Introduction

Large-scale epidemiological studies consistently reveal that women typically develop anxiety disorders at twice the rate of men (Australian Bureau of Statistics, 2007, 2015; Kessler et al., 1994, 2005; McLean et al., 2011). Despite this prevalence, the mechanisms underlying this female vulnerability remain unknown. One possibility is that women display greater emotional reactivity than men (Stevens & Hamann, 2012). Two dominant theoretical models of affective processing exist. The motivational model of attention and affective states (motivational model) proposes a biphasic perspective.

Specifically, stimulus valence elicits activation in underlying appetitive and aversive systems which drive pleasant emotional states and approach

behaviours, and unpleasant emotional states and avoidance respectively (Lang & Bradley; Lang, Bradley, & Cuthbert, 1997). Valence is argued to reflect initial selective attention capture by salient image content as determined by the dominant motive system, while arousal is thought to reflect the level of energy and activation mobilised within each system during the processing of

emotional stimuli (Lang & Bradley, 2010; Lang et al.). Davidson et al. (2002) extended the motivational model to propose the appetitive system led to activation predominantly in the left, and the aversive system in the right hemisphere. The motivational model predicts greater cortical reactivity to both unpleasant and pleasant stimuli compared to neutral stimuli (Cuthbert et al., 2000) and several ERP studies report an inverted ‘U’ function of arousal and valence (related in a nonlinear manner) consistent with this model (e.g., Cuthbert et al.; Keil et al., 2002; Schupp et al., 2003).

In contrast, the negativity bias hypothesis proposes that aversive system activation is greater than appetitive system activation in response to equally intense appetitive and aversive cues (Ito & Cacioppo, 2005; Ito, Cacioppo, & Lang, 1998). One of the key assumptions underlying the

negativity bias is the notion of ‘negative potency’, which refers to the idea that highly unpleasant stimuli and events are more threatening than equally intense pleasant stimuli and events are positive. Specifically, negative stimuli/events are experienced with increased emotional reactivity than pleasant

stimuli/events, and responses to unpleasant events are typically more varied which subsequently results in a larger influence of unpleasant events/stimuli (Rozin & Royzman, 2001). Therefore, the negativity bias hypothesis predicts greater cortical reactivity to unpleasant compared to pleasant and neutral stimuli (Cacioppo & Berntson, 1994; Ito & Cacioppo). A fundamental question in this field is whether women are more cortically reactive to emotional stimuli in general (in line with the motivational model), or whether their responding reflects a specific sensitivity to unpleasant/threat stimuli (reflecting a

negativity bias).

Previous behavioural, physiological, and neuroimaging studies have shown that men and women differentially process emotional stimuli. Men have been shown to rate pleasant stimuli, particularly erotic stimuli, as significantly more pleasant and arousing (e.g., Bianchin & Angrilli, 2012; Bradley & Lang, 2007; Bradley et al., 2001a; Chivers et al., 2010; Lang et al., 1997;

Rozenkrants & Polich, 2008b; Rupp & Wallen, 2008; Sabatinelli et al., 2004; Sass et al., 2010). Conversely, women have been found to have faster reaction times and higher accuracy to emotive (predominantly unpleasant) stimuli

relative to men (e.g., Li et al., 2008; Whittle et al., 2011), and have greater self- reported arousal and unpleasantness ratings of unpleasant stimuli compared to men (e.g., Bradley et al., 2001b). Women have also been shown to exhibit greater physiological reactivity compared to men as demonstrated by higher levels of fear bradycardia (i.e., immobility and sustained cardiac deceleration) and greater facial electromyography activity when viewing unpleasant stimuli (Bianchin & Angrilli;Bradley et al. 2001b; Chentsova-Dutton & Tsai 2007; Hillman, Rosengren, & Smith, 2004; Kemp et al., 2004; Lang & Bradley, 2010). Skin conductance responses (SCR), which provide an index of physiological arousal, have been shown to be greater in response to stimuli depicting animal/human threat and mutilation for both men and women. However, women displayed enhanced SCR changes in response to unpleasant compared to pleasant and neutral stimuli while men showed similar responses for both pleasant and unpleasant stimuli compared to neutral stimuli (Bradley et al., 2001b). Further, while startle reflex, which is sensitive to unpleasant emotional stimuli, has been shown to be enhanced in women (Bianchin & Angrilli), other studies have failed to show sex differences in startle reflex amplitude during both appetitive and aversive conditions (e.g., Bradley et al., 2001b; Hillman, Rosengren, & Smith, 2004), indicating that sex may not influence the startle reflex.

Further, while neuroimaging research has revealed that similar brain areas are stimulated in response to pleasant and unpleasant stimuli in women and men, amygdala and visual cortex activation has been shown to be greater in men relative to women during the viewing of erotic stimuli (Hamann et al., 2004; Karama et al., 2002; Kemp, Silberstein, Armstrong, & Nathan, 2004;

Lithari et al., 2010; Sabatinelli et al., 2004; Wrase et al., 2003). When considered together, present findings are overall suggestive of greater

appetitive system activation in men and increased aversive system activation in women.

Nonetheless, while extensive research into sex differences in appetitive and aversive system processing has been performed using behavioural measures (e.g., valence and arousal ratings), physiological measures (e.g., SCR, heart rate, startle reflex, facial electromyography), and neurophysiological measures (e.g., fMRI), this body of research is

inconclusive and inconsistent, with inconsistencies in findings potentially arising as a result of their poor temporal resolution (Hajcak et al., 2012). Conversely, event-related potentials (ERPs) have high temporal resolution which permits the delineation of precise temporal processes associated with emotion processing and thus extension of knowledge beyond behavioural, physiological, and neuroimaging studies. However, despite their utility of offering unique insights into an emotional response over time, less

experimental focus has been directed towards investigating sex differences in the electrophysiological activation involved in emotion processing.

