Attentional bias for valenced stimuli as a function of personality in the dot-probe task

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1 Journal of Research in Personality 38 (2004) JOURNAL OF RESEARCH IN PERSONALITY Attentional bias for valenced stimuli as a function of personality in the dot-probe task Zenab Amin, a R. Todd Constable, b and Turhan Canli a, * a Department of Psychology, State University of New York at Stony Brook, Stony Brook, NY, USA b Yale University School of Medicine, Yale MRRC, New Haven, CT, USA Abstract Extroversion (E) and neuroticism (N) are associated with positive and negative affect, respectively. This correspondence between each dimension of personality with each dimension of affect may reflect a common mechanism, such as attentional bias to emotional stimuli. We used functional magnetic resonance imaging (fmri) while participants were engaged in an attentional task to identify brain regions that may be involved in attentional bias as a function of E or N. By adapting, for the first time, the dot-probe attentional task for use in the scanner, we discovered that activation in the fusiform gyrus is significantly correlated with E. The greatest activation was observed in conditions in which an attentional probe was placed in a section of the visual field least likely to be attended to by highly extroverted individuals. This activation may reflect increased effort related to visual search, autonomic arousal, or detection of an unexpected occurrence. Ó 2003 Elsevier Inc. All rights reserved. 1. Introduction A long-standing debate in personality psychology has revolved around the usefulness of trait terms in explaining human behavior. Even some proponents of the trait view acknowledge that a model such as the Big Five provides an account of personality that is primarily descriptive rather than explanatory (John & Srivastava, 1999). A more explanatory account may require the integration of the trait view with a processing-oriented approach (Mischel & Shoda, 1998). For example, the association between neuroticism (N) and negative emotional experience, or between * Corresponding author. Fax: address: turhan.canli@sunysb.edu (T. Canli) /$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi: /j.jrp

2 16 Z. Amin et al. / Journal of Research in Personality 38 (2004) extroversion (E) and positive emotional experience (Costa & McCrae, 1980), might be partially explained by attentional biases in response to valenced stimuli. Indeed, trait-anxious individuals exhibit an attentional bias towards negative stimuli (Richards, French, Johnson, Naparstek, & Williams, 1992), whereas extroverted individuals exhibit attentional bias towards positive stimuli (Derryberry & Reed, 1994). Canli (in press) argued that a contemporary form of personality neuroscience can integrate trait and processing views of personality by identifying neural systems, in the intact and healthy human brain, that respond to stimuli from the environment but also exhibit cognitive processing biases consistent with human behavioral dispositions. These biases may be expressed across different psychological domains, such as perception, memory, or attention. Using experimental paradigms borrowed from cognitive psychology and cognitive neuroscience, the neural systems subserving these domains should be accessible to study by neuroscientists. Data from neuroimaging studies demonstrate an association between brain activation and N and E. For example, a positron emission tomography (PET) study reported cerebral blood flow differences in subcortical brain structures as a function of E, as participants passively watched a neutral video film clip (Fischer, Wik, & Fredrikson, 1997). A study using functional magnetic resonance imaging (fmri) reported significant correlations between N, E, and brain activation to negative and positive emotional scenes, respectively (Canli et al., 2001). Yet, the psychological processes associated with these brain activations are unknown, because both studies used passive viewing tasks that were cognitively unconstrained and could have engaged a number of different mental processes, such as perception, memory encoding, autobiographical recall, or attention. To our knowledge, only one neuroimaging study has used a cognitive-affectively constrained task to relate brain activation during the perception of emotional faces to E (Canli, Sivers, Whitfield, Gotlib, & Gabrieli, 2002). Other domains of cognitive-affective processing, such as attention to valenced stimuli, remain to be investigated. One test of attentional bias is the dot-probe task. The participantõs task is to respond to a probe stimulus that is initially hidden from view behind one of two stimuli, but revealed when both stimuli disappear. A fast reaction time (RT) suggests that attention has been directed at the stimulus that obscured the probe, whereas a slow RT suggests that attention has been drawn away from the stimulus that obscured the probe. When negative stimuli were presented to anxious and depressed participants, they exhibited more delayed RTs relative to controls, suggesting attentional bias towards negative stimuli (Mogg, Bradley, & Williams, 1995). In this study, we used fmri to identify brain regions that are activated by the dotprobe task as a function of participantsõ self-reported levels of N and E. Because the dot-probe task has never been used in a neuroimaging study, no specific set of brain structures associated with this task is unknown. However, other tasks that involve attention to emotional stimuli give us some guidance about a priori regions of interest. For example, the amygdala has also been implicated in vigilance (Davis & Whalen, 2001), a state that requires a high degree of attention. Another region involved in attention to emotional stimuli is the anterior cingulate, according to an imaging study that used a variant of the Stroop attention task (Whalen et al., 1998).

