Neural Correlates of Affective Experience in Men and Women
These findings are provocative because they suggest that a different approach should be taken when considering the puzzle of sex differences in emotion. Men and women differed not in the overall intensity of their affective experience, but in the neural correlates of those experiences. Specifically, women's subjective affective experience appears to be relatively more rooted in sensations from within the body, whereas men's subjective affective experience is relatively more rooted in sensations from the world.
Note that women's affective experiences were more strongly correlated than men's with increased activation in the more ventral portion of AI. There are a number of recent studies reporting that the AI—in particular, the right ventral AI (Craig, 2009)—is associated with subjective affective experience (Wager and Barrett, 2004; Wager et al., 2008; Kurth et al., 2010). Our results extend previous findings showing that women (compared with men) have relatively greater activity in insula during negative mood induction (Hofer et al., 2006) and in the ventral AI extending from ventrolateral prefrontal regions in response to negative affective images (Caseras et al., 2007). On the other hand, our results that men place relatively more emphasis (than do women) on visual processing also builds on meta-analytic evidence showing that men produce more frequent activations in occipital cortex, including V1, during affective processing when compared with women (Wager et al., 2003; Stevens and Hamann, 2012), as well as findings that the affectively evocative aspects of the visual world modulate activity in the primary visual cortex (Posner and Gilbert, 1999; Vuilleumier and Driver, 2007). Recent reviews or meta-analysis about sex differences of neural correlates of emotion (Whittle et al., 2011; Stevens and Hamann, 2012) focused mainly on whether men and women respond differently to positive vs negative stimuli, and brain regions typically targeted when a neuroscience research aims at emotional reactions (e.g. the amygdala), although one meta-analysis of them indeed showed increased activation in visual cortex during emotional tasks for men compared with women (Stevens and Hamann, 2012). The previous neuroimaging studies only show sex differences from a quantitative standpoint of comparing intensities. Our results provide clearer explanation, however, such that women might experience more 'self-focused' emotion (i.e. they experience affect as the body's response to the world around them), whereas men might experience more 'world-focused' emotion (i.e. they experience affect as a property of the world, much as people experience color).
A more speculative interpretation of our findings is that men are more effective at automatic affect regulation when compared with women. This is because the AI regions where men showed stronger functional connectivity with dACC were located in its more dorsal sector, which is part of the ventral attention network involved in the regulation of attention (Kurth et al., 2010). Such evidence inspires us to speculate that during evocative episodes, men might be more capable of shifting attention to the processing of exteroceptive cues (through the switching mechanism between the processing internal information vs external cues, see Sridharan et al., 2008; Menon and Uddin, 2010), whereas women remain more interoceptively focused on bodily sensations. Neuroimaging studies also provide support for the idea that men engage in more efficient automatic emotion regulatory processes than women (Thomas et al., 2001; Williams et al., 2005; Koch et al., 2007; Kempton et al., 2009; see the discussion in a recent review Whittle et al., 2011). Extensive evidence suggests that the dACC is a core brain region involved in emotional regulation (Ochsner and Gross, 2008). In light of these previous findings, our result of stronger dAI–dACC connectivity in men also suggests that men have more efficient neural systems for regulation of emotion (Koch et al., 2007; McRae et al., 2008), perhaps, in part, because they are more externally focused. Also we found stronger association between ventrolateral prefrontal cortex activity and subjective ratings in men, which is also suggestive of more regulative process in men.
We found additional results such as more activation related to emotional experiences in the amygdala in women. In fact, however, the previous studies have not shown consistent results regarding sex differences in amygdala response; for example, men exhibited greater amygdala response to sexual images (Hamann et al., 2004), but the same author summarized the pattern of the amygdala response in men and women to emotional stimuli in previously reported studies and suggested a great variety of patterns by different experimental paradigms (see the review in Hamann, 2005). The results from a couple of recent studies also vary in the link between sex and amygdala response to emotional material. For example, individual differences in trait anxiety scores were correlated with amygdala reactivity to angry facial expressions only among men (Carre et al., 2012). On the one hand, women showed greater left amygdala activation in contrast to men, who in turn showed greater right amygdala activation during viewing IAPS pictures (Aikins et al., 2010). Similarly, this sex-related lateralization (female-left/male-right) of amygdala activation was found in other studies (Cahill, 2003a, b), although other studies have failed to find this effect (Kensinger and Schacter, 2006, 2008; Talmi et al., 2008). The sex difference of amygdala seems still inconclusive, thus it is not easy to converge our present finding to the previous evidences. The only difference between our analysis and others is that we correlated amygdala activation with the ratings that represent moment-to-moment subjective emotional experiences. Therefore, our results might reflect neural association with emotional experiences better and the sex difference was enhanced. These are mostly speculations, however, and need further confirmation in the future.
