The valence-specific laterality effect in free viewing conditions: The influence of sex, handedness,...

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The valence-specific laterality effect in free viewing conditions: The influence of sex, handedness, and response bias Paul Rodway, * Lynn Wright, and Scott Hardie Division of Psychology, University of Abertay Dundee, Bell Street, Dundee DD1 1HG, UK Accepted 16 September 2003 Abstract The right hemisphere has often been viewed as having a dominant role in the processing of emotional information. Other evi- dence indicates that both hemispheres process emotional information but their involvement is valence specific, with the right hemisphere dealing with negative emotions and the left hemisphere preferentially processing positive emotions. This has been found under both restricted (Reuter-Lorenz & Davidson, 1981) and free viewing conditions (Jansari, Tranel, & Adolphs, 2000). It remains unclear whether the valence-specific laterality effect is also sex specific or is influenced by the handedness of participants. To explore this issue we repeated Jansari et al.Õs free-viewing laterality task with 78 participants. We found a valence-specific laterality effect in women but not men, with women discriminating negative emotional expressions more accurately when the face was presented on the left-hand side and discriminating positive emotions more accurately when those faces were presented on the right-hand side. These results indicate that under free viewing conditions women are more lateralised for the processing of facial emotion than are men. Handedness did not affect the lateralised processing of facial emotion. Finally, participants demonstrated a response bias on control trials, where facial emotion did not differ between the faces. Participants selected the left-hand side more frequently when they believed the expression was negative and the right-hand side more frequently when they believed the expression was positive. This response bias can cause a spurious valence-specific laterality effect which might have contributed to the conflicting findings within the literature. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Hemisphere; Valence; Laterality; Response bias; Handedness; Sex 1. Introduction Many studies have suggested that the right hemi- sphere (RH) of the brain has a greater role in the pro- cessing of emotional information than the left hemisphere (Christman & Hackworth, 1993; Levy, Heller, Banich, & Burton, 1983; Ley & Bryden, 1979). This research has used both brain-damaged and healthy participants and has examined the role of the RH in both the perception and expression of affect. For ex- ample, RH-damaged patients are more impaired than LH-damaged patients at recognising emotions conveyed by facial expressions (Adolphs, Damasio, Tranel, & Damasio, 1996). In addition, it is believed that emotions are expressed more intensely on the left side of the face because the RH has a greater role in the control of emotional expression (Heller & Levy, 1981; Kowner, 1995; Sackeim, Gur, & Saucy, 1978). With healthy participants the majority of studies in this area have used the divided visual field technique to present faces with different emotional expressions. In accord with the findings from patient studies it has been found that there is a RH advantage (left visual field, LVF) in the perception and interpretation of emotional expressions (Ley & Bryden, 1979; Mandal & Singh, 1990; Stauss & Moscovitch, 1981). The view, however, that the RH is preferentially involved in the processing of all emotional information has been questioned on a number of occasions. Many studies have suggested that hemispheric biases in the processing of emotional in- formation may depend on the valence of the emotion conveyed by that information (Ahern & Schwartz, 1979, * Corresponding author. Fax: +44-1382-223121. E-mail address: [email protected] (P. Rodway). 0278-2626/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S0278-2626(03)00217-3 Brain and Cognition 53 (2003) 452–463 www.elsevier.com/locate/b&c

Transcript of The valence-specific laterality effect in free viewing conditions: The influence of sex, handedness,...

Brain and Cognition 53 (2003) 452–463

www.elsevier.com/locate/b&c

The valence-specific laterality effect in free viewing conditions:The influence of sex, handedness, and response bias

Paul Rodway,* Lynn Wright, and Scott Hardie

Division of Psychology, University of Abertay Dundee, Bell Street, Dundee DD1 1HG, UK

Accepted 16 September 2003

Abstract

The right hemisphere has often been viewed as having a dominant role in the processing of emotional information. Other evi-

dence indicates that both hemispheres process emotional information but their involvement is valence specific, with the right

hemisphere dealing with negative emotions and the left hemisphere preferentially processing positive emotions. This has been found

under both restricted (Reuter-Lorenz & Davidson, 1981) and free viewing conditions (Jansari, Tranel, & Adolphs, 2000). It remains

unclear whether the valence-specific laterality effect is also sex specific or is influenced by the handedness of participants. To explore

this issue we repeated Jansari et al.�s free-viewing laterality task with 78 participants. We found a valence-specific laterality effect in

women but not men, with women discriminating negative emotional expressions more accurately when the face was presented on the

left-hand side and discriminating positive emotions more accurately when those faces were presented on the right-hand side. These

results indicate that under free viewing conditions women are more lateralised for the processing of facial emotion than are men.

Handedness did not affect the lateralised processing of facial emotion. Finally, participants demonstrated a response bias on control

trials, where facial emotion did not differ between the faces. Participants selected the left-hand side more frequently when they

believed the expression was negative and the right-hand side more frequently when they believed the expression was positive. This

response bias can cause a spurious valence-specific laterality effect which might have contributed to the conflicting findings within

the literature.

� 2003 Elsevier Inc. All rights reserved.

Keywords: Hemisphere; Valence; Laterality; Response bias; Handedness; Sex

1. Introduction

Many studies have suggested that the right hemi-sphere (RH) of the brain has a greater role in the pro-

cessing of emotional information than the left

hemisphere (Christman & Hackworth, 1993; Levy,

Heller, Banich, & Burton, 1983; Ley & Bryden, 1979).

This research has used both brain-damaged and healthy

participants and has examined the role of the RH in

both the perception and expression of affect. For ex-

ample, RH-damaged patients are more impaired thanLH-damaged patients at recognising emotions conveyed

by facial expressions (Adolphs, Damasio, Tranel, &

Damasio, 1996). In addition, it is believed that emotions

* Corresponding author. Fax: +44-1382-223121.