3 Z. Amin et al. / Journal of Research in Personality 38 (2004) Both of these regions have also been associated with E (Canli et al., 2001; Canli et al., 2002). Finally, we were interested in the posterior fusiform region, which has been implicated in visual attention (Donner et al., 2000), autonomic arousal (Critchley, Elliott, Mathias, & Dolan, 2000), and the processing of complex social stimuli (Geday, Gjedde, Boldsen, & Kupers, 2003). We expected that E would be associated with individual differences in the processing of picture pairs that contain a positive image in these or associated brain regions. We expected a similar relationship for N and picture pairs that contain a negative image. 2. Methods 2.1. Participants Eleven right-handed individuals (seven males; mean age ¼ 23.2, SD ¼ 3:5) participated in the fmri study, with behavioral RT data available for eight participants. All participants completed the NEO-Five Factor Inventory (NEO-FFI) and T scores were obtained by conversion of participantsõ raw scores according to the conversion table supplied with the NEO-FFI, with the population mean defined as T ¼ 50 and one standard deviation of T ¼ 10 (Costa & McCrae, 1992). Mean T scores were 50.5 (SD ¼ 9:4, range: 34 70) for N and 51.5 (SD ¼ 10:4, range: 38 67) for E. The correlation between these two scales was r ¼ :43. Participants were students of Stony Brook University or Yale University, without any known psychiatric or neurological illness who gave informed consent. All procedures were approved by the institutional review boards of both universities Behavioral procedures The dot-probe task was created using the E-Prime stimulus presentation program (Psychology Software Tools, Pittsburgh, PA). Seventy-two pairs of pictures were presented on a vertical axis on the screen in a block design. All stimuli were selected from a normed picture library (Lang, Bradley, & Cuthbert, 2001) that contained valence ratings on a scale from 1 to 9 (negative positive) and included positive ( pos ; valence range: 7 9), neutral ( neut ; valence range: 4 6), and negative ( neg ; valence range: <3) images. Twenty-four pairs each of neg/neut, pos/neut, and neut/neut were presented. The dot-probe which immediately followed presentation of neg/neut or pos/neut pairs either appeared where the neutral stimulus had appeared (neutral match or NM) or matched the location of the emotional stimulus (emotion match or EM). For neut/neut pairs, the dot appeared with equal frequencies on both halves of the screen. Thus, there were five conditions presented in separate blocks: pos/neut EM and NM, neg/neut EM and NM, and neut/neut. The placement on top or bottom of the screen and the match with either the neutral or emotional item were counterbalanced across two scans conducted during the same scan session, so that each of the 72 pairs was presented four times, for a total of 288 trials. The order of blocks in scan 1 was Neut-NegD-PosF-Neut-NegF-PosD (repeated three times) and for scan 2

