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Attentional control in dysphoria: An investigation using the antisaccade task
Biological Psychology 80 (2009) 251–255
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Brief report
Attentional control in dysphoria: An investigation using the antisaccade task Nazanin Derakshan a,*, Maureen Salt a, Ernst H.W. Koster b a b
School of Psychology, Birkbeck University of London, UK Ghent University, Belgium
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 June 2008 Accepted 19 September 2008 Available online 2 October 2008
We examined inhibitory mechanisms in dysphoria using direct measures of attentional control. Dysphoric and non-dysphoric participants performed standard and delayed versions of the antisaccade and prosaccade tasks with facial expressions as stimuli. Results showed higher error rates in the standard antisaccade task than in the delayed tasks, with the dysphoric group having higher error rates in response to emotional facial expressions, in particular happy expressions. Our findings indicate impaired attentional processing in response to emotional facial expressions, in particular happy expressions, in dysphoria. Implications for understanding the mechanisms underlying attentional control in dysphoria are discussed. Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved.
Keywords: Dysphoria Antisaccade Attentional control Emotional faces
1. Introduction Cognitive models of depression postulate that biased processing of emotional information plays an important role in the aetiology and maintenance of depressive symptoms (Teasdale and Barnard, 1993; Williams et al., 1997). Recently, it has been argued that deficient inhibition of emotional information may underlie the hallmark feature of depression, i.e., sustained negative affect, through its association with rumination and impaired mood regulation (Joormann et al., 2007). In some paradigms (e.g., negative affective priming, modified Sternberg task) although large overall inhibition impairments were not found, depressed individuals showed marked inhibitory deficiencies when processing negative material (Goeleven et al., 2006; Joormann and Gotlib, 2008). In most of these tasks, however, the main dependent variable is reaction time which does not provide a direct measure of attentional processes and is susceptible to alternative explanations. The measurement of eye-movements in visual attentional processing is becoming increasingly important (see Weierich et al., 2008, for a review). Eye-movements have the advantage of being distinguishable in terms of their temporal and spatial characteristics thus providing increased precision in understanding the
* Corresponding author at: Affective and Cognitive Neuroscience Lab, School of Psychology, Birkbeck University of London, Malet Street, London WC1E 7HX, UK. Tel.: +44 7968173484. E-mail address: [email protected] (N. Derakshan).
mechanisms of visual attentional processing. Caseras et al. (2007) measured eye-movements in dysphoric and non-dysphoric groups for negative and positive scenes that were paired with control (neutral) pictures. While the two groups did not differ in terms of orienting towards emotional pictures, relative to control pictures, the dysphorics had longer gaze durations on the negative pictures, indicating sustained attention for negative material. Thus eyemovements provided information on temporal characteristics of attentional processing that would not be obtainable through reaction times alone. Saccadic eye movement tasks can provide us with a precise assessment of some aspects of top-down cognitive control processes that influence attention allocation (Munoz and Everling, 2004; Ridderinkhof et al., 2004). In relation to attentional control, the antisaccade task (Hallet, 1978) offers a promising way forward. In this task participants are required to inhibit the reflexive tendency to look towards a sudden-onset cue, presented peripherally to one side of fixation, and generate a correct saccade to its mirror position as quickly as possible. Antisaccade performance involves competition between the reflexive saccade and voluntary initiation of the antisaccade, with errors occurring when activation in neural systems underlying the antisaccade cannot successfully compete with the prosaccade reflex (Massen, 2004; see Hutton and Ettinger, 2006, for a review). Recent work has used the antisaccade task to examine inhibitory control in anxiety (Derakshan et al., in press; Ansari et al., 2008; Hardin et al., 2007; Jazbec et al., 2006). There is also evidence from the antisaccade task on attentional control in depression (e.g., Sweeney et al., 1998; Jazbec et al.,
0301-0511/$ – see front matter . Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.biopsycho.2008.09.005
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2005). Sweeney et al. (1998) found that depressed participants made more reflexive errors in the antisaccade condition when the abrupt stimulus was an oval-shaped cue (for similar results see Jazbec et al., 2005). The neural structures involved in antisaccade performance show interesting overlap with the neural impairments observed in depression. Recent neuroimaging findings suggest the major involvement of prefrontal brain areas such as the dorsolateral prefrontal cortex (DLPFC) implicated in attentional control using the antisaccade task (Ettinger et al., 2008). Such areas are considered to have substantial involvements in the top-down regulation of emotional processing in anxiety and depression (Davidson et al., 2002; Bishop, 2007). We aimed to examine inhibition in relation to negative and positive emotional information, since depression has been associated both with enhanced attention and impaired inhibition for negative material (see Joormann et al., 2007) and reduced attention and processing deficiencies for positive information (e.g., Cavanagh and Geisler, 2006). To our knowledge, the present antisaccade study is the first to examine inhibitory control in relation to depression using facial expressions of emotion as stimuli. Using the standard anti- and prosaccade tasks (SA; SP) with stimuli comprising angry, happy and neutral facial expressions, we investigated the effects of subclinical depression (dysphoria) on attentional control processes. As this is the first study to investigate antisaccade performance in response to facial expressions of emotion a dysphoric sample was chosen to minimise possible impairments in antisaccade performance attributable to some cognitive deficits typically observed in clinically depressed individuals. We hypothesised that dysphorics, compared to non-dysphorics, would show impaired performance when the to-be-inhibited stimuli are emotional expressions and this would be evident in the standard antisaccade task where top-down attentional control is needed for the effective inhibition of reflexive prosaccades towards the emotional face. Impaired antisaccade performance can reflect deficits in inhibitory control and volitional saccade generation (Reuter et al., 2007). To allow investigation of both processes, in addition to the standard tasks we also administered delayed versions of the anti- and prosaccade tasks (DA; DP) (cf. Reuter et al., 2007). In delayed tasks the demand to inhibit an erroneous prosaccade is not simultaneous with the requirement to generate a volitional saccade. The isolation of the initiation of a volitional response means that the generation of the saccade takes place during the delay period, reducing the competition between stimulus-driven and top-down processes required for the inhibition of the prosaccade. We hypothesised that dysphoria would be associated with impaired inhibition but not impaired volitional saccade generation. 2. Method 2.1. Participants Participants were fifty-nine volunteers (42 female) from the University of London (for group characteristics see Section 3). They had normal or corrected to normal vision (wearing glasses or contact lenses when necessary) and normal hearing. Participants were not paid for their contribution to the experiment. Participants were treated in accordance with Birkbeck’s ethical code of conduct. Upon arriving at the laboratory and reading the relevant instruction sheet they signed a consent form and were given the opportunity to leave the experiment at any point without explanation. Upon completion of the experiment they were fully debriefed.
