Elsevier

NeuroImage

Volume 21, Issue 2, February 2004, Pages 632-646
NeuroImage

Gender differences in the cortical electrophysiological processing of visual emotional stimuli

https://doi.org/10.1016/j.neuroimage.2003.09.055Get rights and content

Abstract

The processing of visual emotional stimuli has been investigated previously; however, gender differences in the processing of emotional stimuli remain to be clarified. The aim of the current study was to use steady-state probe topography (SSPT) to examine steady-state visually evoked potentials (SSVEPs) during the processing of pleasant and unpleasant images relative to neutral images, and to determine whether this processing differs between males and females. Thirty participants (15 males and 15 females) viewed 75 images low on the arousal dimension (categorised as pleasant, neutral or unpleasant) selected from the International Affective Picture System (IAPS), whilst a 13-Hz sinusoidal white visual flicker was superimposed over the visual field and brain electrical activity was recorded from 64 electrode sites. Results suggest that pleasant and unpleasant images relative to neutral images are associated with reductions in frontal latency and occipital amplitude. In addition, electrophysiological gender differences were observed despite there being no differences found between males and females on subjective mood or behavioural ratings of presented images (valence and arousal dimensions). The main gender difference reported in the current study related to the processing of unpleasant images (relative to neutral images) which is associated with widespread frontal latency reductions (predominantly right sided) in females but not in males. Our results suggest that gender differences do exist in the processing of visual emotional stimuli, and illustrate the importance of taking these differences into account during investigations of emotional processing. Finally, these gender differences may have implications for the pathophysiology of mood disorders such as depression.

Introduction

Gender differences in the brain have been well characterised in animals and to a lesser extent, in humans Cooke et al., 1998, Rabinowicz et al., 1999, Rabinowicz et al., 2002, Supprian and Kalus, 1996. Although the functional significance of these differences are unclear Rabinowicz et al., 1999, Supprian and Kalus, 1996, research is now beginning to examine the gender differences in emotion. This is an important endeavour considering that emotion has been described as the key component in personality and vulnerability factors governing risk for psychopathology (Davidson, 2002). With regards to the disorders of emotion, it is known that the lifetime risk for depression is 10–25% for women but only 5–12% for men (American Psychiatric Association, 1994). A more recent survey based on the ICD-10 classification found 6% of adults to suffer from depressive disorders and that twice as many females as males experience depression (Australian Bureau of Statistics, 1997). Differences in biology as well as gender-related environmental experiences are regarded as the key to understanding these gender differences in depression (Kessler, 2003).

‘Emotion’ may be defined as a relatively brief episode of synchronised response involving multiple components including cognitive processes, physiological responses, motivation changes, motor expression and subjective feeling Borod, 1993, Ekman, 1984, Ekman, 1992, Lang, 1968, Lang, 1984, Scherer and Peper, 2001. By contrast, ‘mood’ is generally considered to be a more diffuse state, characterised by low intensity but relatively long duration (lasting hours to days) Ekman, 1992, Ketter et al., 2003, Scherer and Peper, 2001. Although, these terms relate to different behavioural constructs, it is possible that chronic or repeated activation of certain underlying neurophysiological mechanisms may be the connection between emotional experience and mood disorders such as depression and anxiety. For example, theories have been proposed which describe certain neurophysiological processes as they relate to longer-lasting affective phenomena such as depressed and anxious mood (e.g. Heller, 1993). Furthermore, brain activation resulting from the use of certain mood induction techniques in healthy participants is regarded as similar to that seen in mood disorders such as depression (see Lawrence and Grasby, 2001, for discussion).

