Elsevier

NeuroImage

Volume 40, Issue 4, 1 May 2008, Pages 1921-1929
NeuroImage

The neural mechanism underlying the female advantage in identifying negative emotions: An event-related potential study

https://doi.org/10.1016/j.neuroimage.2008.01.033Get rights and content

Abstract

Previous studies have extensively reported an advantage of females in identifying negative facial emotions as compared with males. Nevertheless, why females are better in performance relative to males during emotion recognition tasks is still unknown, and the neural mechanism(s) underlying this phenomenon has yet to be directly investigated. As facial affects convey emotional information which is adaptively important and the recognition of a given facial affect generally evokes individuals' emotion of the same type [Dimberg, U., 1997. Facial reactions: rapidly evoked emotional responses. J. Psychophysiol. 11, 115–123], the present study assumes that the female advantage in emotion recognition may result from the attenuated sensitivity of males to emotionally negative stimuli of lesser valence intensity compared to that of females. In contrast, each gender may be comparably sensitive to emotionally negative stimuli of enhanced salience as suggested by the emotional negativity bias. To test this hypothesis, event-related potentials were recorded for highly negative (HN), moderately negative (MN), and Neutral deviant images while subjects (15 males, 15 females) perform a standard/deviant categorization task, irrespective of the emotional valence of deviants. The results demonstrated more negative ERP deflections during HN condition than during MN and Neutral conditions at early N2 and later P3 components, irrespective of gender. Moreover, MN condition elicited significantly more negative deflections than the Neutral condition across N2 and P3 components only in females, and the MN  Neutral difference waveform in females during 250–450 ms interval was localized to the right prefrontal cortex. Thus, apart from the increased sensitivity of both genders to the highly negative stimuli, the present study demonstrated that women, instead of men, are sensitive to emotionally negative stimuli of lesser saliency, which may be an important mechanism underlying the female advantage in identifying negative emotions, and the right prefrontal cortex may be the neural basis underlying the female-specific sensitivity to emotionally negative stimuli of lesser salience.

Introduction

Considerable studies have revealed a gender-related dimorphism during the processing of emotional stimuli (Montagne et al., 2005, Brebner, 2003, Campanella et al., 2004, Hall, 1978, Schirmer et al., 2002, Miura, 1993, Scholten et al., 2005). Among these studies, one of the most noticeable observations is that males, as compared with females, are less capable of labeling negative affects. Apart from the early reports that females are of advantage to understanding emotional expressions from faces, gestures and voices, males were shown less accurate in recognizing emotions from faces, in particular, in recognizing negative emotions such as fear, disgust, and sadness (Hall, 1978, Miura, 1993). More recently, the studies related to psychosocial aspects of depression suggested that interpersonal communications through non-verbal emotional cues are more pronounced in females than in males (Campanella et al., 2004, Harris, 2001). Moreover, the study by Scholten et al. (2005) found that when asked to identify facial affects, healthy males had lower accuracy scores than healthy females in recognizing negative emotions, and the performances in male patients with schizophrenia were impaired to a greater extent compared with those in female patients. The similar results were also reported by Montagne et al. (2005), who observed that females were more accurate in labeling negative emotions like sadness and could identify negative facial affects (e.g. anger, disgust) at a lower emotional saturation level relative to males.

As stated above, it is apparent that males are less competent in identifying negative emotions as compared to females. This is likely to be attributed to the reduced sensitivity of males to emotionally negative stimuli relative to females since previous studies showed that the same emotionally negative pictures activated more neural substrates as well as greater cerebral activation values (e.g. in amygdala) in females relative to males (Wrase et al., 2003, Hofer et al., 2006, Orozco and Ehlers, 1998). In addition, the semantic processing is less susceptible to emotionally negative prosody in males relative to females, suggesting that the ongoing cognitive activities in males are less likely to be influenced by emotionally negative stimuli than those in females (Schirmer et al., 2004). Nevertheless, since emotional negativity bias that emotionally negative stimuli, due to their important adaptive values, are processed preferentially throughout the information processing stream has been well established (Ito et al., 1998, Delplanque et al., 2004, Huang and Luo, 2006, Yuan et al., 2007a, Yuan et al., 2007b), it seems unlikely that males have reduced sensitivity as compared with females to emotionally negative stimuli at all levels of valence intensity. In fact, the valence of the negative event is important as the human brain has differential sensitivity to emotionally negative events of varying valences, with greater emotional reactivity to extremely negative events than to moderately negative events even when individuals are engaged in a non-emotional task (Yuan et al., 2007a, Yuan et al., 2007b). On the other hand, it is often seen in life settings that males show fewer emotional responses to the negative events of lesser saliency, which, however, could elicit prominent emotional reactivity in females (most noticeably, prominent emotional responses are easily seen in females when they come across unpredictable beetles, which typically elicit less emotional reactivity in males). Thus, it is possible that males, similar to females, are sensitive to emotionally negative events with high salience as predicted by emotional negativity bias, whereas males may be less sensitive to negative stimuli of lesser valence intensity relative to females, which may be an important mechanism underlying the female advantage in identifying negative emotions.