2.2. Materials and procedure 2.2.1. Self-report measure The Beck Depression Inventory-II (BDI-II) (Beck et al., 1996) was used to classify participants as dysphoric or non-dysphoric. This questionnaire consists of 21 items related to the occurrence of depressive symptoms over the past two weeks. Scores range from 0 to 63 with higher scores indicating higher depression severity. We followed the cut-off scores for dysphoria proposed by Beck et al. (1996; 14–19 mild, 20–28 moderate, and >29 severe) to classify participants. 2.2.2. Visual stimuli 18 faces (half female) depicting angry, happy and neutral facial expressions (6 of each valence) were taken from the Pictures of Facial Affect (Ekman and Friesen, 1976) and the NimStim Face Stimulus Set (Tottenham et al., 2002). Non-facial features were removed and faces were resized to 45 mm 70 mm (4.38 6.78) and presented in grayscale against a black background. The experiment involved four blocks (SA, SP, DA, DP) each comprising 90 trials, totalling 360 trials. Each block of 90 trials included 30 angry, 30 happy, and 30 neutral trials. For each of the angry, happy, and neutral facial expressions 6 faces were shown and each face was repeated 5 times per valence. The order of standard (A) and delayed (B) tasks was counterbalanced in an AB-BA design. The order of antisaccade and prosaccade tasks was counterbalanced within each of the standard and delayed tasks, with half of the participants randomly assigned to order of set SA, SP, DP, DA or set SP, SA, DA, DP and the other half to DA, DP, SP, SA, and DP, DA, SA, SP tasks. This ensured that the presentation of standard/delayed as well as anti- and prosaccade tasks was counterbalanced. A complete randomisation of tasks was not done in order to avoid large error variance due to very different temporal characteristics of the tasks. The inter-trial interval varied between 700 ms and 1300 ms. Each trial began with a central fixation cross (1.158 1.158) for 1600 ms. A face then appeared with equal probability to the left or right side of the cross at 118 (800 ms). A 440 Hz tone was presented (50 ms) simultaneously with, (on SA and SP trials) or 800 ms after, (on DA and DP trials) presentation of the face. Participants fixated the cross, then as soon as the face appeared, directed their gaze as quickly as possible away from the face, to its mirror position on the screen (SA) or towards the face (SP). In delayed tasks participants continued fixation and made an antisaccade (DA) or prosaccade (DP) when the tone sounded (Fig. 1a and b). 2.3. Eye-tracking Eye-movements were tracked using the LC Technologies ‘‘Eyegaze’’ system (LC Technologies, 2003), which uses the Pupil-Centre Corneal Reflection method (PCCR; Mason, 1969; Merchant and Morrisette, 1973). The gaze-point position is estimated at 60 Hz, with a typical root mean square error of less than 6.35 mm. Eye-movements were extracted using the R programming environment (Venables and Smith, 2005). Visual stimuli were presented on a 17 in. LCD (refresh rate of 16.6 ms) controlled by the DMDX programme (Forster and Forster, 2003), which ensures millisecond timing accuracy. 2.4. Procedure Participants were tested individually in a dimly lit room. Half completed the BDI-II before completing the task and half afterwards (with a distractor task in between to control for possible confounding effects). As questionnaires may prime a mood state that subsequently influences antisaccade performance, this
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Fig. 2. Percentage immediate errors (with standard errors) as a function of task (standard antisaccade, delayed antisaccade, and delayed prosaccade) and emotional expression of face (angry, happy, neutral) for each of the dysphoric and non-dysphoric groups.
to make these errors compatible in terms of temporal characteristics to errors in the antisaccade task (that are believed to be triggered by the stimulus). Accordingly, we took the average correct saccade latency in the standard prosaccade task plus two standard deviations of individual saccade latencies in this condition, as the upper limit for classifying erroneous prosaccades as immediate errors in the other tasks (see Reuter et al., 2007). For the purpose of statistical analyses, we considered the percentage of immediate errors and the mean latency of correct saccades (with latencies between 80 ms and 1000 ms after tone onset) in all tasks. 3. Results 3.1. Group characteristics
Fig. 1. (a) Example of an antisaccade trial with a happy emotional expression. (b) Example of a prosaccade trial with a happy emotional expression.