4 18 Z. Amin et al. / Journal of Research in Personality 38 (2004) was Neut-NegF-PosD-Neut-NegD-PosF (repeated three times). Each block included eight trials that were 3 s long each. Within each trial, the stimulus pair was presented for 1000 ms, the probe was presented for 1000 ms, and a fixation cross was presented for 1000 ms. Participants were instructed to respond by button press as quickly as possible with the location of the dot Imaging procedures Imaging data were acquired in a 1.5 T GE Signa LX scanner (General Electric, Fairfield, CT). For structural whole brain images, a three-dimensional high resolution spoiled gradient (SPGR) scan was conducted, along with a scan of 35 T1 images (3.5 mm thickness) oriented parallel to the line between the anterior and posterior commissure. For functional images, an echoplanar imaging (EPI) scan was conducted with a flip angle of 80, repetition time (TR) ¼ 3 s, echo time (TE) ¼ 45 ms, and a field of view (FOV) ¼ cm. Functional data were preprocessed and analyzed using SPM2 (Wellcome Department of Cognitive Neurology). Statistical analysis of functional data was based on fixed-effects models (Friston, 1994) at the individual subject level of analysis and random effects models (Holmes & Friston, 1998) for group-level analyses. Contrast images were constructed within each emotion condition, so that pos/neut EM blocks were contrasted with pos/neut NM blocks and neg/neut EM blocks were contrasted with neg/neut NM blocks. Thus, the nature of the stimuli (pos/neut and neg/neut, respectively) is identical across both conditions of the contrast, leaving only the placement of the attentional probe (obscured by either the emotional or neutral image) to differ. Contrasts were then correlated across subjects with participantsõ scores for E and N, using multiple regression analyses with one personality variable partialed out. Multiple regression analysis was chosen to control for common method variance 1 and because there was a substantial correlation between E and N (r ¼ :43). The significance level was set at p <:001 (uncorrected) and the extent threshold was set at 20 voxels. This is a more stringent standard than the significance threshold of p <:001 and the 4-pixel cluster-size constraint thought to be an adequate correction for multiple comparisons (Forman et al., 1995). All coordinates reported here represent Talairach (Talairach & Tournoux, 1988), as opposed to MNI, space. 3. Results 3.1. Behavioral data Table 1 shows RTs (excluding incorrect responses or RTs greater than three SDs from a participantõs mean) for all four emotion conditions, normalized relative to the 1 Simple correlations were also performed and yielded similar, but weaker results, likely due to inclusion of irrelevant method variance (such as social desirability tendencies in answering questions) that is suppressed in the multiple regression analysis.

5 Z. Amin et al. / Journal of Research in Personality 38 (2004) Table 1 Correlations between personality and normalized reaction times Variable N E M SD Positive EM ).43 ) Positive NM ).14 ).35 ) Negative EM Negative NM ).25 ) * p <:05. (one-tailed). neut/neut condition, and partial correlations with participantsõ E and N scores. A significant negative relationship was found between E and normalized reaction time to the negative NM block (r ¼ :72, p <:05, one-tailed), showing faster reaction time when a probe matched a neutral stimulus in a neg/neut pair than in the neut/ neut condition fmri data Table 2 lists clusters where E was significantly (p <:001) correlated with brain activation to pos/neut and neg/neut NM versus EM conditions. For pos/neut stimulus presentations, there was significantly greater activation, as a function of E, in the right fusiform gyrus and in the left middle frontal gyrus and cerebellum when the probe was obscured by the neutral stimulus than when it was obscured by the positive stimulus. For neg/neut stimulus presentations, there was significantly greater activation, as a function of E, in the right fusiform gyrus when the probe was obscured by the negative stimulus than when it was obscured by the neutral stimulus. Fig. 1 illustrates the location of clusters located in the fusiform gyrus and corresponding scatterplots of brain activation as a function of E. There were no regions where N was significantly correlated at the chosen significance thresholds with brain activation based on neg/neut or pos/neut contrasts. Table 2 Loci of brain reactivity correlating with E Location Coordinates Cluster size in voxels Z x y z Correlation with increased brain activation in positive NM condition (relative to positive EM condition) Right fusiform gyrus +42 )57 ) Left middle frontal gyrus ) Left cerebellum )4 )42 ) Correlation with increased brain activation in negative EM condition (relative to negative NM condition) Right fusiform gyrus +48 )47 ) Note. Regions are identified by name of location and coordinates in the brain atlas of Talairach and Tournoux (1988). x, distance in millimeters to the right (+) or left ()) of midline; y, distance anterior (+) or posterior ()) to the anterior commissure; and z, distance superior (+) or inferior ()) to a horizontal plane through the anterior and posterior commissures.

