ReviewSex differences in the neural correlates of emotion: Evidence from neuroimaging
Highlights
► There are marked sex differences in the neural activation underlying emotion processing. ► Ignoring sex differences in affective neuroimaging may mask meaningful results. ► Males and females likely use different strategies during emotional processing.
Introduction
Sex differences in emotional behaviors represent some of the most robust sex stereotypes worldwide (Grossman and Wood, 1993, Plant et al., 2000, Timmers et al., 2003). For example, females are often viewed as more emotionally reactive and expressive than males. Indeed, many views of sex differences in emotional behaviors appear to be supported by striking sex differences in the prevalence of emotional disorders (Gater et al., 1998). However, empirical evidence on sex differences in specific emotional processes is mixed (Bradley et al., 2001, Fujita et al., 1991, Grossman and Wood, 1993, Seidlitz and Diener, 1998). While there is some evidence for sex differences across a range of emotional processes (i.e., emotion perception, reactivity, regulation and experience), negative findings are also common (Barrett et al., 1998). Further, most research has utilized self-report measures, which are open to language, retrospective and stereotype biases (Fischer, 2000, Fugate et al., 2009).
Neuroimaging research, which provides opportunities for the objective measurement of the neural mechanisms underlying human cognitions and behaviors, has contributed greatly to our knowledge of human emotional processes and the neural systems underlying these processes (e.g., Davidson et al., 2000, Ochsner and Gross, 2008). Thus, using neuroimaging methodologies to investigate sex differences in emotional processes may contribute to current theories of sex differences in emotion that are based largely on more subjective measures. Further, while there has been an interest in understanding the underlying causes of sex differences in emotional processes (Rutter et al., 2003), there is relatively little known about neurobiological mechanisms. Thus, neuroimaging studies of sex differences in emotional processing may also contribute to understanding such mechanisms.
Although few at present, there is a growing number of neuroimaging studies that have investigated the effects of sex on the neural function associated with emotional processes. While there have been some recent reviews that address (1) sex differences in memory and cognitive functions from a neuroscientific perspective (Andreano and Cahill, 2009, Cahill, 2006), and (2) mechanisms underlying sex differences in psychiatry (Rutter et al., 2003), to-date there are no reviews of the neuroimaging literature that focus specifically on mechanisms underlying sex differences in emotional processing in healthy individuals. Thus, the purpose of this review is to provide a synthesis of functional neuroimaging studies that have investigated sex differences in emotional processes. Due to the relatively small number of such studies, and the methodological variation between them, a meta-analysis of results was not considered appropriate. Rather, the aims of this review are to: (1) explore whether the behavioral sex differences reported (or speculated) are supported by functional neuroimaging research; (2) summarize what this research suggests about mechanisms; (3) highlight how neuroimaging findings have prompted some new hypotheses about sex differences in emotional processes; and (4) identify important methodological considerations and limitations, and provide recommendations for future research.
In the following sections, we discuss how neuroimaging research has addressed some key assertions in the literature about sex differences in emotional processes. The general assertions that will be discussed were identified based on those theories that neuroimaging research has specifically set out to test. It is notable, however, that these assertions represent those (1) that are most commonly discussed in the broader literature, and (2) for which there has been some attempts at empirically investigation (Vigil, 2009, Wester et al., 2002).These assertions are as follows. First, females are more emotionally perceptive than males. Second, females are more reactive to emotional stimuli, especially those that are threatening or traumatic. Third, females and males differ in their emotion regulation strategies and efficiency. Fourth, females have a heightened experience of emotions, especially those that are negative.
The empirical studies cited in the following review were selected on the basis that they directly (i.e., statistically) compared brain function between males and females. Because of the interpretive limitations associated with studies that simply report separate results for males and females without directly statistically assessing these differences, such studies will not be reviewed (Kaiser et al., 2009). Relevant studies were identified via Web of Science and Pub Med search engines. Functional Magnetic Resonance Imaging (fMRI) or positron emission tomography (PET) brain imaging studies were identified (note that we excluded other methodologies such as electroencephalography) that were published or in press before June 2010, where the title, abstract, or keywords included “gender” OR “sex” AND “emotion” OR “affect”, and where research was conducted with healthy control (i.e., no psychiatric) samples. All were conducted with adults unless otherwise stated. Studies were also identified via cross-referencing citations. We placed no restriction on the type of image analysis employed (e.g., whole brain voxel-based versus region of interest). We identified studies investigating aspects of emotional perception (including recognition), reactivity, regulation and experience, and only those investigating what are typically thought of as basic emotions (Bradley and Lang, 1994, Russell, 1980), including happiness, sadness, fear, anxiety, anger, disgust, contempt, and excitement. We excluded studies on hunger, thirst, monetary reward, or pain, as well as social emotions such as empathy, as these constructs are more complex and their discussion was beyond the scope of this paper. The Web of Science search resulted in 1080 papers and the PubMed search resulted in 1315 papers. From these papers, on the basis of the above criteria (plus cross-referencing), thirty two functional imaging studies (employing fMRI or PET) were identified and comprise the basis of the following discussion (see Table 1).