E-mail address: [email protected] (P. Rodway).

0278-2626/$ - see front matter � 2003 Elsevier Inc. All rights reserved.

doi:10.1016/S0278-2626(03)00217-3

are expressed more intensely on the left side of the face

because the RH has a greater role in the control of

emotional expression (Heller & Levy, 1981; Kowner,1995; Sackeim, Gur, & Saucy, 1978).

With healthy participants the majority of studies in

this area have used the divided visual field technique to

present faces with different emotional expressions. In

accord with the findings from patient studies it has been

found that there is a RH advantage (left visual field,

LVF) in the perception and interpretation of emotional

expressions (Ley & Bryden, 1979; Mandal & Singh,1990; Stauss & Moscovitch, 1981). The view, however,

that the RH is preferentially involved in the processing

of all emotional information has been questioned on a

number of occasions. Many studies have suggested that

hemispheric biases in the processing of emotional in-

formation may depend on the valence of the emotion

conveyed by that information (Ahern & Schwartz, 1979,

P. Rodway et al. / Brain and Cognition 53 (2003) 452–463 453

1985; Davidson, 1992; Reuter-Lorenz & Davidson,1981; Tucker, 1981). For example, Reuter-Lorenz and

Davidson (1981) found that when happy faces were

presented to the LH they were perceived more quickly

compared with sad faces. Conversely sad faces presented

to the RH were perceived faster than happy faces. They

concluded that there was a valence-specific laterality

effect, with a LH advantage for the perception of posi-

tive emotions and a RH advantage for the perception ofnegative emotions. Evidence in support of the valence

hypothesis has been obtained from a range of other

measures (Davidson, 1992, 1993a, 1993b) including the

expression of facial affect, with the LH showing a

greater involvement in the expression of positive emo-

tions (Ross, Homan, & Buck, 1994), and the experience

of emotions induced by films, with activation of anterior

regions of each hemisphere being specific to the valenceof the emotion experienced (Jones & Fox, 1992).

The validity of the valence hypothesis, however,

continues to be a source of debate within the literature

(Borod, Zgaljardic, Tabert, & Koff, 2001). Several early

studies produced findings consistent with the right-

hemisphere hypothesis rather than the valence hypoth-

esis. For example, Ley and Bryden (1982), using a

dichotic listening task, obtained a left ear advantage(RH) when participants were required to detect the af-

fective tone of spoken sentences, regardless of whether

the sentences had been spoken in a happy, sad, angry, or

neutral tone of voice. Some studies have also suggested

that both hemispheres are involved in the processing of

positive emotions whereas the processing of negative

emotions is lateralised in the RH (Asthana & Mandal,

2001; Mandal, Tandon, & Asthana, 1991). Moreover, arecent review of the literature (Borod et al., 2001) found

little evidence for the valence-specific effect in facial

emotion perception. Of the 20 studies reviewed, only one

produced results consistent with the valence hypothesis

and this was in women but not men (Burton & Levy,

1989). Of the 19 remaining studies, 17 produced results

consistent with the right-hemisphere hypothesis and two

showed no laterality effects.It is important to note that two versions of the va-

lence hypothesis have been proposed (Borod et al.,

2001). One version suggests that the RH is specialised

for negative emotions whereas the LH is specialised for

positive emotions (e.g., Silberman & Weingartner,

1986). A second version makes the important distinction

between the perception of an emotion and the experi-

ence of an emotion (Davidson, 1984). According to thistheory the RH is dominant for the perception of both

positive and negative emotions, but for emotional ex-

perience the RH is specialised for negative emotions and

the LH for positive emotions. In accord with this view,

Borod (1993) has proposed that posterior regions of the

RH are specialised for the perceptual identification of an

emotion regardless of the valence of the emotion.

However, for emotional experience, it is suggested thatanterior regions of the LH are preferentially involved in

the experience of positive emotions whereas anterior

regions of the RH are involved in the experience of

negative emotions (Borod, 1993; Davidson, 1993a,

1993b).

If valence-specific hemispheric asymmetries are pres-

ent for emotional experience then valence effects may

only emerge in tasks which cause participants to expe-rience an emotion. The idea that valence effects may be

dependent on the task used was suggested by Ley and

Strauss (1986) who concluded from their review of the

literature that evidence for the RH hypothesis came

from tasks involving the rapid classification of emotions

(e.g., Ley & Bryden, 1979; Suberi & McKeever, 1977)

whereas evidence in favour of the valence-specific hy-

pothesis came from studies where different stimuli werecompared for affect (e.g., Reuter-Lorenz & Davidson,

1981; Reuter-Lorenz, Givis, & Moscovitch, 1983).

van Strien and van Beek (2000) made the same point

and suggested that studies which have required partici-

pants to match emotional expressions of faces (e.g., Ley

& Bryden, 1979) may show a RH advantage because

these predominantly perceptual tasks are carried out by

posterior regions of the RH. However, for tasks whichrequire an evaluation of the intensity of an emotional

expression, either directly (e.g., Davidson, Mednick,

Moss, Saron, & Schaffer, 1987), or when identifying one

face to be more expressive than another (e.g., Reuter-

Lorenz & Davidson, 1981), then anterior regions of each

hemisphere, involved in emotional experience, may be

utilised. It is possible that participants, when evaluating

subtle differences in the intensity of emotional expres-sions, use their own affective responses to facial ex-

pressions to aid them in reaching a decision (Jansari et

al., 2000). This is plausible as it has been found that

viewing an emotionally expressive face can elicit an ex-

perience of that emotion in the perceiver (Wild, Erb, &

Bartels, 2001). Moreover, this may be one of the ways in

which we decode the expressions of other people

(Adolphs, 2002; Wild et al., 2001). If the perception offacial affect causes participants to experience the emo-

tion expressed in the face, anterior regions of each

hemisphere will be utilised, resulting in the emergence of

valence-specific laterality effects (van Strien & van Beek,

2000).

