective experience is realized differently in different people, such that women's feelings are relatively more self-focused, whereas men's feelings are relatively more world-focused.

Introduction

Western culture is preoccupied with the question of whether women are more emotional than men. People assume that women are more emotionally intense, complex and expressive, whereas men are more stoic and reserved (Lutz, 1990; Pease and Pease, 1999; Baron-Cohen, 2003; Nagourney, 2006). There is such a profound belief in this sex difference that it influences political attitudes about who can be president of the United States (Nagourney, 2006) and is used to justify why women continue to be underrepresented in positions of economic and political power that require a level head and a steady hand (Lutz, 1990). Despite the prevailing belief that women are the more emotional sex, however, objective measures of emotion do not consistently show sex differences. For example, some studies report that women show larger physiological changes in evocative situations (Bradley et al., 2001), whereas others do not (Quigley and Barrett, 1999; Kelly et al., 2006), and some studies report the opposite pattern of results (Greenwald et al., 1989). Sometimes women smile more than men (LaFrance et al., 2003) and sometimes less (Ansfield, 2007). Men and women do not differ in the magnitude of physical reactivity like cortisol level and autonomic responding when exposed to an experimental social stress (e.g. preparation for speech), although they differed in reporting irritability and fear after the task (Kelly et al., 2008). Men and women also do not differ in their subjective reports of moment-to-moment emotional experiences in response to specific events as they occur in everyday life when measured using an experience-sampling procedure, although women describe themselves as more emotional when using memory-based self-report measures (Barrett et al., 1998), this is most likely because such measures tap stereotypes and other beliefs that are strongly gendered (Robinson and Clore, 2002).

One of the reasons for the inconsistent scientific results on sex differences is that studies mainly measure the 'intensity' of experience from a quantitative standpoint. One intriguing possibility is that men and women differ not in the extent to which they experience feelings, but rather in the ingredients involved in constructing those experiences (Barrett, 2006). More specifically, both philosophical (Lambie and Marcel, 2002) and experimental (Lindquist and Barrett, 2008) evidence indicate that affective experiences are constructed from both interoceptive (i.e. self-focused) and exteroceptive (i.e. world-focused) information (Barrett, 2009a). We hypothesized that perhaps men and women differ in the relative contributions of these aspects, such that women's affective experience includes relatively more interoceptive information, whereas men's includes relatively more exteroceptive information.

This hypothesis setting is derived from published empirical evidence in the psychological literature, although this idea has not yet been tested directly. Previous studies frequently suggest that women 'somatize' more than men, i.e. women report more functional somatic symptoms (Tibblin et al., 1990; Wool and Barsky, 1994), and the researchers proposed the idea that this is because women are more attentive to their internal state (Pennebaker, 1982; Tibblin et al., 1990). On the other hand, people suppose that 'men are visual' creatures (Smith, 2000) and express their emotions in ways consistent with visual perception. Men also have the advantage in visuospatial abilities to process and interpret visual information about external objects (Voyer et al., 1995). In addition, men have a more 'externally oriented thinking' style, measured by a questionnaire (Moriguchi et al., 2007), which might translate into their more externally focused experiences of emotion when compared with women who have a more 'internal' style. Moreover, human perceivers tend to make more 'internal' attributions about the emotional behaviors that they observe in women (i.e. people understand smiles, scowls and frowns to reveal something about a woman's internal state), whereas they make more 'external' attributions about the emotional behaviors that they observe in men (i.e. expressions indicate something about a man's situational demands; Brescoll and Uhlmann, 2008; Barrett and Bliss-Moreau, 2009).

In this study, we tested the hypothesis that men and women would not differ in the intensity of their momentary subjective affective experiences but that they would differ relatively in the neural correlates of those experiences. To this end, using functional neuroimaging, we investigated whether there are differences in the regional neural activations most robustly engaged as men and women rated their affective experiences while viewing evocative images. We predicted that women's affective experience would be more strongly correlated with changes in activation in brain regions involved in representing bodily sensations, such as the anterior insula (AI), when compared with men. Based on its anatomical connections, the AI is considered to be a critical node in representing sensations from within the body and incorporating them into mental life, providing a critical substrate for the interoceptive awareness of affective experience (Mesulam and Mufson, 1982; Augustine, 1996; Craig, 2009). Importantly, the processing of the interoceptive information—information from one's own body—should be always involved in constructing all sorts of perceptual, cognitive and emotional mental events (Barrett, 2009a, b), which is why neuroimaging studies routinely report increased AI activation in thousands of experiments across a range of psychological phenomena (Craig, 2002, 2009; Herbert and Pollatos, 2012). Thus, if we find an activation in the AI in response to a mental task, it is highly suggestive that interoceptive processing is relevant to the task.

In contrast, we predicted that men would be relatively more exteroceptively focused, deriving their subjective affective experiences more from representations of visual sensations, so that such experiences would be more correlated with activation in the visual cortex, such as the primary visual cortex (V1), because this activation reflects the motivational and attentional relevance of the outer visual world (Vuilleumier and Driver, 2007; Damaraju et al., 2009). Thirty-four normal healthy adults (17 male and 17 female) rated their subjective experiences of arousal (1 = low, 2 = mid and 3 = high) while viewing 132 full-color positive, negative and neutral images while undergoing functional magnetic resonance imaging (fMRI). Positive and negative images were matched on their intensity according to published norms (see Materials and Methods).

Furthermore, we explored sex differences in the functional connectivity between the AI and the anterior cingulate cortex (ACC) while men and women rated their affective experiences in response to evocative images. The dorsal portion of the ACC is intrinsically connected to the more dorsal aspect of the AI as part of a 'ventral attention network' (Corbetta et al., 2008) that is involved in the signaling of the importance of and the regulation of attention to events and objects in the world (Dosenbach et al., 2007). Moreover, it has been proposed that spindle ('Von Economo') neurons localized within the AI and ACC (Nimchinsky et al., 1999; Allman et al., 2002; Craig, 2009) subserve a fast signaling mechanism underlying the switch between the engagement of large-scale networks processing internal information vs those at least partly devoted to processing external cues (Sridharan et al., 2008; Menon and Uddin, 2010). We expected that if men's subjective experience is more infused with exteroceptive information when compared with women, then this might occur because men show increased functional connectivity between the AI and the ACC when viewing images that evoked stronger subjective feelings.

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