procedure allowed us to control for this. Participants were seated in front of the Eyegaze system at a distance of 60 cm with their chin on a chin-rest. 18 practice trials and calibration of the eye-tracker preceded each block and speed and accuracy were emphasised. The session lasted approximately 60 min. 2.5. Data preparation Saccades were defined on the basis of amplitude (>38) and velocity (>308/s) made after cue onset (presentation of face in standard blocks and tone in delayed blocks). Only the initial saccade was used to evaluate performance (Fischer et al., 1993). Anticipatory saccades (<80 ms of face onset) were removed from analyses. Consistent with Reuter et al. (2007) we defined errors and latencies in the following manner: In the SA, DA, and the DP tasks, errors (erroneous prosaccades) were defined as saccades that were directed towards the face and had a latency of greater than 80 ms after face onset. Inspection of the latencies of erroneous prosaccades in the delayed tasks and the standard antisaccade task revealed different distributions, suggesting that not all errors in the delayed tasks were triggered by the face. Accordingly, an upper limit was defined for error classification in the delayed tasks
Using the criteria proposed by Beck et al. (1996), 12 participants (11 female) with BDI-II scores >13 were classified as dysphoric (M = 20.25, SD = 9.18) and 12 participants (10 female) with BDI-II scores < 5 (M = 1.75, SD = 1.54), as non-dysphoric. They were matched for age (dysphorics: M = 32.5, SD = 5.99; non-dysphorics: M = 32.67, SD = 4.45, t < 1) and gender (x2 = .38, N.S.). No participant reported a medical history of depression or that they were being treated for depression or any anxiety-related disorder at the time of experiment. 3.2. Errors Fig. 2 shows the percentage of errors committed by both groups across tasks. To examine the effects of inhibition and volitional saccade generation on errors, a 3 3 2 Mixed ANOVA with Task (SA, DA, DP) and Valence of face (angry, happy, neutral) as within-subject factors and Group (dysphoric, non-dysphoric) as between-subject factor was conducted.1 In line with our 1 Consistent with Reuter et al. (2007) we did not include the SP condition in the analysis. Research has generally found that the percentage of errors in this task tends to be extremely low and negligible. In the current study, both dysphoric and non-dysphoric groups had negligible error rates in the SP task (dysphorics, M = .09%; non-dysphorics, M = 0%). There was no effect of Valence, F = 1, nor was there an interaction effect of Task Valence, F = 1. Our manipulations concentrated on the effects of inhibition vs. saccade generation processes (with prior inhibition), neither of which is measured by the SP task as there is no competition between reflexive and top-down processes in the SP task.
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hypotheses, we carried out Helmert contrasts on Task to examine the effect of delay (SA vs. DA and DP). Analysis found a significant main effect of Task, F(2,44) = 5.24, p < .01, with more errors in SA compared with DA and DP tasks, F(1,22) = 9.15, p < .007. This effect was qualified by an interaction with Group, F(2,44) = 3.25, p < .05, which indicated that the dysphoric group committed greater percentages of errors in the SA task than in the DA and DP tasks (16.5% vs. 6.3% and 9.2%) compared with the non-dysphoric group who showed no differences (10.8% vs. 9.6% and 9.8%), F(1,22) = 5.81, p < .03. Additional analyses showed that the two groups did not differ on the delayed antisaccade nor delayed prosaccade tasks (all Fs < 1). Collectively, these results indicated that while dysphorics and nondysphorics did not differ in terms of volitional saccade generation, they differed in inhibition, as evidenced by higher error rates in the SA task of dysphorics compared with non-dysphoric participants (see Fig. 2). Further analysis therefore concentrated on the SA task only. A 3 2 Mixed ANOVA with Valence (angry, happy, neutral) as within-subject factor and Group (dysphoric, non-dysphoric) as between-subject factor was performed. A main effect of Valence showed greater percentages of errors in response to emotional (14.8%) compared with neutral expressions (11.5%), F(2,44) = 3.1, p < .05; an effect that interacted with Group, F(2,44) = 4.12, p < .03. Dysphorics committed more errors in response to emotional than neutral stimuli (18.3% vs. 12.3%) an effect that was not evident in the non-dysphorics, (11.0% vs. 10.6%), F(1,22) = 4.36, p < .05. Polynomial contrasts showed that group differences were particularly pronounced in response to happy expressions (dysphorics: 21.0%; non-dysphorics: 10.0%), F(1,22) = 8.75, p < .008. 3.3. Latencies Mean correct saccade latencies are depicted in Fig. 3. A 4 3 2 mixed ANOVA, with Helmert contrasts on Task, was conducted with Task (SP, SA, DA, DP), Valence (angry, happy, neutral) and Group (dysphoric, non-dysphoric) as factors. There was a main effect of Task, F(3,66) = 16.10, p < .001, with faster saccades in SP compared with SA, DA and DP tasks, F(1,22) = 62.21, p < .001. No effects involving Valence, Task or Group were significant (Fs < 1).
Fig. 3. Mean correct saccade latencies (with standard errors) as a function of task (standard antisaccade, delayed antisaccade, and delayed prosaccade) and emotional expression of face (angry, happy, neutral) for each of the dysphoric and non-dysphoric groups.