If this account is correct then tasks involving a quick

perceptual identification of facial affect are unlikely to

produce valence-specific effects (van Strien & van Beek,2000). However, if a task requires subtle gradations in

emotional expression to be compared, perhaps causing

participants to rely on the recruitment of their own af-

fective responses to reach a decision (Jansari et al.,

2000), then a valence-specific effect may be present.

Partial support for this suggestion comes from a study

conducted by Safer (1981) who found a LVF superiority

454 P. Rodway et al. / Brain and Cognition 53 (2003) 452–463

when participants had to judge whether two facialemotions were the same or not. Prior to making the

judgement, in one condition participants were instructed

to think of a brief one or two-word label description of

the expression, and in a second condition they were in-

structed to ‘‘empathize fully with the person in the slide,

as if [they] were that person. . .’’ Importantly the in-

struction to empathise with the expressed emotion in-

creased the RH advantage. This suggests that thelateralised perception of facial affect can change within

the same task if emotional experience is recruited during

the task.

It certainly seems to be the case that studies which

have used tasks which require faces to be compared for

affect are more likely to obtain valence-specific effects

(Ley & Strauss, 1986). One such study by Jansari et al.

(2000) provides further support for the valence-specifichypothesis. This experiment differed from previous work

in that it examined laterality effects for emotional pro-

cessing under free-viewing conditions. Thus, rather than

the faces being presented very briefly the participants

were able to examine the faces for as long as it took

them to respond. The task was similar to that employed

by Reuter-Lorenz and Davidson (1981), and consisted

of presenting participants with two versions of the samemale face, one of which displayed an emotion and one of

which displayed a neutral expression. The faces were

morphed so that differences in expression between the

two faces ranged from very subtle to clear and they were

presented on either side of a computer screen. In support

of the valence hypothesis Jansari et al. (2000) found

more accurate discrimination of faces with positive

emotional expressions when they were presented on theright-hand side than when they were presented on the

left-hand side. Conversely, greater accuracy in discrim-

ination was found for faces with negative expressions

when they were presented on the left-hand side rather

than the right-hand side. These findings suggest that

laterality effects in emotional processing are valence-

specific and that they are present under free-viewing

conditions.It is also possible that evidence in support of the

valence hypothesis has been inconsistent because most

studies have ignored the influence of the participant�sgender. The majority of research which has examined

differences in brain lateralisation between men and wo-

men has indicated that lateralisation of certain types of

processing is more pronounced in men than in women.

It appears that in men there is a RH advantage for non-verbal tasks and a LH advantage for verbal tasks,

whereas women show less clear laterality effects on these

tasks (Davidson, Cave, & Sellner, 2000; Hausmann &

Gunturkun, 1999; Hellige, 1993; Iaccino, 1993; Inglis &

Lawson, 1981).

Given that sex differences in lateralisation exist it is

possible that hemispheric functioning differs between

men and women for the processing of emotional stimuli(Eviatar, Hellige, & Zaidel, 1997; Sanz-Martin & Loyo,

2001). For example, Ladavas, Umilt�aa, and Ricci-Bitti

(1980) found that women showed a LVF superiority in

discriminating emotions whereas men showed no con-

sistent asymmetries in emotional discrimination. In ad-

dition, Burton and Levy (1989) found that women, but

not men, perceived faces with negative emotions fastest

when presented in the LVF and faces with positiveemotions fastest when presented to the RVF. These re-

sults indicate that women are more lateralised for the

perception of emotion than are men.

Findings by van Strien and van Beek (2000) support

this view. They examined the influence of sex and

handedness on ratings of emotion in laterally presented

cartoon faces. On each trial a face was presented briefly

(150ms) to the left or right visual field and participantswere required to rate the intensity of the emotion ex-

pressed by the face. They found no effect of handedness

but found that sex influenced ratings of emotion, with

women rating neutral and mildly positive faces as more

positive when they were presented in the RVF compared

to when they were presented in the LVF. For the men

the visual field did not affect how they rated the faces.

These results, and those of Burton and Levy (1989),suggest that the valence hypothesis may depend upon

the sex of the subject, with only women showing the

valence-specific laterality effect. It is also possible that

some of the conflicting results within the literature may

have been caused by gender differences in emotional

processing which went undetected because the effect of

sex was not examined (e.g., Reuter-Lorenz & Davidson,

1981).It should be noted, however, that reviews of the lit-

erature have found little evidence for sex differences in

asymmetries of facial expression of emotion (Borod,

Koff, Yecker, Santschi, & Schmidt, 1998) or the per-

ception of facial affect (Borod et al., 2001). Moreover,

van Strien and van Beek�s results conflict with those of

Jansari et al. (2000) who found the valence-specific lat-

erality effect in both male and female participants. Thus,the issue of whether the valence-specific laterality effect

is sex specific is unresolved. One of the purposes of the

present study was to determine whether the valence-

specific effect applies only to female participants, when

completing the same free-viewing task as used by Jansari

et al. (2000), or is limited to restricted viewing condi-

tions.

A further factor which may influence asymmetries inemotional processing is the handedness of participants.

Differences in cortical organisation and processing be-

tween left- and right-handers have been reported and it

is conceivable that these differences influence the later-

alisation of emotional processing (Everhart, Harrison, &

Crews, 1996). Many studies have avoided the handed-

ness issue by selecting only right-handed participants.

P. Rodway et al. / Brain and Cognition 53 (2003) 452–463 455

While findings have been inconsistent, there is someevidence to suggest that right- and left-handers may

have different asymmetries for emotional processing.