ERPs constitute a powerful tool for exploring and providing insight into cortical mechanisms associated with emotional processing (Fabiani et al., 2000), with enhanced ERP amplitudes reflecting early emotional reactivity and later processing of emotionally salient stimuli (Carretie, Martin-Loeches, Hinojosa, & Mercado, 2001). The temporal courses of ERP valence and arousal differ whereby valence is thought to influence relatively early (100- 200ms) ERP components and arousal to affect later (200-1000ms) ERP

components (Codispoti et al., 2007; Gianotti et al., 2008; Olofsson & Polich, 2007; Olofsson et al., 2008; Zhang, Zhou, & Oei, 2011). Further, several ERP research studies have also associated early cortical reactivity to emotional stimuli with early ERP components, such as the P1 which is seen to reflect early preconscious visual processing when activated at occipital sites (Hillyard & Anllo-Vento, 1998; Luck et al., 2000; Olofsson et al., 2008). Early

emotional reactivity has also been associated with the N1 and N2 components, which are maximal at frontal sites (Hajcak et al., 2010), and which are seen to reflect automatic preconscious and early conscious processing of emotional stimuli respectively (Lithari et al., 2010; Näätänen, 1992). The emotional ERP literature has revealed that the P3 component, maximal at parietal sites, is involved in the later conscious appraisal of emotional stimuli, and subsequent allocation of attention to emotionally salient stimuli and modulation of emotional responses prior to later emotion regulation processes (Luck, 2014; Moser et al., 2009; Olofsson et al., 2008; O’Reilly et al., 2004). Previous emotional ERP research has reported an index of later conscious processing in the Late Positive Potential (LPP) which has been found to be maximal at parietal sites (Krug et al., 2000). The LPP has been reported as a consistent, non-habituating regulative response, which is highly sensitive towards high- arousing, emotionally salient stimuli compared to neutral stimuli (Hajcak et al., 2010; Hajcak & Olvet, 2008; Hot et al., 2006; Olofsson et al.; Schupp et al., 2000).

Providing evidence for the motivational model, enhanced ERP amplitudes in response to highly arousing pleasant and unpleasant stimuli compared to low arousing or neutral stimuli have been demonstrated for both

women and men (Cuthbert et al., 2000; Schupp et al., 2000). Campanella et al. (2004) demonstrated that while men and women have exhibited greater N2 reactivity to fearful faces, women also displayed greater N2 to happy faces. Studies which have examined sex differences in ERP activation to positive stimuli have reported greater cortical response to pleasant, particularly erotic, stimuli in men as compared to women (Kemp et al., 2004). However, other studies have failed to demonstrate any sex differences in the processing of either pleasant or unpleasant stimuli (Rozenkrants & Polich, 2008). ERP studies have revealed greater P3 amplitude to unpleasant compared to pleasant stimuli, in line with the negativity bias model (Delplanque et al., 2005, 2006; Ito et al., 1998). Recent ERP studies provide further evidence for a negativity bias in women, revealing that women relative to men have greater N1 and N2 amplitudes to unpleasant images (Gardener et al., 2013; Lithari et al., 2010). A further ERP study found that while both men and women displayed greater N2 and P3 amplitudes to highly unpleasant images, only women displayed greater N2 and P3 amplitudes to moderately unpleasant stimuli, reflecting greater sensitivity to unpleasant images in women (Li et al., 2008). Gasbarri et al. (2007) reported that both men and women displayed greater P3 amplitudes to unpleasant stimuli, but women displayed greater P3 amplitudes in the left hemisphere and men in the right. Given the variation in responses to emotional stimuli in women and men, the question regarding whether women display specific cortical reactivity to negative stimuli or to emotional stimuli in general requires further investigation.

In summary, two key theories have been proposed to explain the processing of emotional information, the motivational model and the negativity

bias hypothesis. With respect to cortical reactivity, the motivational model predicts greater ERP component amplitudes in response to both unpleasant and pleasant relative to neutral stimuli, with women shown to have greater

reactivity relative to men (Cuthbert et al., 2000). In contrast, the negativity bias hypothesis would predict greater ERP component amplitudes to unpleasant compared to pleasant and neutral stimuli, with women showing greater cortical reactivity than men (Cacioppo & Berntson, 1994; Ito & Cacioppo, 2005). This negativity bias in women is thought to result in heightened threat sensitivity, which if intense and generalised, can result in vulnerability for developing anxiety. Previously reported sex differences to emotional stimuli in behavioural, physiological, neurophysiological, and electrophysiological responses are varied and inconclusive.

Consequently, the current study aimed to explore sex differences in ERPs to pleasant, unpleasant, and neutral stimuli to investigate whether women display greater processing to negative stimuli specifically, in line with the negativity bias hypothesis, or to emotional stimuli in general, as outlined in the motivational model of emotion processing. As discussed previously, women have vulnerability for anxiety disorders (Australian Bureau of Statistics, 2007, 2015; Kessler et al., 1994, 2005; McLean et al., 2011) and have been shown to demonstrate greater aversive systen activation while men demonstrate increased appetitive system activation (e.g., Lithari et al., 2010; Rozenkrants & Polich, 2008). Accordingly, it was hypothesised, in accordance with the negativity bias hypothesis, that women relative to men would display greater cortical reactivity to unpleasant than pleasant or neutral stimuli, as reflected by larger ERP (P1, N1, N2, P3, and LPP) component amplitudes.

Alternatively, if women display enhanced emotional processing in general (in line with the motivational model), we predicted ERP amplitudes to pleasant and unpleasant relative to neutral stimuli to be greater for women as compared to men.