The goal of the present study was to investigate attentional biases in SAD during a dot-probe task using ERP and source localization techniques. Several findings relevant to the initial hypotheses emerged. First, SAD, but not control, participants showed increased P1 amplitudes and FG activation to angry-neutral vs. happy-neutral face-pairs, and a reliable Emotion × Group interaction indicated that SAD participants had a significantly larger P1 potentiation to angry faces relative to happy faces compared to control participants. Second, SAD participants had smaller P1 amplitudes to probes replacing emotional rather than neutral faces, whereas control participants showed an opposite pattern. A significant Probe-Position × Group interaction indicated that SAD participants had significantly reduced P1 responses to probes replacing emotional vs. neutral faces compared to control participants. Third, SAD participants reacted faster to probes replacing angry vs. happy faces, although no group differences emerged from the RT data. Finally, SAD, but not control, participants showed higher sensitivity (d′ values) in response to probes following the presentation of angry versus happy faces.
Previous studies have shown that the P1 component is amplified in response to negatively valenced facial expressions (Streit et al. 2003
; Klucharev & Sams, 2004
; Pourtois et al. 2005
) and that increased P1 to threat-related cues is larger for high compared to low trait anxious individuals (Li et al. 2008
; see also Kolassa & Miltner, 2006
). Similar to P1 enhancements due to heightened attention in studies with non-emotional stimuli (Hillyard & Anllo-Vento, 1998
), P1 enhancements to threat-stimuli were found to originate from extrastriate generators (e.g. FG) (Pourtois et al. 2005
) and have therefore been assumed to indicate increased attention to threat (Vuilleumier & Pourtois, 2007
). In SAD participants, the finding of enhanced P1 amplitudes when an angry face was present might thus indicate initial hypervigilance to threat and mirrors (a) the reaction time data suggesting shorter reaction times to probes replacing angry than happy faces and (b) the increased visual sensitivity following angry versus happy faces. Analyses of d
′ values indeed revealed that SAD participants were characterized by an increased visual sensitivity in both visual fields after the presentation of an angry face. Moreover, reaction times were shortened at locations cued by an angry face. Interestingly, SAD participants also reacted faster to probes preceded by neutral versus happy faces. When seen within the framework of prior findings indicating that SAD participants show increased activation relative to controls in anxiety-related brain regions in response to both neutral (Cooney et al. 2006
) and angry (Straube et al. 2004
) faces, the present ERP and behavioral findings converge in suggesting that in SAD, attention is initially oriented toward the relatively more threatening cue in the environment. These results are consistent with the cognitive model of SAD (Clark & Wells, 1995
; Rapee & Heimberg, 1997
; Hofmann, 2007
In the present study, source localization analyses indicated that potentiated P1 responses to angry vs. happy face-pairs were associated with hyperactivation in the posterior FG. FG activation within the P1 time range has been reported in healthy controls in response to aversive stimuli (Pizzagalli et al. 2003
; Streit et al. 2003
). Moreover, P1 amplitudes have been associated with changes in posterior FG activation measured with positron emission tomography (Mangun et al. 1998
). Importantly, the FG receives direct projections from the amygdala (Amaral et al. 1992
), which has been found to (a) respond to facial stimuli as early as 120 ms after presentation (Halgren et al. 1994
); (b) be sensitive to threat-related cues (Buchel & Dolan, 2000
); and (c) be implicated in the pathophysiology of SAD (Etkin & Wager, 2007
). Based on the convergence of these findings, we speculate that the P1 finding of hypervigilance to angry faces might be linked to increased amygdalar activation in SAD.
Extending prior fMRI findings highlighting FG hyperactivation in SAD (Etkin & Wager, 2007
), the present results provide important insight into the temporal dynamics of brain mechanisms associated with early attentional biases in SAD. Specifically, we showed that functional abnormalities within the visual cortex unfold as early as 100 ms after stimulus presentation. ERP techniques cannot be used, however, to ascertain whether this potentiated activation reflects top-down influences from the fronto-parietal network or direct influences from the amygdala (Vuilleumier & Pourtois, 2007
). Consequently, future studies that combine ERP and hemodynamic measurements in SAD should further investigate this important issue.
In contrast to the face-evoked P1 findings, this study also found evidence that individuals with SAD might show at later stages of the information processing flow reduced visual processing at emotionally cued locations. In SAD participants, probes replacing angry and happy faces in fact elicited smaller P1 amplitudes than probes replacing neutral faces. Control participants showed the opposite pattern. 5
Similarly, Santesso et al. (2008)
showed that non-anxious adults exhibited larger P1s to emotionally vs. neutrally cued probes, but only following angry faces.