6 20 Z. Amin et al. / Journal of Research in Personality 38 (2004) Fig. 1. Correlations between E and brain activation in the right fusiform gyrus when comparing EM and NM conditions. The positive correlation in A signifies greater reactivity in the positive NM compared to EM condition with higher extroversion scores. The positive correlation in B signifies greater reactivity in the negative EM compared to NM condition with higher extroversion scores. L/R, left/right. 4. Discussion This is the first brain imaging study to use the dot-probe task and the first to relate brain activation during performance of this task to personality traits. Our analyses controlled for the presence of affective stimuli by utilizing contrasts that only differed in the placement of the attention probe, as it was obscured either by the emotional or neutral item of a stimulus pair. We used a multiple regression approach to identify brain activation that was uniquely associated with either E or N. Using these methods, we discovered a significant correlation between E and activation primarily in the right fusiform gyrus when the attention probe was either obscured by the neutral item of a pos/neut pair, or by the negative item of a neg/ neut pair. 2 2 Activations in other a priori regions of interest, namely the anterior cingulate and amygdala, did not correlate significantly with E or N under the chosen criterion of statistical significance (p <:001). However, when the significance threshold was reduced to p <:01, significant correlations did emerge. For example, E was associated with greater anterior cingulate and amygdala activation when the probe was obscured by the positive item of a pos/neut pair. N was associated with anterior cingulate activation when the probe was obscured by the negative item of a neg/neut pair.

7 Z. Amin et al. / Journal of Research in Personality 38 (2004) The interpretation of these neuroimaging data is aided by the behavioral observation that participants scoring high in E exhibited significantly faster RTs when the probe was placed behind the neutral than the negative stimulus, suggesting that their attention was drawn away from the negative item of neg/neut pairs. This pattern of responding is consistent with other reports that healthy, compared to depressed, individuals direct attention away from negative stimuli (McCabe, Gotlib, & Martin, 2000). With empirical behavioral data suggesting that E is associated with a shift of attention away from negative stimuli, it is striking that fusiform activation was correlated with E when the probe was located behind the negative item of a neg/neut pair, i.e., the location least likely to be attended to by highly extroverted participants. Individuals who score high in E would therefore be expected to expend more effort searching for the attention probe than participants who score lower on E. Thus, we interpret the observed fusiform activation as an index of increased effort during visual search. Consistent with this view of fusiform function, Donner and colleagues reported right fusiform activation in four out of five participants during a complex visual search task (Donner et al., 2000). The only other condition in which fusiform activation was correlated with E was when the probe was located behind the neutral item of a pos/neut pair. Although our behavioral data did not reveal a processing bias (perhaps due to lacking statistical power), other data demonstrate that highly extroverted individuals are slow to shift attention away from locations of positive incentive value (Derryberry & Reed, 1994). Thus, fusiform activation as a function of E was again associated with a condition where the probe was placed in the location less likely to be attended to by highly extroverted participants and consequently requiring greater effort in visual search. Other interpretations of fusiform activation associated with E are plausible. For example, efforts by highly extroverted individuals to keep attention away from negative stimuli may lead to increased autonomic arousal, which has been associated with right fusiform gyrus activation (Critchley et al., 2000). Fusiform activation may also represent response to an unexpected event (i.e., presentation of the probe in the location that was not attended to), consistent with a study by Strange and colleagues that found increased fusiform activation during the detection of oddball stimuli, i.e., stimuli that deviated from an expected rule (Strange, Henson, Friston, & Dolan, 2000). The absence of correlations associated with N may reflect lacking statistical power to exceed a conservative threshold of significance. A conservative threshold (p <:001) was chosen to minimize the false positive rate, since this study was using a novel task. At a lower threshold, significant correlations related to N did indeed emerge (see Footnote 2). Thus, rather than denying any association between N and brain activation during the dot-probe task, it is more appropriate to characterize this association as less robust than for E. A possible reason is the distribution of N scores in our sample, which was somewhat unusual (five of eleven participants scored identical in N). In the absence of direct verification of eye gaze, we cannot state with certainty that the observed correlation between fusiform activation and E represents attentional