For example, Reuter-Lorenz et al. (1983) found that

left-handers who did not show an inverted handwriting

posture had an opposite pattern of valence asymmetry

from right-handers and inverted left-handers. In addi-

tion, Everhart et al. (1996) showed that left-handers had

a RVF bias for rating neutral expressions more nega-tively. This suggests that the processing of negative

emotions is more strongly lateralised in the LH for left-

handers. In contrast, however, van Strien and van Beek

(2000) found no influence of handedness on the rating of

emotional expressions as conveyed by cartoon faces.

Thus, it is unclear whether handedness influences

asymmetries in emotional processing. Moreover, it is

likely that there are complex interactions betweenhandedness, sex, and cortical organisation (Eviatar

et al., 1997) which may only be clarified when these

factors are studied in relation to one another.

To summarise, while some results indicate that the

RH is predominantly involved in the processing of all

emotions (Borod et al., 2001; Ley & Bryden, 1979),

other evidence suggests that each hemisphere has a bias

for processing emotions of a particular valence (Da-vidson, 1992, 1993a, 1993b; Jansari et al., 2000; Reuter-

Lorenz & Davidson, 1981; van Strien & van Beek, 2000).

It is also possible that there is a valence-specific laterality

effect for women but not men (Burton & Levy, 1989; van

Strien & van Beek, 2000), with women preferentially

using the RH to process negative emotions and the LH

to process positive emotions. Finally, the effect of

handedness on the lateralised processing of emotionalexpressions has produced inconsistent findings, with

some studies reporting an effect (Everhart et al., 1996;

Reuter-Lorenz et al., 1983) and others reporting no ef-

fect (van Strien & van Beek, 2000).

In view of the contradictory findings within the lit-

erature the aim of the present study was to extend pre-

vious work and examine the effects of sex and

handedness on the lateralised processing of emotionalexpressions. A primary purpose of the study was to

determine whether the valence-specific laterality effect

applies to both men and women in free viewing condi-

tions using the task employed by Jansari et al. In addi-

tion, the influence of handedness on emotional

processing was examined.

In accord with van Strien and van Beek�s results it

was predicted that valence-specific effects would be re-stricted to female participants but not men. Moreover if

valence effects emerge when a task requires subtle dif-

ferences in emotional expression to be compared (van

Strien & van Beek, 2000) then valence-specific effects

may be largest when the discrimination of emotional

expression is most difficult. As the effect of handedness

on lateralised emotional processing has proved to be

inconsistent we made no clear predictions regarding thisfactor.

2. Method

2.1. Participants

Seventy-eight participants were used in this study.Thirty-five were right-handed (17 men and 18 women)

and 43 were left-handed (19 men and 24 women). All

participants were staff and students of the University of

Abertay Dundee. All had normal colour vision and

normal or corrected-to-normal visual acuity.

2.2. Hand preference

Hand preference was measured by a 27 item hand-

edness questionnaire which consisted of 25 questions

taken from Peters� (1998) handedness inventory and a

further two questions which enabled the inclusion of all

of the items used in the Edinburgh (Oldfield, 1971) and

Annett (1970) handedness questionnaires. The items

concerned the following activities: drawing, using a

knife, combing hair, picking up small objects, throwinga ball, striking a match. Each question had five choices:

right hand always, right hand most of the time, either

hand, left hand most of the time and left hand always,

which were scored, 2, 1, 0, )1, )2, respectively. Only

participants with a strong hand preference were used in

the study: mean left-handed score ()24.79, SD¼ 12.7),

and mean right-handed score (37.95, SD¼ 11.31).

2.3. Discrimination task

2.3.1. Stimuli

Ekman and Freisen�s (1976) pictures of facial affect

were used as stimuli. The same male face (J.J.) was used

for the neutral expression and for the expression of six

emotions, two of which were positive (happiness, sur-

prise) and four were negative (fear, sadness, disgust, andanger). Surprise was treated as a positive expression for

three reasons. First, we wished to replicate and extend

the findings of Jansari et al.�s study and therefore de-

cided that it was important to use the same expressions.

Second, facial expressions of surprise tend to be rated as

more pleasant than unpleasant (Adolphs, Russell, &

Tranel, 1999), although this rating does not differ sig-

nificantly from that given to neutral expressions. Thus,the expression of surprise possesses a marginally posi-

tive, or neutral, valence. In accord with this view, some

studies using posed expressions have included �pleasantsurprise� as an expression of positive valence (Christman

& Hackworth, 1993; Workman, Peters, & Taylor, 2000).

Third, as the alternative to using �surprise� is to restrict

positive valence to happy expressions, and negative

456 P. Rodway et al. / Brain and Cognition 53 (2003) 452–463

valence to one or two negative expressions, the test ofthe valence hypothesis then becomes limited to a small

set of emotions. As we believe that the valence hy-

pothesis applies to a range of positive and negative

emotions, rather than a restricted set, the expression of

surprise was included.

In replication of Jansari et al., the Morph 2.5 soft-

ware (Gryphon Software, 1997) was used to create the

stimuli by morphing the neutral face with the emotionalface. The morphing procedure consisted of identifying

corresponding features on both faces. The morphing

algorithm then consisted of spatially transforming one

image into another and averaging the luminance values

of both images. For each of the six emotional expres-

sions five different levels of morphing were used (5, 10,

15, 20, and 25%). For example, the happy expression

was morphed at 5% with the neutral expression, so 5%of the morph was the happy expression and 95% was the

neutral expression. At this level of morphing the ex-

pression was extremely subtle, showing a very faint

emotion (see Fig. 1). The 5 morphs for each of the 6

emotional expressions gave a set of 30 morphed faces.

Fig. 1. Examples of stimuli. (A) Neutral face on the left and happy face

on the right at the 5% morph level. (B) Neutral face on the left and

happy face on the right at the 25% morph level.

2.4. Procedure

A Compaq laptop computer with a coloured screen

and standard keyboard was used to present the face

stimuli and measure accuracy. The software used for

creating and running the experiment was Superlab Pro

v1.2 for Windows.