A limited but growing number of studies have investigated whether gender differences in brain activation exist on tasks designed to assess a broad range of emotional processes. These studies are important to enable researchers to move beyond employment of behavioural methodologies which have been criticised for their inability to illuminate processes inaccessible to consciousness (e.g. Davidson et al., 2003). Studies that have investigated emotional perception have reported either no gender differences (Meyers and Smith, 1986), subtle differences between males and females Morita et al., 2001, Wildgruber et al., 2002, or sex-specific areas of brain activation Killgore and Yurgelun-Todd, 2001, Lee et al., 2002. Tasks that involve more the experience of emotion (e.g. Del Parigi et al., 2002, George et al., 1996, Pardo et al., 1993, Pendergrass et al., 2003, Schneider et al., 2000) have reported more consistent gender differences. Healthy women have been shown to display more activity (i.e. larger number and more widespread significant differences between transient induced negative mood states and baseline) than healthy men in anterior limbic structures such as the inferior frontal, orbital and prefrontal cortices, during transient induced sadness (e.g. George et al., 1996 and Pardo et al., 1993). These studies have also demonstrated that women show more bilateral activation without asymmetries during induced sadness. For example, in a female-only study, increases in activity were reported within the thalamus and medial prefrontal using both film as well as recall-induced emotional states (Lane et al., 1997a). Pardo et al. (1993) demonstrated left-sided activation of inferior frontal and orbitofrontal cortices in males, whilst bilateral activation of these areas was reported in females. In addition, sadness has been associated with amygdala activation in males but not females (Schneider et al., 2000). The authors suggested that females produce less concentrated and less lateralised brain activation than males. Bilateral findings in females are consistent with a widely held neuropsychological theory on the organisation of the brain, which posits that females are more bilateralised than men Iaccino, 1993, Levy and Heller, 1992, McGlone, 1986. Whilst these studies examining emotional experience have shown gender differences, inconsistent differences have been reported. For example, George et al. (1996) report that women activate a greater portion of their limbic system than men during transient sadness, whilst Schneider et al. (2000) report that processing of sadness is more focal and subcortical in men. The literature focusing on transient happiness has also been inconsistent. For example, decreases as well as increases in activity have been reported for happiness (see George et al., 1995 and Lane et al., 1997a, respectively). Gender differences in transient happiness however may be more subtle. This is supported by previous studies which report either slight or no differences for happiness (George et al., 1996 and Schneider et al., 2000, respectively).

It should be noted however that many problems arise when attempting to compare studies that have investigated gender differences in emotion. First, brain imaging studies have used a variety of different paradigms. These paradigms have included recollection of sad events (Pardo et al., 1993), perception and experience of human emotional nonverbal sounds Meyers and Smith, 1986, Smith et al., 1995, recollection of affect-specific events (George et al., 1996), viewing of faces with either happy or sad facial expressions to aid mood induction (Schneider et al., 2000), the recognition of facial affect Kesler-West et al., 2001, Killgore and Yurgelun-Todd, 2001, Lee et al., 2002, Morita et al., 2001, the processing of emotionally evocative images Canli et al., 2002, Pendergrass et al., 2003, the detection of emotional intonation (Wildgruber et al., 2002), and the experience of hunger and satiation (Del Parigi et al., 2002). Second, there are a large number of different neuroimaging techniques used, which range from PET Del Parigi et al., 2002, George et al., 1996, Pardo et al., 1993, fMRI Canli et al., 2002, Kesler-West et al., 2001, Lee et al., 2002, Killgore and Yurgelun-Todd, 2001, Pendergrass et al., 2003, Schneider et al., 2000, Wildgruber et al., 2002 and different electroencephalographic techniques Meyers and Smith, 1986, Morita et al., 2001, Smith et al., 1995.

The International Affective Picture System (IAPS) (Lang et al., 1999) has become increasingly used amongst brain imaging studies to investigate emotional processes as it allows for systematic selection of images that range in emotional content. Specifically, these images are associated with standardised ratings for valence and arousal which allows researchers to easily replicate published findings for a specific selection of images and also aid interpretation of and allow conclusions to be drawn from multiple studies using this task. Previous studies using the IAPS have investigated emotional processing with haemodynamic imaging techniques such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) (e.g. Canli et al., 1998, Canli et al., 2002, Lane et al., 1997b, Lane et al., 1997c, Lang et al., 1998, Paradiso et al., 1999, Pendergrass et al., 2003, Taylor et al., 1998, Wrase et al., 2003), electroencephalographic-based techniques (e.g. Aftanas et al., 2001a, Aftanas et al., 2001b, Aftanas et al., 2002, Junghofer et al., 2001, Kawasaki et al., 2001, Kemp et al., 2002, Mini et al., 1996, Palomba et al., 1997, Schupp et al., 2000, Schupp et al., 2003) as well as magnetoencephalography Northoff et al., 2000, Northoff et al., 2002.