4. Discussion We investigated inhibitory control in dysphoric and nondysphoric individuals using the antisaccade task. The main result was that the dysphoric group, compared with the non-dysphoric group, had higher error rates when stimuli were emotional expressions, particularly in response to happy facial expressions in the standard antisaccade task. This finding indicates that dysphoric individuals show impairments in inhibiting the impact of emotional faces, especially happy facial expressions of emotion. Delayed tasks involved a much lower error rate compared to the standard antisaccade task for all participants, across all facial expressions, indicating that the dysphoric and non-dysphoric groups did not differ in terms of volitional saccade generation, even when emotional faces were present. Correct antisaccade latencies were not influenced by emotional facial expressions, and there were no group differences across tasks: all participants had shorter latencies in the standard prosaccade compared with the antisaccade task, replicating previous findings (Reuter et al., 2007). The innovative feature of the current experiment is that it used a direct measure of attentional control to examine inhibitory processes in relation to emotional facial expressions in dysphoria. The finding of higher error rates in the standard antisaccade task in response to emotional expressions compared with neutral expressions in the dysphoric group is important, as it implicates dysfunctional inhibition in relation to emotional information in attentional control in dysphoria. It indicates that not only deficient inhibition of negative information (Caseras et al., 2007; Joormann et al., 2008), but also processing of positive information is affected in dysphoria. Our finding of higher error rates with happy emotional expressions in the dysphoric group is particularly interesting and deserves further investigation. A growing body of psychophysiological evidence has recently established that depressed individuals have reduced N2 amplitudes in response to happy faces in the right parietal cortex (Deldin et al., 2000), indicating deficits in processing happy faces. Similarly, Cavanagh and Geisler (2006) showed that depressed individuals had lower P3 amplitudes and longer P3 latencies when viewing happy faces, which indicated that depressed people allocate less attentional resources when processing happy faces and need longer to process them. Our results relating to errors made by the dysphoric group provide an interesting extension to these findings, showing that dysphoric individuals fail to exercise attentional control effectively when the to-be-inhibited stimuli are emotional, especially happy expressions. In an extension of these findings, our results showed no group difference in inhibitory processes when the to-beinhibited stimulus was a neutral face suggesting that salient emotional stimuli modulate inhibitory processes in dysphoria. One tentative explanation for the observed effects with happy faces is that the positive expression is unexpected and surprising to the dysphoric group. As depression is related to negative beliefs about the world, the self, and the future (Beck, 1967), the presentation of positive information could violate the expectations of the dysphoric individuals, causing enhanced errors. There is evidence from eye-movements (Caseras et al., 2007) as well as reaction times (Koster et al., 2005) to show that depression is associated with an attentional bias for negative material when presented for long durations indicating sustained processing of negative material in dysphoria. These results collectively support the view that attentional bias for salient emotional material can impair the efficient top down regulation of attentional control, especially under conditions when the inhibition of this material is needed for effective task performance (see Eysenck et al., 2007, for a review).
N. Derakshan et al. / Biological Psychology 80 (2009) 251–255
There are a number of ways in which future research can address the limitations of the current investigation. Although the distribution of gender was balanced across groups the majority of the sample was female. Future research should include equal numbers of males and females and adopt a more stringent classification method to equate both groups in terms of demographic variables. Second, it is important to examine inhibitory impairments in response to a wider range of negative and positive material. We used angry facial expressions as they signal personal rejection thus having more personal relevance (Gilboa-Schechtman et al., 2004), but it is important to examine inhibitory processes in response to sad faces that also carry negative information congruent with depressed schemas. Third, there is a need to investigate the specific conditions leading to impaired inhibition of positive as well as negative material in clinical depression. Fourth, future research should include a condition to evaluate the mechanisms associated with voluntary initiation of a saccade; one that is free of any current or prior demand to suppress an erroneous prosaccade. The inclusion of this condition (especially in the context of clinical depression) would not only isolate any effects associated with inhibition, but would also be informative of the processes involved in volitional saccade generation, and maintenance of relationships between goals and action. In sum, the present study is the first to study inhibition of facial expressions of emotion using the antisaccade task. Our results distinctively add to previous antisaccade findings on inhibitory processes in dysphoria (e.g., Jazbec et al., 2005; Sweeney et al., 1998) by examining the modulatory role of emotional material in inhibitory processes. That is, in the present study inhibition involved ignoring irrelevant emotional information at the visual modality with only limited processing of emotional material. In view of the results presented it will be important to further elucidate the conditions that are associated with inhibitory deficits for negative and positive material. Acknowledgements This work was supported by a Royal Society International Joint Project Grant awarded to Nazanin Derakshan (ND) and Ernst Koster (EK). The research was carried out by Maureen Salt, under the supervision of ND and EK, at the Affective and Cognitive Neuroscience Lab at Birkbeck University of London. The authors would like to thank Tahereh L. Ansari and Leor Shoker for help with programming and data preparation. References Ansari, T.L., Derakshan, N., Richards, A., 2008. Effects of anxiety on task switching: evidence from the mixed antisaccade task. Cognitive, Affective, and Behavioural Neuroscience 8 (3), 229–238. Beck, A.T., 1967. Depression: Clinical, Experimental, and Theoretical Aspects. Hoeber, New York. Beck, A.T., Steer, R.A., Brown, G.K., 1996. Manual for the Beck Depression InventorySecond Edition (BDI-II). The Psychological Corporation, San Antonio, Texas. Bishop, S.J., 2007. Neurocognitive mechanisms of anxiety: an integrative account. Trends in Cognitive Sciences 11, 307–316. Caseras, X., Garner, M., Bradley, B.P., Mogg, K., 2007. Biases in visual orienting to negative and positive scenes in dysphoria: an eye movement study. Journal of Abnormal Psychology 116 (3), 491–497. Cavanagh, J., Geisler, M.W., 2006. Mood effects on the ERP processing of emotional intensity in faces: a P3 investigation with depressed students. International Journal of Psychophysiology 60 (1), 27–33. Davidson, R.J., Pizzagalli, D., Nitschke, J.B., Putnam, K., 2002. Depression: perspectives from affective neuroscience. Annual Review of Psychology 58, 259–289.