For each trial participants were presented with two

faces. The faces were presented side by side, each facewas 16 cm� 11 cm and the participants sat approxi-

mately 40 cm from the screen. On the screen, directly

above the mid-point between the two faces, a label in-

dicating one of the six emotions was presented simul-

taneously with the faces. The participants were

instructed to select the face which best depicted the

emotion corresponding to the emotion label. They were

instructed to press �Z� if they thought the emotion facewas on the left, and press �M� if they thought it was on

the right. The faces were presented until participants

made a response, after which the stimuli were removed

from the screen and a mask was presented for 700ms

until the next trial began. Participants were given six

practice trials prior to completing the experimental tri-

als.

There were 72 experimental trials. For 60 trials one ofthe two faces was a neutral face and the other face was

an emotion morph expressing the same emotion as the

emotion label. To counterbalance the side of presenta-

tion, each one of the 30 morphs was shown twice, once

to the left of the neutral face and once to the right of the

neutral face. A further 12 control trials were also in-

cluded to determine whether there was a response bias in

participants, with them preferentially selecting the rightor left side. These trials consisted of presenting two

identical neutral faces with an emotion label. Even

though the faces did not differ the participants were

required to select the face which they thought best de-

picted the emotion label. Each of the emotion labels was

presented twice. The order of presentation of the 72

trials was randomised. After completing the discrimi-

nation task the participants completed the handednessquestionnaire. The whole session took approximately

15min.

3. Results

A 2� 2� 2� 2� 5 [sex (male vs. female) handedness

(left vs. right) side (left vs. right) valence (positive vs.negative) morphing (5, 10, 15, 20, 25%)] mixed-model

ANOVA was conducted on the mean accuracy data. Sex

and handedness were between-subject factors and side,

valence, and morphing were within-subject factors.

Analyses revealed a significant main effect of valence,

F ð1; 74Þ ¼ 79:66, p < :0001, with participants more ac-

curately classifying positive emotions (mean¼ 77%)

P. Rodway et al. / Brain and Cognition 53 (2003) 452–463 457

compared to negative emotions (mean¼ 61%). As ex-pected there was also a main effect of morphing,

F ð4; 296Þ ¼ 40:43, p < :00001, reflecting greater accu-

racy in detecting emotions as the emotional expression

became stronger (see Table 1). There was also a signif-

icant two-way interaction between morphing and group

F ð4; 296Þ ¼ 4:37, p < :0020. This was due to the women

being significantly less accurate than the men at the 5%

morph level F ð1; 74Þ ¼ 10:40, p < :0019, (women 53%,men 64%), but being as accurate as the men at the 10,

15, 20, and 25% morph levels (p > :05) (Table 2).

The main effects of handedness, sex, and side, failed

to reach significance (all F �s < 1). However, there was a

significant two-way interaction between side and va-

lence, F ð1; 74Þ ¼ 8:17, p < :0055, which was qualified by

a significant three-way interaction between side, valence,

and sex, F ð1; 74Þ ¼ 7:67, p < :0071. This three-way in-teraction was examined by conducting two further

ANOVAs, one for the male participants and one for

female participants. Analysis of the performance of the

women showed a significant effect of valence,

F ð1; 40Þ ¼ 55, p < :0001, reflecting greater accuracy for

detecting positive emotional expressions (mean¼ 76%)

compared with negative emotions (mean¼ 61%). In

addition, for the female participants, there was a sig-nificant side� valence interaction, F ð1; 40Þ ¼ 15:44,p < :0003, which was examined further by conducting

two additional ANOVAs, one for negative emotions and

able 2

he mean accuracy (percentage) scores for each condition collapsed across levels of morphing

Left handed Right handed

Female Male Female Male

Positive left 74 (19) 77 (13) 69 (13) 77 (16)

Positive right 85 (15) 73 (24) 78 (22) 85 (13)

Negative left 65 (14) 61 (20) 66 (19) 62 (13)

Negative right 55 (17) 61 (20) 56 (15) 66 (13)

Standard deviations are in parentheses.

Table 1

The mean accuracy scores (percentage) and standard deviations (SD) for each condition at each of the five levels of morphing

Left handed Right handed

Female Male Female Male

Positive left 45, 70, 77, 85, 91 68, 71, 84, 81, 79 55, 69, 67, 69, 86 71, 62, 82, 76, 94

SD 41, 32, 36, 27, 19 29, 25, 23, 24, 30 33, 30, 34, 34, 23 35, 33, 24, 25, 16

Positive right 77, 79, 85, 89, 96 66, 71, 79, 74, 79 58, 78, 78, 88, 91 82, 76, 82, 88, 97

SD 29, 25, 23, 25, 14 29, 34, 30, 30, 34 35, 35, 35, 27, 25 24, 39, 24, 21, 12

Negative left 53, 64, 64, 68, 76 59, 58, 53, 66, 71 58, 68, 65, 71, 75 48, 51, 72, 62, 76

SD 27, 19, 27, 24, 26 17, 31, 27, 26, 33 24, 28, 27, 31, 30 28, 27, 21, 23, 16

Negative right 37, 46, 54, 67, 76 61, 45, 62, 67, 71 42, 42, 53, 60, 80 59, 53, 65, 73, 82