Although we are focusing on the sex difference of emotional experiences especially in interoceptively or exteroceptively oriented neural process in the insula and visual cortex, the findings in this study could be viewed from other perspectives. For example, whereas women exhibited more activation during perception of 'suffering' or 'compassion' experiences in areas involved in basic emotional, empathic and moral phenomena, such as basal regions and cingulate and frontal cortices, activation in men was restricted mainly to the occipital cortex and parahippocampal gyrus (Mercadillo et al., 2011). This is partly consistent with our findings in terms of the dominance of the occipital cortex in men. According to the empathizing-systemizing theory (Baron-Cohen, 2005), women are stronger empathizers than men. Our ROIs—the insula and ACC—are key areas of the 'social brain' (Happe et al., 1996; Baron-Cohen et al., 1999; Castelli et al., 2002; Frith and Frith, 2003; Baron-Cohen, 2009), where sex differences have been previously found (Han et al., 2008; Rueckert and Naybar, 2008; Schulte-Ruther et al., 2008; Proverbio et al., 2009). In particular, AI is consistently involved in other complex mental phenomena like empathy, compassion, fairness and cooperation, such that AI plays an important role in 'social emotions' (affective states that arise when interacting with other people; see Lamm and Singer, 2010). In this regard, another explanation for our findings might be that women are more empathetic and have enriched social cognition relative to men, such that they show greater activation in social brain—the insula in particular—whereas men are better at systemizing reflected in greater activation in the occipital visual cortex. Given that the task used in this experiment was not a social task, and that the brain regions within the 'social brain' are largely overlapping with those in the 'emotional brain' (Barrett and Satpute, 2013), this explanation seems highly speculative.
If we were to speculate on the biological basis of this sex difference, a hormonal effect is the most interpretable and what we can most easily think of. In the brain—both human and nonhuman animals (e.g. rhesus monkeys, rats)—there are high concentrations of male sex hormone (androgen) receptors throughout cerebral cortex, especially in the visual cortex (Clark et al., 1988; Nunez et al., 2003; DonCarlos et al., 2006). Androgens, not estrogen, are also responsible for controlling the development of neurons in the visual cortex during embryogenesis, meaning that males have >20% more of these neurons than females (Nunez et al., 2000, 2001). These evidences are highly suggestive of hormonal effect on the men's tendency to rely on exteroceptive visual input. On the other hand, it is still unclear whether female sex hormones influence directly interoceptive processes in insula. But some evidence implies this possibility; the insula was differentially activated in response to affective words between the follicular and luteal phases of the menstrual cycle (Protopopescu et al., 2005). The insula was also differently activated between different kinds of estrogen therapy for postmenopausal women (specifically, whether progestin was added or not) in response to emotional picture rating task (Shafir et al., 2012). The two studies show that insula activation in response to affective stimuli is considerably influenced by hormonal changes related to menstrual cycle in women. Further, neural response in insula to affective conditioned stimuli (simple geometric figures) was reduced in men but enhanced in women after treatment of cortisol, which like estrogen, is a steroid (Merz et al., 2010). These findings suggest the possibility that the estrogen may influence emotional experiences through insula activation representing interoceptive processing in women
Finally, our findings suggest that the same content (in this case, subjective experiences of affective arousal), although predictably engaging particular brain circuits, can engage nodes in these circuits to different degrees in different individuals. Even if the participants in the present study reported feeling the same experience, this report could contain subjective content that varied in its exteroceptive vs interoceptive focus. In this regard, our findings are consistent with a large body of behavioral evidence suggesting that even though people use the same words to represent and communicate their subjective affective experiences, they use those words to communicate particular properties of those experiences (e.g. 'valence' and 'arousal' properties; see Barrett, 2004). For example, some people use the word 'angry' to communicate a highly aroused, unpleasant feeling that involves the perception of offense, whereas others use the word to communicate just an 'unpleasant' feeling. Future studies should consider the possibility that it is the focus on the interoceptive vs exteroceptive aspects of affective experience, rather than its intensity per se, that might best reveal individual differences in subjective experience, whether due to sex, age, personality differences or psychopathology.