However, few of these studies have examined gender differences Canli et al., 2002, Pendergrass et al., 2003, Wrase et al., 2003. These studies suggest gender differences in several neural structures including the insular, prefrontal and parietal cortices, bilateral visual processing areas, thalamic nuclei, amygdala, caudate, putamen and pons regions, and the postcentral and parahippocampal gyri during the processing of visual emotional stimuli. By contrast, a recent behavioural study that examined gender differences in IAPS images in terms of valence and arousal ratings, facial EMG, skin response and heart rate suggests that ‘remarkable congruence’ was displayed in the physiological profile between the two genders when viewing images having less arousing appetitive and defensive contexts (Bradley et al., 2001). In addition, Wrase et al. (2003) have recently reported that although no significant differences were found between males or females in valence, arousal, skin conductance response and startle modulation, men displayed stronger brain activity for positive visual stimuli in the inferior and medial frontal gyrus, whilst women displayed stronger brain activity for negative visual stimuli in the anterior and medial cingulate gyrus. These findings suggest that although males and females may not differ in terms of behavioural and peripheral physiological measures of emotional responsivity, the two genders may well differ in neurophysiology.

The present study focuses on aspects of emotion that relate to the processing of emotional stimuli or emotional processing. Emotional processing may be defined as the perception and evaluation of emotional stimuli which may or may not involve emotional experience. For example, emotional processing may involve recognition of emotional facial expressions (emotional perception), recollection of an emotional event (emotional experience), or the viewing of emotional film or images (emotional perception and experience). Note however, that such categorisations are a simplification as studies have clearly demonstrated the presence of autonomic arousal during tasks involving recognition of emotional facial expressions (e.g. Williams et al., 2001). Although the present study involves presentation of images rated low on the dimension of arousal, these pictures do appear to involve aspects of emotional experience, such as alterations in heart rate (Kemp and Nathan, in press).

It has been suggested that techniques with a superior temporal resolution may better address gender differences in emotional processing (e.g. Schneider et al., 2000). Event-related potential techniques however are unable to elucidate time-extended processes following stimulus presentation (Silberstein et al., 1990). Two other techniques, magnetoencephalography (MEG) and steady-state probe topography (SSPT) provide such information; however, relatively few studies using these techniques have investigated how the brain differentially responds to emotional stimuli over time. In the current study, SSPT was used to investigate gender differences during the viewing of emotional stimuli selected from the IAPS. SSPT may be characterised by three features which include (1) the presentation of a rapid and repetitive visual flicker distinct from and irrelevant to the cognitive task undertaken by the participants, (2) the recording of brain electrical activity from 64 scalp-electrode sites within the area defined by the International 10-20 system and (3) a relatively short integration period which enables the rapid changes in brain electrical activity as well as the time-extended processes following stimulus presentation to be tracked Gray et al., 2003, Kemp et al., 2002, Silberstein et al., 1990. We have previously shown that transient widespread and bilateral frontal SSVEP latency and occipital amplitude reductions are associated with the cortical processing of pleasant and unpleasant emotional stimuli in a mixed-gender sample (Kemp et al., 2002). The aim of the current study was to investigate how cortical steady-state visually evoked potentials (SSVEPs) recorded using the SSPT technique are modulated by pleasant and unpleasant images (relative to neutral images) in a larger sample size, and to investigate whether this processing differs between males and females. Based on the extant literature reviewed above, we hypothesise (1) that males and females will not differ in subjective verbal report, (2) that females will display bilateral frontal latency reductions during the processing of both unpleasant and pleasant images relative to neutral images, and (3) that males will display more focal changes.

Section snippets

Participants

Thirty healthy participants (mean age 23.00 ± 4.21 years), consisting of 15 males (mean age 23.73 ± 5.04 years) and 15 females (mean age 22.27 ± 3.20 years), were included in the current study. All participants were right handed as assessed by the Edinburgh Inventory (Oldfield, 1971), nonsmokers, drug-free, and had no history of epilepsy, head injury, stroke, psychiatric disorders, neurological conditions or alcoholism. A medical examination was conducted by a physician who, from physical- and

Behavioural results

A series of independent-samples t tests were conducted on age, education and each of the POMS subscales separately to determine whether any differences exist between males and females. None of these variables were found to significantly differ between males and females (P > 0.05). Means (M), standard deviations (SD) and range are provided for age, years of education and all six POMS subscales for males and females (grouped as well as separated by gender) in Table 1.

Participants rated each image

Discussion

The current study investigated the spatiotemporal characteristics of the SSVEP associated with the processing of low arousal, unpleasant and pleasant images relative to neutral images in males and females using the SSPT technique. SSVEP results support our previous study (Kemp et al., 2002) which reports that processing of emotional valence (pleasant and unpleasant) is associated with frontal SSVEP latency and occipital amplitude reductions; however, substantial gender differences exist

Acknowledgements

The authors would like to thank Cindy Van Roy for assistance in data analysis as well as Jim Thompson and Peter Line for help with computer programming.

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