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Biological Psychology journal homepage: www.elsevier.com/locate/biopsycho
Brief report
Attentional control in dysphoria: An investigation using the antisaccade task Nazanin Derakshan a,*, Maureen Salt a, Ernst H.W. Koster b a b
School of Psychology, Birkbeck University of London, UK Ghent University, Belgium
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 June 2008 Accepted 19 September 2008 Available online 2 October 2008
We examined inhibitory mechanisms in dysphoria using direct measures of attentional control. Dysphoric and non-dysphoric participants performed standard and delayed versions of the antisaccade and prosaccade tasks with facial expressions as stimuli. Results showed higher error rates in the standard antisaccade task than in the delayed tasks, with the dysphoric group having higher error rates in response to emotional facial expressions, in particular happy expressions. Our findings indicate impaired attentional processing in response to emotional facial expressions, in particular happy expressions, in dysphoria. Implications for understanding the mechanisms underlying attentional control in dysphoria are discussed. Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved.
Keywords: Dysphoria Antisaccade Attentional control Emotional faces
1. Introduction Cognitive models of depression postulate that biased processing of emotional information plays an important role in the aetiology and maintenance of depressive symptoms (Teasdale and Barnard, 1993; Williams et al., 1997). Recently, it has been argued that deficient inhibition of emotional information may underlie the hallmark feature of depression, i.e., sustained negative affect, through its association with rumination and impaired mood regulation (Joormann et al., 2007). In some paradigms (e.g., negative affective priming, modified Sternberg task) although large overall inhibition impairments were not found, depressed individuals showed marked inhibitory deficiencies when processing negative material (Goeleven et al., 2006; Joormann and Gotlib, 2008). In most of these tasks, however, the main dependent variable is reaction time which does not provide a direct measure of attentional processes and is susceptible to alternative explanations. The measurement of eye-movements in visual attentional processing is becoming increasingly important (see Weierich et al., 2008, for a review). Eye-movements have the advantage of being distinguishable in terms of their temporal and spatial characteristics thus providing increased precision in understanding the
* Corresponding author at: Affective and Cognitive Neuroscience Lab, School of Psychology, Birkbeck University of London, Malet Street, London WC1E 7HX, UK. Tel.: +44 7968173484. E-mail address: [email protected] (N. Derakshan).
mechanisms of visual attentional processing. Caseras et al. (2007) measured eye-movements in dysphoric and non-dysphoric groups for negative and positive scenes that were paired with control (neutral) pictures. While the two groups did not differ in terms of orienting towards emotional pictures, relative to control pictures, the dysphorics had longer gaze durations on the negative pictures, indicating sustained attention for negative material. Thus eyemovements provided information on temporal characteristics of attentional processing that would not be obtainable through reaction times alone. Saccadic eye movement tasks can provide us with a precise assessment of some aspects of top-down cognitive control processes that influence attention allocation (Munoz and Everling, 2004; Ridderinkhof et al., 2004). In relation to attentional control, the antisaccade task (Hallet, 1978) offers a promising way forward. In this task participants are required to inhibit the reflexive tendency to look towards a sudden-onset cue, presented peripherally to one side of fixation, and generate a correct saccade to its mirror position as quickly as possible. Antisaccade performance involves competition between the reflexive saccade and voluntary initiation of the antisaccade, with errors occurring when activation in neural systems underlying the antisaccade cannot successfully compete with the prosaccade reflex (Massen, 2004; see Hutton and Ettinger, 2006, for a review). Recent work has used the antisaccade task to examine inhibitory control in anxiety (Derakshan et al., in press; Ansari et al., 2008; Hardin et al., 2007; Jazbec et al., 2006). There is also evidence from the antisaccade task on attentional control in depression (e.g., Sweeney et al., 1998; Jazbec et al.,
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2005). Sweeney et al. (1998) found that depressed participants made more reflexive errors in the antisaccade condition when the abrupt stimulus was an oval-shaped cue (for similar results see Jazbec et al., 2005). The neural structures involved in antisaccade performance show interesting overlap with the neural impairments observed in depression. Recent neuroimaging findings suggest the major involvement of prefrontal brain areas such as the dorsolateral prefrontal cortex (DLPFC) implicated in attentional control using the antisaccade task (Ettinger et al., 2008). Such areas are considered to have substantial involvements in the top-down regulation of emotional processing in anxiety and depression (Davidson et al., 2002; Bishop, 2007). We aimed to examine inhibition in relation to negative and positive emotional information, since depression has been associated both with enhanced attention and impaired inhibition for negative material (see Joormann et al., 2007) and reduced attention and processing deficiencies for positive information (e.g., Cavanagh and Geisler, 2006). To our knowledge, the present antisaccade study is the first to examine inhibitory control in relation to depression using facial expressions of emotion as stimuli. Using the standard anti- and prosaccade tasks (SA; SP) with stimuli comprising angry, happy and neutral facial expressions, we investigated the effects of subclinical depression (dysphoria) on attentional control processes. As this is the first study to investigate antisaccade performance in response to facial expressions of emotion a dysphoric sample was chosen to minimise possible impairments in antisaccade performance attributable to some cognitive deficits typically observed in clinically depressed individuals. We hypothesised that dysphorics, compared to non-dysphorics, would show impaired performance when the to-be-inhibited stimuli are emotional expressions and this would be evident in the standard antisaccade task where top-down attentional control is needed for the effective inhibition of reflexive prosaccades towards the emotional face. Impaired antisaccade performance can reflect deficits in inhibitory control and volitional saccade generation (Reuter et al., 2007). To allow investigation of both processes, in addition to the standard tasks we also administered delayed versions of the anti- and prosaccade tasks (DA; DP) (cf. Reuter et al., 2007). In delayed tasks the demand to inhibit an erroneous prosaccade is not simultaneous with the requirement to generate a volitional saccade. The isolation of the initiation of a volitional response means that the generation of the saccade takes place during the delay period, reducing the competition between stimulus-driven and top-down processes required for the inhibition of the prosaccade. We hypothesised that dysphoria would be associated with impaired inhibition but not impaired volitional saccade generation. 2. Method 2.1. Participants Participants were fifty-nine volunteers (42 female) from the University of London (for group characteristics see Section 3). They had normal or corrected to normal vision (wearing glasses or contact lenses when necessary) and normal hearing. Participants were not paid for their contribution to the experiment. Participants were treated in accordance with Birkbeck’s ethical code of conduct. Upon arriving at the laboratory and reading the relevant instruction sheet they signed a consent form and were given the opportunity to leave the experiment at any point without explanation. Upon completion of the experiment they were fully debriefed.