SD 23, 28, 30, 27, 21 29, 31, 30, 28, 27 28, 29, 34, 27, 18 23, 24, 23, 20, 17

Mean 53, 65, 70, 77, 85 63, 61, 69, 72, 75 53, 64, 66, 72, 83 65, 61, 75, 74, 87

T

T

one for positive emotions. The analysis of negativeemotions in the female participants revealed a significant

effect of side, F ð1; 40Þ ¼ 10:66, p < :0022, demonstrat-

ing that women were significantly more accurate at de-

tecting negative emotions when they were presented on

the left side (mean¼ 65%) compared to when they were

presented on the right side (mean¼ 55%). Similarly, for

positive emotions the female participants also showed a

significant effect of side, F ð1; 40Þ ¼ 5:92, p < :019, re-flecting greater accuracy at detecting positive expres-

sions presented on the right side (mean¼ 82%)

compared to the left side (mean¼ 72%). These two

comparisons remain significant when a bonferroni cor-

rection for running two comparisons is applied. Thus

the female participants demonstrated the valence-spe-

cific laterality effect under free viewing conditions

(Fig. 2).The analysis of the performance of the male partici-

pants also showed a significant main effect of valence,

F ð1; 34Þ ¼ 29:63, p < :0001, which was due to greater

accuracy at classifying positive (mean¼ 78%) versus

negative (mean¼ 62%) emotions. However, in contrast

to the women, the male participants failed to show a

significant valence� side interaction, F ð1; 34Þ ¼ 0:01,p ¼ :9, with the accuracy of the men at detecting eachtype of emotion being unaffected by the side that the

faces were presented at (Fig. 3). Therefore, the signifi-

cant three-way interaction between side, valence, and

Fig. 2. Female discrimination accuracy as a function of side and va-

lence (positive, negative).

Fig. 3. Male discrimination accuracy as a function of side and valence

(positive, negative).

Table 3

Response scores (percentage) for the control condition

Side chosen

Left Right

Positive label 41 (24) 59 (24)

Negative label 56 (19) 44 (19)

Standard deviations are in parentheses.

Fig. 4. Side chosen as a function of side and valence label (positive,

negative).

458 P. Rodway et al. / Brain and Cognition 53 (2003) 452–463

sex, obtained in the main analysis, was due to the female

participants, but not the males, showing the valence-

specific laterality effect.

Finally a trend in the three-way interaction between

side, valence, and morphing, was obtained

F ð4; 296Þ ¼ 2:17, p ¼ :072. We ran additional analysesto examine this interaction in more detail. Although this

interaction did not reach significance, these comparisons

were theory driven, and justified by the view outlined in

the introduction, that the valence-specific effect may be

strongest when the discrimination task is most difficult.

Additional analyses for each level of morphing demon-

strated a significant interaction between side� valence

at the 5% morph, F ð1; 74Þ ¼ 4:47, p < :037, and the 10%morph, F ð1; 74Þ ¼ 11:77, p < :0010, but not at the 15%

morph, F ð1; 74Þ ¼ 1:51, p ¼ :22, 20% morph, F ð1; 74Þ ¼1:63, p ¼ :21, and 25% morph, F ð1; 74Þ ¼0:01, p ¼ :95.These results indicate that the valence-specific effect is

larger when the discrimination is most difficult. Finally,

the four-way interaction between side, valence, sex, and

morphing did not reach significance, F ð4; 296Þ ¼ 1:04,p ¼ :38. It is possible that this effect, and any five-wayinteractions, did not reach significance because of a lack

of power. However, we make no claims regarding these

effects.

4. Control condition

For the control trials the two faces were identical but

the emotion label differed and the participants were re-

quired to select the side that they thought the �emo-

tional� face was on. In this condition, the dependent

variable was the percentage of times participants chose

the left side (with the right side simply being its com-

plement to 100%). As the faces were identical thereshould have been no systematic differences between the

sides chosen, with participants selecting either side 50%

of the time on average.

A 2� 2� 2 [sex (male vs. female) handedness (left vs.

right) valence label (positive vs. negative)] mixed-model

ANOVA was conducted on the response data for the

control trials. The main effects of sex and handedness

failed to reach significance (F �s < 1). However, the effectof valence reached significance, F ð1; 74Þ ¼ 10:31,p < :002, demonstrating that the emotional label influ-

enced the side selected even when the faces were iden-

tical (Table 3, Fig. 4).

The valence effect was analysed further by conducting

separate one-sample t tests against 50% for each valence

label. For the negative label there was a significant dif-

ference tð77Þ ¼ 2:12, p < :0037, with participants se-lecting the left side more than the right side (56% vs.

44%). For the positive label there was also a highly

significant effect, tð77Þ ¼ �2:82, p < :006, with partici-

pants selecting the right side more frequently than the

left side (59% vs. 41%). Thus, the valence of the label

caused a response bias in participants when the faces did

P. Rodway et al. / Brain and Cognition 53 (2003) 452–463 459

not differ in emotional expression, with participants se-lecting the face on the left more frequently when the

label was negative and the face on the right more fre-

quently when the label was positive.

5. Discussion

The participants were more accurate at discriminat-ing positive emotions than negative emotions. This

replicates Jansari et al.�s (2000) results, and those of

Hugdahl, Iverson, and Johnsen (1993), who also found

participants to be more accurate at identifying positive

emotions. This finding also corresponds to other work

which suggests that some negative emotional expres-

sions, such as sadness and fearfulness, may be more

difficult to recognise than other emotions (Adolphset al., 1996; Ekman & Freisen, 1976).

It was found that women showed the valence-specific

laterality effect whereas the male participants did not.

Women discriminated negative expressions more accu-

rately when they were presented on the left-hand side

and discriminated positive expressions more accurately

when they were presented on the right-hand side. Dis-

crimination of facial expressions by the male partici-pants was unaffected by side of presentation. These

results replicate those of van Strien and van Beek (2000)

under free-viewing conditions and demonstrate that

their findings were not caused by the use of cartoon

faces as the use of real faces in this study resulted in the

same pattern of results. An implication of these findings

is that previous reports of a valence-specific laterality

effect, for example by Reuter-Lorenz and Davidson(1981), may have been caused by female participants

within their sample, which remained undetected because

the effect of sex was not analysed. Finally, these results

do not support the view that the RH selectively pro-

cesses negative emotions and both hemispheres are in-

volved in processing positive motions, as suggested by

Asthana and Mandal (2001).