Section snippets
Females are more emotionally perceptive than males
Females have been found to be more skilled at decoding the emotional dispositions of others (Neff and Karney, 2005, Rosip and Hall, 2004), and more accurate in perceiving emotional prosody and facial expression (Montagne et al., 2005), although there have been some negative findings (e.g., Grimshaw et al., 2004). Such findings have fuelled the suggestion that females are generally more emotionally perceptive than males.
Five neuroimaging studies that have investigated sex differences in the
Females are more reactive to emotional stimuli
Females have been found to be more reactive to emotional stimuli, particularly those stimuli that are unpleasant, threatening or traumatic. Greater female reactivity has been found in the domains of self-report (e.g., rating stimuli according to hedonic valence, Lang et al., 1993), behavioral response (e.g., laughing and crying, Vigil, 2009), and physiological responding (e.g., event related potentials, Lithari et al., 2010), although there are also some negative findings (Fugate et al., 2009).
Males are more efficient in emotion regulation
Emotion regulation refers to any process that serves to initiate, inhibit or modulate emotional feelings or behavior. There is some evidence that males and females differ in the type and effectiveness of strategies that they employ to regulate (particularly negative) emotions. For example, females have been found to use more emotion-focused and maladaptive regulation strategies such as resignation and rumination (Donaldson et al., 2000, Hampel, 2007, Nolen-Hoeksema and Jackson, 2001). Males, on
Females experience emotions with greater frequency and intensity
There is some evidence, largely from self-report data, that females experience emotions with greater intensity than males (Brebner, 2003, Vrana and Rollock, 2002). Research has also suggested that whereas females report experiencing both positive and negative affect more often than males, sex differences in self-report are greatest for negative emotions such as fear (Canary et al., 1997, Manstead, 1998) and jealousy (Guerrero and Reiter, 1998).
We identified eleven neuroimaging studies that have
Summary
This review highlights that sex differences in the neural correlates of emotion processing are often striking. Although findings were not always consistent, some compelling patterns did emerge. These are illustrated in Fig. 1. Regarding emotion perception, although it is difficult to comment about discrete emotions (because studies often grouped emotions in analyses), emotion perception in general appeared to be associated with greater levels of limbic/subcortical and temporal activation in
Theoretical implications
The emotions that females appear to be more neurally “sensitive” to relative to males might be described as submissive or interpersonal in nature (Vigil, 2009), especially with regard to emotional reactivity. On the other hand, males may more readily recruit brain regions to engage in automatic regulation of these negative emotions, but may be more neurally sensitive than females to stimuli signalling cues of dominance or interpersonal hierarchy. These findings are consistent with evolutionary
Limitations of existing studies and future directions
This review of sex differences in the neural correlates of emotional processes provides some support for some common assertions in the extant literature regarding sex differences in emotional processes, and also affords insights into some of the potential mechanisms underlying these sex differences while providing support for some existing theoretical accounts. However, there are a number of significant gaps still to be filled. In the following section we offer a summary of the limitations of
Strengths and limitations of this review
An important strength of this review is that it represents the first attempt to synthesize the existing empirical literature on sex differences in emotional brain function. Secondly, care has been taken to separate out studies addressing different aspects of emotion processing, including perception, reactivity, regulation and experience. Thirdly, only studies where sex differences were statistically tested were included. Studies simply reporting separate tests for males and females are limited
Conclusions
We have highlighted research showing marked sex differences in the neural correlates of emotional processing. This research offers some support for existing assertions in the broader literature regarding sex differences in emotional processes, and provides clues to the neural mechanisms underlying these differences. Firstly, there is evidence that females might recruit different neurocircuitry to males during perceptual emotion processing, which may in some cases lead to more accurate or faster
Acknowledgements
This work was supported by an Australian Research Council Postdoctoral Fellowship (to S.W.), a Centre for Clinical Research Excellence Postdoctoral Fellowship (to M.B.H.Y.), and a National Health and Medical Research Council Clinical Career Development Award, Grant ID 509345 (to M.Y.).
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