8 22 Z. Amin et al. / Journal of Research in Personality 38 (2004) bias. Nonetheless, we presented converging behavioral and neuroimaging evidence that E is associated with differential responding to negative and positive stimuli in a manner that engages the fusiform gyrus. The observed activation pattern is consistent with an extroverted behavioral profile that is attracted to positive and avoidant of negative emotional stimuli. Future work will require additional measures such as eye tracking and measures of autonomic arousal, along with fmri, to define the role of the right fusiform gyrus in extroversion more clearly. Acknowledgments This study was funded by SUNY Stony Brook and by NSF Grant BCS References Canli, T. (in press). Functional brain mapping of extraversion and neuroticism: Learning from individual differences in emotion processing. Journal of Personality. Canli, T., Sivers, H., Whitfield, S. L., Gotlib, I. H., & Gabrieli, J. D. (2002). Amygdala response to happy faces as a function of extraversion. Science, 296(5576), Canli, T., Zhao, Z., Desmond, J. E., Kang, E., Gross, J., & Gabrieli, J. D. E. (2001). An fmri study of personality influences on brain reactivity to emotional stimuli. Behavioral Neuroscience, 115(1), Costa, P. T., Jr., & McCrae, R. R. (1980). Influence of extraversion and neuroticism on subjective wellbeing: Happy and unhappy people. Journal of Personality and Social Psychology, 38, Costa, P. T., & McCrae, R. R. (1992). Professional manual of the revised NEO personality inventory and NEO five-factor inventory. Odessa, FL: PAR Inc. Critchley, H. D., Elliott, R., Mathias, C. J., & Dolan, R. J. (2000). Neural activity relating to generation and representation of galvanic skin conductance responses: A functional magnetic resonance imaging study. The Journal of Neuroscience, 20(8), Davis, M., & Whalen, P. J. (2001). The amygdala: Vigilance and emotion. Molecular Psychiatry, 6(1), Derryberry, D., & Reed, M. A. (1994). Temperament and attention: Orienting towards and away from positive and negative signals. Journal of Personality and Social Psychology, 66, Donner, T., Kettermann, A., Diesch, E., Ostendorf, F., Villringer, A., & Brandt, S. A. (2000). Involvement of the human frontal eye field and multiple parietal areas in covert visual selection during conjunctive search. European Journal of Neuroscience, 12, Fischer, H., Wik, G., & Fredrikson, M. (1997). Extraversion, neuroticism and brain function: A pet study of personality. Personality and Individual Differences, 23(2), Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fmri): Use of a clustersize threshold. Magnetic Resonance in Medicine, 33, Friston, K. J. (1994). Statistical parametric mapping. In R. Thatcher (Ed.), Functional neuroimaging: Technical foundations (pp ). San Diego, CA: Academic Press. Geday, J., Gjedde, A., Boldsen, A., & Kupers, R. (2003). Emotional valence modulates activity in the posterior fusiform gyrus and inferior medial prefrontal cortex in social perception. Neuroimage, 18, Holmes, A. P., & Friston, K. J. (1998). Generalisability, random effects and population inference. Neuroimage, 7, S754. John, O. P., & Srivastava, S. (1999). The big five trait taxonomy: History, measurement, and theoretical perspectives. In L. A. Pervin & O. P. John (Eds.), Handbook of personality: Theory and research (2nd ed., pp ). New York: The Guilford Press.

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