Discussion
These findings are provocative because they suggest that a different approach should be taken when considering the puzzle of sex differences in emotion. Men and women differed not in the overall intensity of their affective experience, but in the neural correlates of those experiences. Specifically, women's subjective affective experience appears to be relatively more rooted in sensations from within the body, whereas men's subjective affective experience is relatively more rooted in sensations from the world.
Note that women's affective experiences were more strongly correlated than men's with increased activation in the more ventral portion of AI. There are a number of recent studies reporting that the AI—in particular, the right ventral AI (Craig, 2009)—is associated with subjective affective experience (Wager and Barrett, 2004; Wager et al., 2008; Kurth et al., 2010). Our results extend previous findings showing that women (compared with men) have relatively greater activity in insula during negative mood induction (Hofer et al., 2006) and in the ventral AI extending from ventrolateral prefrontal regions in response to negative affective images (Caseras et al., 2007). On the other hand, our results that men place relatively more emphasis (than do women) on visual processing also builds on meta-analytic evidence showing that men produce more frequent activations in occipital cortex, including V1, during affective processing when compared with women (Wager et al., 2003; Stevens and Hamann, 2012), as well as findings that the affectively evocative aspects of the visual world modulate activity in the primary visual cortex (Posner and Gilbert, 1999; Vuilleumier and Driver, 2007). Recent reviews or meta-analysis about sex differences of neural correlates of emotion (Whittle et al., 2011; Stevens and Hamann, 2012) focused mainly on whether men and women respond differently to positive vs negative stimuli, and brain regions typically targeted when a neuroscience research aims at emotional reactions (e.g. the amygdala), although one meta-analysis of them indeed showed increased activation in visual cortex during emotional tasks for men compared with women (Stevens and Hamann, 2012). The previous neuroimaging studies only show sex differences from a quantitative standpoint of comparing intensities. Our results provide clearer explanation, however, such that women might experience more 'self-focused' emotion (i.e. they experience affect as the body's response to the world around them), whereas men might experience more 'world-focused' emotion (i.e. they experience affect as a property of the world, much as people experience color).
A more speculative interpretation of our findings is that men are more effective at automatic affect regulation when compared with women. This is because the AI regions where men showed stronger functional connectivity with dACC were located in its more dorsal sector, which is part of the ventral attention network involved in the regulation of attention (Kurth et al., 2010). Such evidence inspires us to speculate that during evocative episodes, men might be more capable of shifting attention to the processing of exteroceptive cues (through the switching mechanism between the processing internal information vs external cues, see Sridharan et al., 2008; Menon and Uddin, 2010), whereas women remain more interoceptively focused on bodily sensations. Neuroimaging studies also provide support for the idea that men engage in more efficient automatic emotion regulatory processes than women (Thomas et al., 2001; Williams et al., 2005; Koch et al., 2007; Kempton et al., 2009; see the discussion in a recent review Whittle et al., 2011). Extensive evidence suggests that the dACC is a core brain region involved in emotional regulation (Ochsner and Gross, 2008). In light of these previous findings, our result of stronger dAI–dACC connectivity in men also suggests that men have more efficient neural systems for regulation of emotion (Koch et al., 2007; McRae et al., 2008), perhaps, in part, because they are more externally focused. Also we found stronger association between ventrolateral prefrontal cortex activity and subjective ratings in men, which is also suggestive of more regulative process in men.
We found additional results such as more activation related to emotional experiences in the amygdala in women. In fact, however, the previous studies have not shown consistent results regarding sex differences in amygdala response; for example, men exhibited greater amygdala response to sexual images (Hamann et al., 2004), but the same author summarized the pattern of the amygdala response in men and women to emotional stimuli in previously reported studies and suggested a great variety of patterns by different experimental paradigms (see the review in Hamann, 2005). The results from a couple of recent studies also vary in the link between sex and amygdala response to emotional material. For example, individual differences in trait anxiety scores were correlated with amygdala reactivity to angry facial expressions only among men (Carre et al., 2012). On the one hand, women showed greater left amygdala activation in contrast to men, who in turn showed greater right amygdala activation during viewing IAPS pictures (Aikins et al., 2010). Similarly, this sex-related lateralization (female-left/male-right) of amygdala activation was found in other studies (Cahill, 2003a, b), although other studies have failed to find this effect (Kensinger and Schacter, 2006, 2008; Talmi et al., 2008). The sex difference of amygdala seems still inconclusive, thus it is not easy to converge our present finding to the previous evidences. The only difference between our analysis and others is that we correlated amygdala activation with the ratings that represent moment-to-moment subjective emotional experiences. Therefore, our results might reflect neural association with emotional experiences better and the sex difference was enhanced. These are mostly speculations, however, and need further confirmation in the future.