2.2. Materials and procedure 2.2.1. Self-report measure The Beck Depression Inventory-II (BDI-II) (Beck et al., 1996) was used to classify participants as dysphoric or non-dysphoric. This questionnaire consists of 21 items related to the occurrence of depressive symptoms over the past two weeks. Scores range from 0 to 63 with higher scores indicating higher depression severity. We followed the cut-off scores for dysphoria proposed by Beck et al. (1996; 14–19 mild, 20–28 moderate, and >29 severe) to classify participants. 2.2.2. Visual stimuli 18 faces (half female) depicting angry, happy and neutral facial expressions (6 of each valence) were taken from the Pictures of Facial Affect (Ekman and Friesen, 1976) and the NimStim Face Stimulus Set (Tottenham et al., 2002). Non-facial features were removed and faces were resized to 45 mm 70 mm (4.38 6.78) and presented in grayscale against a black background. The experiment involved four blocks (SA, SP, DA, DP) each comprising 90 trials, totalling 360 trials. Each block of 90 trials included 30 angry, 30 happy, and 30 neutral trials. For each of the angry, happy, and neutral facial expressions 6 faces were shown and each face was repeated 5 times per valence. The order of standard (A) and delayed (B) tasks was counterbalanced in an AB-BA design. The order of antisaccade and prosaccade tasks was counterbalanced within each of the standard and delayed tasks, with half of the participants randomly assigned to order of set SA, SP, DP, DA or set SP, SA, DA, DP and the other half to DA, DP, SP, SA, and DP, DA, SA, SP tasks. This ensured that the presentation of standard/delayed as well as anti- and prosaccade tasks was counterbalanced. A complete randomisation of tasks was not done in order to avoid large error variance due to very different temporal characteristics of the tasks. The inter-trial interval varied between 700 ms and 1300 ms. Each trial began with a central fixation cross (1.158 1.158) for 1600 ms. A face then appeared with equal probability to the left or right side of the cross at 118 (800 ms). A 440 Hz tone was presented (50 ms) simultaneously with, (on SA and SP trials) or 800 ms after, (on DA and DP trials) presentation of the face. Participants fixated the cross, then as soon as the face appeared, directed their gaze as quickly as possible away from the face, to its mirror position on the screen (SA) or towards the face (SP). In delayed tasks participants continued fixation and made an antisaccade (DA) or prosaccade (DP) when the tone sounded (Fig. 1a and b). 2.3. Eye-tracking Eye-movements were tracked using the LC Technologies ‘‘Eyegaze’’ system (LC Technologies, 2003), which uses the Pupil-Centre Corneal Reflection method (PCCR; Mason, 1969; Merchant and Morrisette, 1973). The gaze-point position is estimated at 60 Hz, with a typical root mean square error of less than 6.35 mm. Eye-movements were extracted using the R programming environment (Venables and Smith, 2005). Visual stimuli were presented on a 17 in. LCD (refresh rate of 16.6 ms) controlled by the DMDX programme (Forster and Forster, 2003), which ensures millisecond timing accuracy. 2.4. Procedure Participants were tested individually in a dimly lit room. Half completed the BDI-II before completing the task and half afterwards (with a distractor task in between to control for possible confounding effects). As questionnaires may prime a mood state that subsequently influences antisaccade performance, this
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Fig. 2. Percentage immediate errors (with standard errors) as a function of task (standard antisaccade, delayed antisaccade, and delayed prosaccade) and emotional expression of face (angry, happy, neutral) for each of the dysphoric and non-dysphoric groups.
to make these errors compatible in terms of temporal characteristics to errors in the antisaccade task (that are believed to be triggered by the stimulus). Accordingly, we took the average correct saccade latency in the standard prosaccade task plus two standard deviations of individual saccade latencies in this condition, as the upper limit for classifying erroneous prosaccades as immediate errors in the other tasks (see Reuter et al., 2007). For the purpose of statistical analyses, we considered the percentage of immediate errors and the mean latency of correct saccades (with latencies between 80 ms and 1000 ms after tone onset) in all tasks. 3. Results 3.1. Group characteristics
Fig. 1. (a) Example of an antisaccade trial with a happy emotional expression. (b) Example of a prosaccade trial with a happy emotional expression.
