Neural Processing of Fearful Faces: Effects of Anxiety are Gated by Perceptual Capacity Limitations

Abstract

Debate continues as to the automaticity of the amygdala's response to threat. Accounts taking a strong automaticity line suggest that the amygdala's response to threat is both involuntary and independent of attentional resources. Building on these accounts, prominent models have suggested that anxiety modulates the output of an amygdala-based preattentive threat evaluation system. Here, we argue for a modification of these models. Functional magnetic resonance imaging data were collected while volunteers performed a letter search task of high or low perceptual load superimposed on fearful or neutral face distractors. Neither high- nor low-anxious volunteers showed an increased amygdala response to threat distractors under high perceptual load, contrary to a strong automaticity account of amygdala function. Under low perceptual load, elevated state anxiety was associated with a heightened response to threat distractors in the amygdala and superior temporal sulcus, whereas individuals high in trait anxiety showed a reduced prefrontal response to these stimuli, consistent with weakened recruitment of control mechanisms used to prevent the further processing of salient distractors. These findings suggest that anxiety modulates processing subsequent to competition for perceptual processing resources, with state and trait anxiety having distinguishable influences upon the neural mechanisms underlying threat evaluation and "top-down" control.

Visual Attention Modulates Brain Activation to Angry Voices

“…Generally, our data are in accordance with findings from the visual modality showing the limitation of automatic brain responses to visual threat (Pessoa et al, 2002;Bishop et al, 2007). In these studies, the variation of perceptual load by means of a demanding task, which is presented either peripheral (Pessoa et al, 2002) or central (Bishop et al, 2007) to fixation, led to the exhaustion of processing capacity. However, in contrast to these studies, our results cannot be explained by effects of task difficulty per se.…”

“…Amygdalar responses were found even when subjects' attention was distracted from facial expressions (Vuilleumier et al, 2001) or when the presentation of the stimuli was below the threshold of conscious perception (Whalen et al, 2004), supporting the hypothesis of a crucial role of the amygdala in the automatic detection of threat (LeDoux, 1996). However, the assumption of completely automatic amygdalar responses to visual threat was questioned by findings showing the absence of activation in the amygdala and visual areas to threat-related visual stimuli during exhaustion of attentional resources (Pessoa et al, 2002;Bishop et al, 2007;Straube et al, 2007) or when controlling for perceptual (Straube et al, 2010) or experimental artifacts (Pessoa et al, 2005).…”

Emotional Automaticity Is a Matter of Timing

“…Early findings of automatic amygdala activity that was not reduced by reduced attention were thought to reflect activity via this subcortical route (Vuilleumier et al, 2001;Anderson et al, 2003). Later fMRI work, however, indicated that increased attention to nonemotional stimulus features did significantly reduce the amygdala's response to emotional stimulus features (e.g., Pessoa et al, 2002;Bishop et al, 2007;Blair et al, 2007;Mitchell et al, 2008;Pessoa, 2009). It is possible that the early amygdala activity seen in the current study that was independent of attentional modulation was a result of stimulation of the amygdala via the subcortical route.…”

“…It has been proposed that these dual routes are present in humans too, and because of the existence of the subcortical route, the amygdala's response to emotional stimuli is largely automatic and can occur independently of attention (de Gelder et al, 2003;Vuilleumier et al, 2003;Whalen et al, 2004; for review, see Dolan and Vuilleumier, 2003;Johnson, 2005). Others have suggested that it is unlikely that representations of emotional stimuli are independent of representational competition and that increased attention to nonemotional stimulus features should significantly reduce the amygdala's response to emotional stimulus features (Pessoa et al, 2002;Bishop et al, 2007;Blair et al, 2007;Mitchell et al, 2008;Pessoa, 2009; for review, see Pessoa and Ungerleider, 2004). It is possible, however, that this debate has been fostered by the limited temporal resolution of blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) data.…”

Anxiety in old age and dementia - implications for clinical and research practice

“…Research evidence indicates that some aspects of attention-related function can be influenced and modulated by anxiety [12,47,[99][100][101]. These include attentional narrowing [100], selective attention, attentional control [7,102], inhibition, alerting, orienting and attentional resource allocation [7,15,[102][103][104][105][106][107][108][109][110][111][112][113][114][115][116][117], pre-attentive change detection, sensory processing, contrast sensitivity involved in low level visual processing, processing speed, increased processing of task-irrelevant information [106,[118][119][120][121][122][123] and selective attention bias in relation to threat-relevant information [108][109][110]120,122,123], and which in some cases, is related to state or trait anxiety [114].…”