The findings of this study partially replicate Jansariet al.�s (2000) results by showing that laterality effects

can be obtained in free viewing conditions. An impor-

tant difference is that in this study the valence-specific

laterality effect was limited to the female participants. As

more participants were used in the present experiment

compared to Jansari et al.�s (78 vs. 28) the difference in

results might have been due to a difference in power

between the studies. However, van Strien and van Beek(2000) only used 32 participants and found the valence-

specific laterality effect for the female participants but

not the men. It is possible that van Strien and van Beek�semotional rating task, which consisted of presenting

cartoon faces for 150 ms, is more sensitive than the free

viewing task used by Jansari and in this study. Thus, it

remains possible that the sex-specific nature of the va-

lence-specific laterality effect only emerges when a studyhas enough power.

Handedness did not influence the lateralised pro-

cessing of emotional expressions. This finding replicates

van Strien and van Beek�s results with a larger number

of participants and a different task and indicates that

left- and right-handers do not differ in the way that they

process emotional expressions. Previously Everhart

et al. (1996) found that left-handers classified faces withneutral expressions (those without an emotional ex-

pression) as angry more often when they were presented

in the RVF than the LVF, whereas right-handers did not

show visual field differences for neutral faces. This might

suggest that for left-handers the perception of negative

emotions is more strongly lateralised in the LH than it is

for right-handers. However, this interpretation should

be treated with caution because handedness did not af-fect the perception of faces with emotional expressions

(happy or angry), which actually suggests no effect of

handedness on the perception of facial emotion. More-

over, as noted by Everhart et al., the power of their

study is likely to have been weak because of the small

sample size, with only 14 left-handed and 14 right-han-

ded participants. Given the mixed findings of Everhart

et al.�s study, and the results of this experiment and vanStrien and van Beek�s (2000), the weight of evidence

indicates that the lateralised processing of facial emotion

is not affected by handedness. Thus, differences in cor-

tical organisation between left- and right-handers do not

seem to influence the lateralised perception of facial

affect.

As only the female participants showed the valence-

specific laterality effect this suggests that women aremore lateralised, than are men, for the perception and

interpretation of emotional expressions. This result

concords with other findings (Burton & Levy, 1989;

Ladavas et al., 1980; van Strien & van Beek, 2000; Voyer

& Rodgers, 2002). A recent functional magnetic reso-

nance imaging study by Lee et al. (2001), found that the

brain regions used by men and women, to perceive facial

affect, differ in several ways. When perceiving happyfacial expressions, activation of the LH was greatest in

both men and women, but the women showed activation

of additional regions, including the left thalamic area

and right temporal and occipital regions. Moreover, for

sad expressions, men and women showed very different

patterns of activation, with women showing greater LH

activation and men showing greater RH activation.

These findings suggest that the perception of facial ex-pressions is both gender and valence specific (Lee et al.,

2001) and may indicate that women are more lateralised

for the perception of facial affect.

It might be expected that if women are more latera-

lised for perceiving emotional expressions then they may

show superiority in emotional discrimination in com-

parison to men. Although other studies using auditory

1 We are grateful to an anonymous reviewer for suggesting this

interpretation of the results.

460 P. Rodway et al. / Brain and Cognition 53 (2003) 452–463

stimuli have indicated that this may be the case (Voyer& Rodgers, 2002), the present results found no evidence

for a female superiority. In fact, while there was no

overall difference in accuracy between men and women,

the men were superior when the emotional discrimina-

tion was most difficult (5% morphing). This indicates

that men may be more sensitive than women to ex-

tremely subtle changes in emotional expression.

An important finding of the present study is that forthe control trials the emotional label caused a bias in

responding to faces which were identical. If the emotion

label was positive the participants selected the right side

more frequently than the left side. Conversely, if the

emotion label was negative the participants selected the

left side more than the right side.

This finding has important implications for other

studies which have examined the valence-specific later-ality effect. As the response bias is in the same direction

as the valence effect, with the left-hand side associated

with negative valence and the right-hand side with po-

sitive valence, it is possible for it to have affected pre-

vious research findings. Studies which have used a

discrimination task and have presented participants with

an emotional label at the same time as the face may have

been particularly affected by the response bias. In thesetasks the label may have strongly influenced the side

selected.

A further implication of this finding is that the more

difficult the emotional discrimination is, either due to

brief presentation, or subtle differences between stimuli,

then the more participants will guess and the more likely

it is that the response bias will occur. The valence-spe-

cific laterality effect may emerge when the difficulty of atask is increased so that participants guess more fre-

quently. As described in the introduction, van Strien and

van Beek (2000) also suggest that the valence-specific

laterality effect emerges when a task requires a difficult

discrimination of emotions, rather than an easier per-

ceptual matching of emotions. However, they argue that

this difference occurs because, to make a successful

discrimination, anterior regions of each hemisphere areutilised, whereas a perceptual task relies on posterior

regions of each hemisphere. An alternative suggestion is

that an increase in the difficulty of making the emotional

discrimination increases guessing by participants, and

the response bias, which then causes a spurious valence-

specific laterality effect.

The present results provide mixed support for the

idea that a response bias caused the valence-specific ef-fect. If increased discrimination difficulty increases the

response bias, then the valence-specific laterality effect

should have interacted with the degree of morphing,

with a larger effect for the most difficult discrimination

level. This interaction was short of significance in the

main analysis (F ¼ 2:17, p ¼ :07), and was due to va-

lence-specific laterality effects at the 5 and 10% morph

levels, but no such effect at the 15, 20, and 25% levels.This result therefore supports the view that a response

bias for difficult discriminations may contribute to the

valence-specific effect.