procedure allowed us to control for this. Participants were seated in front of the Eyegaze system at a distance of 60 cm with their chin on a chin-rest. 18 practice trials and calibration of the eye-tracker preceded each block and speed and accuracy were emphasised. The session lasted approximately 60 min. 2.5. Data preparation Saccades were defined on the basis of amplitude (>38) and velocity (>308/s) made after cue onset (presentation of face in standard blocks and tone in delayed blocks). Only the initial saccade was used to evaluate performance (Fischer et al., 1993). Anticipatory saccades (<80 ms of face onset) were removed from analyses. Consistent with Reuter et al. (2007) we defined errors and latencies in the following manner: In the SA, DA, and the DP tasks, errors (erroneous prosaccades) were defined as saccades that were directed towards the face and had a latency of greater than 80 ms after face onset. Inspection of the latencies of erroneous prosaccades in the delayed tasks and the standard antisaccade task revealed different distributions, suggesting that not all errors in the delayed tasks were triggered by the face. Accordingly, an upper limit was defined for error classification in the delayed tasks
Using the criteria proposed by Beck et al. (1996), 12 participants (11 female) with BDI-II scores >13 were classified as dysphoric (M = 20.25, SD = 9.18) and 12 participants (10 female) with BDI-II scores < 5 (M = 1.75, SD = 1.54), as non-dysphoric. They were matched for age (dysphorics: M = 32.5, SD = 5.99; non-dysphorics: M = 32.67, SD = 4.45, t < 1) and gender (x2 = .38, N.S.). No participant reported a medical history of depression or that they were being treated for depression or any anxiety-related disorder at the time of experiment. 3.2. Errors Fig. 2 shows the percentage of errors committed by both groups across tasks. To examine the effects of inhibition and volitional saccade generation on errors, a 3 3 2 Mixed ANOVA with Task (SA, DA, DP) and Valence of face (angry, happy, neutral) as within-subject factors and Group (dysphoric, non-dysphoric) as between-subject factor was conducted.1 In line with our 1 Consistent with Reuter et al. (2007) we did not include the SP condition in the analysis. Research has generally found that the percentage of errors in this task tends to be extremely low and negligible. In the current study, both dysphoric and non-dysphoric groups had negligible error rates in the SP task (dysphorics, M = .09%; non-dysphorics, M = 0%). There was no effect of Valence, F = 1, nor was there an interaction effect of Task Valence, F = 1. Our manipulations concentrated on the effects of inhibition vs. saccade generation processes (with prior inhibition), neither of which is measured by the SP task as there is no competition between reflexive and top-down processes in the SP task.
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hypotheses, we carried out Helmert contrasts on Task to examine the effect of delay (SA vs. DA and DP). Analysis found a significant main effect of Task, F(2,44) = 5.24, p < .01, with more errors in SA compared with DA and DP tasks, F(1,22) = 9.15, p < .007. This effect was qualified by an interaction with Group, F(2,44) = 3.25, p < .05, which indicated that the dysphoric group committed greater percentages of errors in the SA task than in the DA and DP tasks (16.5% vs. 6.3% and 9.2%) compared with the non-dysphoric group who showed no differences (10.8% vs. 9.6% and 9.8%), F(1,22) = 5.81, p < .03. Additional analyses showed that the two groups did not differ on the delayed antisaccade nor delayed prosaccade tasks (all Fs < 1). Collectively, these results indicated that while dysphorics and nondysphorics did not differ in terms of volitional saccade generation, they differed in inhibition, as evidenced by higher error rates in the SA task of dysphorics compared with non-dysphoric participants (see Fig. 2). Further analysis therefore concentrated on the SA task only. A 3 2 Mixed ANOVA with Valence (angry, happy, neutral) as within-subject factor and Group (dysphoric, non-dysphoric) as between-subject factor was performed. A main effect of Valence showed greater percentages of errors in response to emotional (14.8%) compared with neutral expressions (11.5%), F(2,44) = 3.1, p < .05; an effect that interacted with Group, F(2,44) = 4.12, p < .03. Dysphorics committed more errors in response to emotional than neutral stimuli (18.3% vs. 12.3%) an effect that was not evident in the non-dysphorics, (11.0% vs. 10.6%), F(1,22) = 4.36, p < .05. Polynomial contrasts showed that group differences were particularly pronounced in response to happy expressions (dysphorics: 21.0%; non-dysphorics: 10.0%), F(1,22) = 8.75, p < .008. 3.3. Latencies Mean correct saccade latencies are depicted in Fig. 3. A 4 3 2 mixed ANOVA, with Helmert contrasts on Task, was conducted with Task (SP, SA, DA, DP), Valence (angry, happy, neutral) and Group (dysphoric, non-dysphoric) as factors. There was a main effect of Task, F(3,66) = 16.10, p < .001, with faster saccades in SP compared with SA, DA and DP tasks, F(1,22) = 62.21, p < .001. No effects involving Valence, Task or Group were significant (Fs < 1).
Fig. 3. Mean correct saccade latencies (with standard errors) as a function of task (standard antisaccade, delayed antisaccade, and delayed prosaccade) and emotional expression of face (angry, happy, neutral) for each of the dysphoric and non-dysphoric groups.