Although we are focusing on the sex difference of emotional experiences especially in interoceptively or exteroceptively oriented neural process in the insula and visual cortex, the findings in this study could be viewed from other perspectives. For example, whereas women exhibited more activation during perception of 'suffering' or 'compassion' experiences in areas involved in basic emotional, empathic and moral phenomena, such as basal regions and cingulate and frontal cortices, activation in men was restricted mainly to the occipital cortex and parahippocampal gyrus (Mercadillo et al., 2011). This is partly consistent with our findings in terms of the dominance of the occipital cortex in men. According to the empathizing-systemizing theory (Baron-Cohen, 2005), women are stronger empathizers than men. Our ROIs—the insula and ACC—are key areas of the 'social brain' (Happe et al., 1996; Baron-Cohen et al., 1999; Castelli et al., 2002; Frith and Frith, 2003; Baron-Cohen, 2009), where sex differences have been previously found (Han et al., 2008; Rueckert and Naybar, 2008; Schulte-Ruther et al., 2008; Proverbio et al., 2009). In particular, AI is consistently involved in other complex mental phenomena like empathy, compassion, fairness and cooperation, such that AI plays an important role in 'social emotions' (affective states that arise when interacting with other people; see Lamm and Singer, 2010). In this regard, another explanation for our findings might be that women are more empathetic and have enriched social cognition relative to men, such that they show greater activation in social brain—the insula in particular—whereas men are better at systemizing reflected in greater activation in the occipital visual cortex. Given that the task used in this experiment was not a social task, and that the brain regions within the 'social brain' are largely overlapping with those in the 'emotional brain' (Barrett and Satpute, 2013), this explanation seems highly speculative.
If we were to speculate on the biological basis of this sex difference, a hormonal effect is the most interpretable and what we can most easily think of. In the brain—both human and nonhuman animals (e.g. rhesus monkeys, rats)—there are high concentrations of male sex hormone (androgen) receptors throughout cerebral cortex, especially in the visual cortex (Clark et al., 1988; Nunez et al., 2003; DonCarlos et al., 2006). Androgens, not estrogen, are also responsible for controlling the development of neurons in the visual cortex during embryogenesis, meaning that males have >20% more of these neurons than females (Nunez et al., 2000, 2001). These evidences are highly suggestive of hormonal effect on the men's tendency to rely on exteroceptive visual input. On the other hand, it is still unclear whether female sex hormones influence directly interoceptive processes in insula. But some evidence implies this possibility; the insula was differentially activated in response to affective words between the follicular and luteal phases of the menstrual cycle (Protopopescu et al., 2005). The insula was also differently activated between different kinds of estrogen therapy for postmenopausal women (specifically, whether progestin was added or not) in response to emotional picture rating task (Shafir et al., 2012). The two studies show that insula activation in response to affective stimuli is considerably influenced by hormonal changes related to menstrual cycle in women. Further, neural response in insula to affective conditioned stimuli (simple geometric figures) was reduced in men but enhanced in women after treatment of cortisol, which like estrogen, is a steroid (Merz et al., 2010). These findings suggest the possibility that the estrogen may influence emotional experiences through insula activation representing interoceptive processing in women
Finally, our findings suggest that the same content (in this case, subjective experiences of affective arousal), although predictably engaging particular brain circuits, can engage nodes in these circuits to different degrees in different individuals. Even if the participants in the present study reported feeling the same experience, this report could contain subjective content that varied in its exteroceptive vs interoceptive focus. In this regard, our findings are consistent with a large body of behavioral evidence suggesting that even though people use the same words to represent and communicate their subjective affective experiences, they use those words to communicate particular properties of those experiences (e.g. 'valence' and 'arousal' properties; see Barrett, 2004). For example, some people use the word 'angry' to communicate a highly aroused, unpleasant feeling that involves the perception of offense, whereas others use the word to communicate just an 'unpleasant' feeling. Future studies should consider the possibility that it is the focus on the interoceptive vs exteroceptive aspects of affective experience, rather than its intensity per se, that might best reveal individual differences in subjective experience, whether due to sex, age, personality differences or psychopathology.