At least two interpretations for the P1-Probe effect in SAD can be advanced. First, it is possible that visual processing of the probes was disrupted by continuing processing of preceding emotional faces (Rossignol et al. 2007
), resulting in smaller P1 amplitudes. Although plausible, this interpretation cannot explain the finding of increased
amplitudes to emotionally cued probes in control participants. An alternative explanation is that SAD participants either attended the more ambiguous stimulus present in the visual field (i.e., the neutral face) (Cooney et al. 2006
) or showed attentional avoidance away from emotional faces (Mansell et al. 1999
) at later stages of the information processing flow. If the latter is true, it remains to be tested whether attentional avoidance in SAD participants might occur automatically or might be controlled by strategic influences (Amir et al. 1998
). Regardless of the mechanisms, it is interesting to note that SAD participants showed significantly reduced overall face-locked C1 and N170 amplitudes relative to controls. This finding is consistent with the hypotheses that certain aspects of face processing might be avoided (Chen et al. 2002
) or disrupted (e.g. Horley et al. 2004
) in SAD (we note, however, that in contrast to P1, the C1 and N170 group differences were not modulated by emotions).
Similar to our previous study (Santesso et al. 2008
), LORETA analyses of probe-evoked ERPs did not reveal differential activation in brain regions typically associated with attention-related P1-effects (i.e., extrastriate visual areas) (Mangun et al. 1998
). A possible explanation is that differences between neutrally and emotionally cued probes emerging at the scalp level were not strong enough to reach statistical significance in the LORETA analyses, which used a higher statistical threshold and might be affected by additional sources of variance (e.g., assumption of a spherical head, issues with the inverse problem). However, it should be emphasized that the P1 effect to the probe was right-lateralized, replicating prior findings (Pourtois et al. 2004
). Similarly, the P1 to the face was also more pronounced in the right hemisphere, in line with a substantial literature emphasizing right hemisphere dominance for face processing (Adolphs, 2002
The limitations of the present study should be acknowledged. First, although ERP analyses provided evidence for abnormal attentional processes in SAD participants, no group differences emerged for RT data. This may be due to our relatively small sample size, which represents one of the main limitations of this study, and/or to the specific characteristics of our paradigm, particularly the chosen stimulus-onset asynchronies and its go/no-go component. Unlike classic dot-probe studies in which a behavioral response is required on each trial, our participants had to withhold responses on no-go trials, possibly introducing novel sources of variance (e.g. decision-making, inhibition of motor-responses). Moreover, by design, ERP waveforms were derived exclusively from no-go trials to avoid potential contamination of movement artefacts to early ERP components (e.g., C1), whereas RT data were assessed during go trials. Thus, although this particular version of the dot-probe paradigm has been found to induce reliable ERP correlates of attentional biases in two independent control samples (e.g., Pourtois et al. 2004
; Santesso et al. 2008
), the integration of RT and ERP data is suboptimal.
An alternative explanation for the lack of group RT differences may be reduced power for the behavioral analyses, particularly since only 30% of the trials (i.e., go trials) could be used for behavioral analyses. Nevertheless, separate analyses for each group revealed that SAD - but not control - participants did react significantly faster to probes cued by angry as opposed to happy or neutral faces (“within-subjects bias”; Bar-Haim et al. 2007
A final limitation of the present study arises from presenting probes with random interstimulus intervals (100–300 ms). Even though this technique reduces overlap from early and later ERP components, it also prevents a precise delineation of the time course of attentional effects. In order to better understand the temporal unfolding of attentional biases in SAD, ERP studies using both short (e.g., 100 ms) and long (e.g., 500 ms) stimulus-onset asynchronies in the same participants will be required.
Notwithstanding these limitations, the present study suggests that for participants with SAD, early (possibly amygdala-related) threat detection may trigger increased activation in visual areas (including the FG) leading to rapid hypervigilance, which was reflected in potentiated P1 responses, increased accuracy, and shortened RTs to angry faces. In addition to this initial hypervigilance, SAD participants were characterized by reduced visual processing of emotionally cued locations during the P1-Probe time-window. When seen within the framework of other studies (e.g. Amir et al. 1998
; Vassilopoulos, 2005
; Garner et al. 2006
), the present ERP findings suggest the presence of a hypervigilant-avoidant pattern of attention in SAD. We recommend that future studies examine whether these ERP findings extend to emotional expressions of varying degrees and valences, and/or to other anxiety disorders in order to clarify how hypervigilance and avoidance play a role in the maintenance of these disorders and their potential cognitive treatments.