4. Discussion We investigated inhibitory control in dysphoric and nondysphoric individuals using the antisaccade task. The main result was that the dysphoric group, compared with the non-dysphoric group, had higher error rates when stimuli were emotional expressions, particularly in response to happy facial expressions in the standard antisaccade task. This finding indicates that dysphoric individuals show impairments in inhibiting the impact of emotional faces, especially happy facial expressions of emotion. Delayed tasks involved a much lower error rate compared to the standard antisaccade task for all participants, across all facial expressions, indicating that the dysphoric and non-dysphoric groups did not differ in terms of volitional saccade generation, even when emotional faces were present. Correct antisaccade latencies were not influenced by emotional facial expressions, and there were no group differences across tasks: all participants had shorter latencies in the standard prosaccade compared with the antisaccade task, replicating previous findings (Reuter et al., 2007). The innovative feature of the current experiment is that it used a direct measure of attentional control to examine inhibitory processes in relation to emotional facial expressions in dysphoria. The finding of higher error rates in the standard antisaccade task in response to emotional expressions compared with neutral expressions in the dysphoric group is important, as it implicates dysfunctional inhibition in relation to emotional information in attentional control in dysphoria. It indicates that not only deficient inhibition of negative information (Caseras et al., 2007; Joormann et al., 2008), but also processing of positive information is affected in dysphoria. Our finding of higher error rates with happy emotional expressions in the dysphoric group is particularly interesting and deserves further investigation. A growing body of psychophysiological evidence has recently established that depressed individuals have reduced N2 amplitudes in response to happy faces in the right parietal cortex (Deldin et al., 2000), indicating deficits in processing happy faces. Similarly, Cavanagh and Geisler (2006) showed that depressed individuals had lower P3 amplitudes and longer P3 latencies when viewing happy faces, which indicated that depressed people allocate less attentional resources when processing happy faces and need longer to process them. Our results relating to errors made by the dysphoric group provide an interesting extension to these findings, showing that dysphoric individuals fail to exercise attentional control effectively when the to-be-inhibited stimuli are emotional, especially happy expressions. In an extension of these findings, our results showed no group difference in inhibitory processes when the to-beinhibited stimulus was a neutral face suggesting that salient emotional stimuli modulate inhibitory processes in dysphoria. One tentative explanation for the observed effects with happy faces is that the positive expression is unexpected and surprising to the dysphoric group. As depression is related to negative beliefs about the world, the self, and the future (Beck, 1967), the presentation of positive information could violate the expectations of the dysphoric individuals, causing enhanced errors. There is evidence from eye-movements (Caseras et al., 2007) as well as reaction times (Koster et al., 2005) to show that depression is associated with an attentional bias for negative material when presented for long durations indicating sustained processing of negative material in dysphoria. These results collectively support the view that attentional bias for salient emotional material can impair the efficient top down regulation of attentional control, especially under conditions when the inhibition of this material is needed for effective task performance (see Eysenck et al., 2007, for a review).
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There are a number of ways in which future research can address the limitations of the current investigation. Although the distribution of gender was balanced across groups the majority of the sample was female. Future research should include equal numbers of males and females and adopt a more stringent classification method to equate both groups in terms of demographic variables. Second, it is important to examine inhibitory impairments in response to a wider range of negative and positive material. We used angry facial expressions as they signal personal rejection thus having more personal relevance (Gilboa-Schechtman et al., 2004), but it is important to examine inhibitory processes in response to sad faces that also carry negative information congruent with depressed schemas. Third, there is a need to investigate the specific conditions leading to impaired inhibition of positive as well as negative material in clinical depression. Fourth, future research should include a condition to evaluate the mechanisms associated with voluntary initiation of a saccade; one that is free of any current or prior demand to suppress an erroneous prosaccade. The inclusion of this condition (especially in the context of clinical depression) would not only isolate any effects associated with inhibition, but would also be informative of the processes involved in volitional saccade generation, and maintenance of relationships between goals and action. In sum, the present study is the first to study inhibition of facial expressions of emotion using the antisaccade task. Our results distinctively add to previous antisaccade findings on inhibitory processes in dysphoria (e.g., Jazbec et al., 2005; Sweeney et al., 1998) by examining the modulatory role of emotional material in inhibitory processes. That is, in the present study inhibition involved ignoring irrelevant emotional information at the visual modality with only limited processing of emotional material. In view of the results presented it will be important to further elucidate the conditions that are associated with inhibitory deficits for negative and positive material. Acknowledgements This work was supported by a Royal Society International Joint Project Grant awarded to Nazanin Derakshan (ND) and Ernst Koster (EK). The research was carried out by Maureen Salt, under the supervision of ND and EK, at the Affective and Cognitive Neuroscience Lab at Birkbeck University of London. The authors would like to thank Tahereh L. Ansari and Leor Shoker for help with programming and data preparation. References Ansari, T.L., Derakshan, N., Richards, A., 2008. Effects of anxiety on task switching: evidence from the mixed antisaccade task. Cognitive, Affective, and Behavioural Neuroscience 8 (3), 229–238. Beck, A.T., 1967. Depression: Clinical, Experimental, and Theoretical Aspects. Hoeber, New York. Beck, A.T., Steer, R.A., Brown, G.K., 1996. Manual for the Beck Depression InventorySecond Edition (BDI-II). The Psychological Corporation, San Antonio, Texas. Bishop, S.J., 2007. Neurocognitive mechanisms of anxiety: an integrative account. Trends in Cognitive Sciences 11, 307–316. Caseras, X., Garner, M., Bradley, B.P., Mogg, K., 2007. Biases in visual orienting to negative and positive scenes in dysphoria: an eye movement study. Journal of Abnormal Psychology 116 (3), 491–497. Cavanagh, J., Geisler, M.W., 2006. Mood effects on the ERP processing of emotional intensity in faces: a P3 investigation with depressed students. International Journal of Psychophysiology 60 (1), 27–33. Davidson, R.J., Pizzagalli, D., Nitschke, J.B., Putnam, K., 2002. Depression: perspectives from affective neuroscience. Annual Review of Psychology 58, 259–289.
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