Importantly, however, the response bias obtained on

the control trials did not interact with the sex of the

participant (or handedness). If the valence effect in the

women had been due to a response bias then the women

should have shown this bias more strongly than the menin the control task. As this was not the case, it appears

that a response bias cannot account for the valence-

specific laterality effect in women. Thus, the present

findings suggest that women are more strongly latera-

lised for processing emotional expressions. In addition,

it is unlikely that a response bias can account for all

valence-specific laterality effects, particularly where

brain activity has been measured and correlated withemotional processing (e.g., Ahern & Schwartz, 1985).

However, the hypothesis that guessing contributes to the

valence-specific laterality effect certainly requires further

investigation.

There are several possible causes of the response bias.

It could be explained in terms of Kinsbourne�s selectivehemispheric activation theory (1970)1 which suggests

that an expectancy for certain material activates thehemisphere that is most specialised for dealing with such

material. This activation spreads throughout the hemi-

sphere and automatically increases the allocation of at-

tention to the visual field contralateral to the activated

hemisphere, resulting in the more detailed analysis of

information presented in the contralateral hemifield. In

the present experiment it is possible that the attempt to

discriminate identical faces resulted in the recruitment ofanterior regions, so as to experience the emotion de-

scribed by the label and aid the discrimination process.

As the experience of positive and negative emotions

activates left-frontal and right-frontal regions, respec-

tively (Davidson, 1993a, 1993b), this could then create a

behavioural bias in favouring the right or left hand.

That is, activation of anterior regions of a hemisphere

may have increased the activation of adjacent regionsinvolved in motor control, causing a bias in favouring

the hand controlled by the activated hemisphere.

Based on Kinsbourne�s theory it could be the case

that each emotional label activated a particular hemi-

sphere, and in accord with the valence hypothesis this

might have been the RH when the label had negative

valence and the LH when the label had positive valence.

As a result, neutral faces on the left-hand side mighthave been perceived as more negative and neutral faces

on the right-hand side as more positive. Thus, in this

case the response bias would have been caused by a

P. Rodway et al. / Brain and Cognition 53 (2003) 452–463 461

difference in the way neutral faces were perceived whenon the left- or right-hand side.

A similar proposal can be made without suggesting a

role for the valence label in promoting hemispheric ac-

tivation. It could be the case that the perception of

neutral expressions is determined by valence-specific

asymmetries. Thus, a neutral face on the left might be

viewed more negatively than a neutral face on the right

because the RH has a greater role in negative valence.Similarly, a face on the right might be viewed more

positively because the LH has a greater role in pro-

cessing positive valence. An implication of this would be

that valence-specific laterality effects might be obtained

for the perception of neutral expressions.

A further suggestion is that the participants perceived

no differences between the neutral faces but they asso-

ciated the left side with �negative� and the right side with�positive� and when they were required to guess their

responses reflected this bias. The association of left with

�bad� (and right with �good�) is a strong association

which has been prevalent throughout history and within

many cultures. For example, it is traditional for �evil�characters in the theatre to always exit and enter the

stage on the left, whereas �good� characters use the rightside of the stage. Moreover in practically every culturethe term for left, or left-handed, carries negative con-

notations (e.g., worthless in old English, clumsy in

French, and sinister in Italian). If participants uncon-

sciously associated left with �bad� then this could have

caused the response bias on this forced choice task.

A limitation of this study is that no assessment of the

emotional and psychological state of the participants

was made. This is important because a participant�semotional state has been found to influence their per-

ception of facial affect (David, 1989; Gage & Safer,

1985). Moreover, as women have higher rates of de-

pression than men (Nolen-Hoeksema, 1987) then this

may be one reason why women show stronger valence-

specific effects. It is therefore important for future re-

search to include an assessment of the emotional state of

participants.A further limitation, which may have influenced the

present findings, is that the stimuli were of a male face.

The valence-specific effect may have been present in

women because the men were either less able, or less

willing, to analyse the emotional expression of a male

face. However, this is unlikely because the male partic-

ipants were as accurate as the women at discriminating

emotions. Also, it can be noted that van Strien and vanBeek (2000) and Jansari et al. (2000) used male faces as

stimuli. Thus, the different findings between these stud-

ies cannot be due to the use of male faces. Finally, as

suggested by van Strien and van Beek, it appears un-

likely that the use of male faces has affected results in

this area because other studies have found that the sex of

the face does not interact with the sex of the participant

(Cutler, Gilgen, & Gilpin, 1985; Hugdahl et al., 1993).However, while we suggest these results were not de-

pendent on the use of a male face this possibility cannot

be discounted and it is therefore important that future

research in this area include facial stimuli of both sexes.

To summarise, the present study found that the va-

lence-specific laterality effect, in free viewing conditions,

only applied to female participants. This suggests that

women are more lateralised for the processing of emo-tional facial expressions than are men, with the LH

devoted to processing positive emotions and the RH

devoted to processing negative emotions. Conflicting

findings within the literature may have been caused, in

part, by ignoring the influence of sex on emotional

processing. It is possible that the sex-specific nature of

the valence laterality effect is apparent when the task is

sensitive, or when a large number of participants areused. Moreover as a free viewing task was used the re-

sults suggest that these findings apply to natural viewing

conditions.

There was no evidence that handedness influences the

lateralised processing of emotional information. Evi-

dence for a role of handedness has been weak and in-

consistent and the present findings, and those of van

Strien and van Beek, strongly suggest that handednessdoes not influence the lateralised processing of facial

affect. Finally, the participants demonstrated a response

bias when required to discriminate between identical

faces. This response bias requires further investigation

as it may have contributed both to valence-specific lat-

erality effects and the conflicting results within the lit-

erature. Future research needs to be aware that this

response bias can produce laterality effects which mightnot be caused by a difference in the way the hemispheres

process emotional information.

Acknowledgments

We thank two anonymous reviewers for comments

on an earlier version of the manuscript and Astrid

Schepman for useful discussions.

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