Thus, the present study hypothesizes that humans, irrespective of gender, are sensitive to emotionally negative stimuli of high saliency such that both genders would show pronounced processing biases for highly negative stimuli at some information processing stages; however, as the valence intensity decreases to a moderate level, it is possible to observe a gender-related dimorphism that the brain sensitivity to the negative stimuli is preserved in females whereas this sensitivity is prominently reduced in males. As a result, females would still manifest prominent emotional responses to the lesser valenced negative stimuli whereas the emotional responses to the same stimuli in males would be unapparent, or even absent if subjects are engaged in a non-emotional task. For a test of this hypothesis, via high temporal resolution ERP technique, the present study mainly investigated the effect of gender on human emotional responses to negative stimuli of varying valences. As emotional responses are often triggered by unpredictable stimuli during non-emotional activities in the natural settings (most commonly in social interaction situations, some accidental words from other people offend us in a conversation) (Delplanque et al., 2005, Yuan et al., 2007a). Thus, the present study used an implicit emotional task that does not require subjects to evaluate valence, consequently to allow emotional responses in the laboratory setting to more closely resemble nature (Yuan et al., 2007a). More specifically, previous studies indicated that the early perceptual and attentional processes, as indexed by early P2 and N2 components, were modulated by emotional valence (Carreti′e et al., 2001, Huang and Luo, 2006, Carretie′ et al., 2004), and the later higher cognitive processes such as the stimulus evaluation and response decision making, as is typically reflected by late positive complex (LPC), are also influenced by emotional saliency (Ito et al., 1998, Yuan et al., 2007a, Yuan et al., 2007b). We predicted that some ERP components, such as attention-related N2 and evaluation-related P3, would see Gender by Valence interaction effects and manifest some temporal features of gender differences during the processing of emotional stimuli of varying valences.

The present study used a modified oddball paradigm that required subjects to make a standard/deviant distinction by pressing different keys, irrespective of the emotional valence of the deviants. Rather than requiring a single response for the deviants, we designed two responses to mask the true purpose of the experiment, so as to avoid a “relevance-for-task” effect that was repeatedly reported to obscure the effect of valence on ERPs (Carreti′e et al., 1996, Carreti′e et al., 2001). Moreover, according to P.J Lang's theory of emotional dimensions (Lang, 1995), valence (ranging from unpleasant to pleasant) and arousal (ranging from calm to excited) are the two primary dimensions that should be considered in emotional studies. Thus, the emotional studies that address valence effect on ERPs need to control for arousal influences across valence conditions (Lang, 1995, Johnson, 1993). Because the present study focuses on the gender-related valence effect on ERPs, and arousal influence was indicated to mask the valence effect on ERPs non-specifically (Carretie’ et al., 1997, Johnson, 1993), the stimulus materials used in the present study were the standardized emotional pictures whose valence and arousal values were normatively rated, consequently to facilitate the control for arousal influences on ERPs (Carretie’ et al., 1997, Johnson, 1993). Since a cultural bias for the International Affective Picture System (IAPS) has been reported in Chinese subjects (Huang and Luo, 2004), the pictures used to elicit emotional responses in the current study were from the native Chinese Affective Picture System (CAPS)1 (Yuan et al., 2007a, Bai and Ma, 2005). In addition, as the arousal variation from emotional stimuli to Neutral stimuli would confound the emotional effect on ERPs, in the present study, emotional pictures were selected in such a way that the arousal level was matched across the three valence conditions, in particular, between the neutral images and the two valence-differed image groups.

Section snippets

Subjects

As paid volunteers, 15 female (18–22 years; M = 20.6 years) and 15 male (18–23 years; M = 21.1 years) undergraduate students participated in the experiment. All subjects were healthy, right-handed, had normal or corrected to normal vision, and had no history of affective disorder. All participants signed an informed consent form for the experiment. The experimental procedure was in accordance with the ethical principles of the 1964 Declaration of Helsinki (World Medical Organization, 1996).

Stimuli

The

Behavioral performance

The false responses or responses exceeding time limits were rare as nearly all 30 subjects achieved 100% accuracy rates for both standard and deviant stimuli. A two-way ANOVA on RT data for deviant stimuli (Valence as within-subjects factor whereas Gender as between-subjects factor) demonstrated no significant Valence effect, or Valence by Gender interaction effect [F(2,56) = 0.96, P = 0.37; F(2,56) = 0.48, P = 0.58]. The averaged RTs in females were 518.30 ± 53.01 ms for HN, 519.50 ± 59.86 ms for MN and

Discussion

In agreement with our hypothesis, the present study observed a gender-related dimorphism in processing emotionally negative stimuli of varying valences. Apart from prominent emotional responses of both genders to the highly negative stimuli, females further showed conspicuous sensitivity to the emotionality of the MN stimuli, whose emotional salience was largely reduced compared with that of the HN stimuli. In contrast, the emotional responses to the MN stimuli were absent in males in the

Conclusion

The present study demonstrated a gender-related dimorphism in neural responses to emotionally negative stimuli of varying valences during a covert emotional task. Aside from the prominent emotional responses of both genders to the highly negative stimuli, females showed remarkable attentional and evaluative biases for the moderately negative stimuli whereas males showed neither biases for these stimuli. This suggests that the well-known female advantage in identifying negative emotions may be

Acknowledgments

This study was supported by Postgraduate Innovation Foundation of Science and Technology in Southwest University (Jiajin Yuan, b2007005), National Natural Science Foundation of China (NSFC30770727) and the National Key Discipline of Basic Psychology in Southwest University (NSKD08003).

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