In the present study, 7-month-old infants took considerably longer to disengage their attention from centrally presented fearful faces as compared to happy and neutral faces, and fearful eyes alone, in order to shift their attention to a peripheral target. This result is similar to what has been observed in adults (Georgiou et al., 2005
) and it extends our previous study (Peltola et al., 2008
) which showed that 7-month-olds displayed a relatively stronger tendency to remain fixated on fearful than happy faces and control stimuli. The findings are also in line with previous research showing that infants start to allocate attention differentially to fearful vs. happy faces by the age of 7 months as studied by looking time and ERP measures (e.g., Leppänen et al., 2007
; Peltola et al., in press
Why should one expect relatively longer disengagement latencies from threat-related stimuli? Functionally, the stronger holding of attention may be considered a way to attain processing priority for emotionally significant stimuli and to enable a more detailed analysis of the source of the potential threat. A substantial delay in the disengagement process, however, may result in dwelling on threat-related stimuli and feelings of anxiety (Fox, Russo, Bowles, & Dutton, 2001
). Moreover, a fearful face in particular can be considered an ambiguous stimulus that calls for extended processing in order to derive its communicative intent (Whalen, 1998
). The ambiguity of the fearful faces used in the present study was obviously heightened by the fact that as the fearful faces gazed directly at the observer, they did not provide explicit information about the source of the potential threat as a face with an averted gaze might do.
The neural mechanisms underlying the modulation of disengagement by threat-related stimuli are currently not known. However, the amygdala is considered as the key neural structure in mediating the influence of emotional stimuli on attentional processing, mainly by producing transient increases in perceptual responsivity for stimuli tagged as emotionally significant (Phelps, 2006
). These enhanced sensory representations may act to bias attentional selection in favor of emotional stimuli when there is a competition of attentional resources (Vuilleumier, 2005
). In addition to amplifying extrastriate visual responses, threat-related stimuli may also result in transient suppression of neural activity in parietal areas associated with shifts of attention, thereby producing temporarily lower responsiveness to competing stimuli (Pourtois, Schwartz, Seghier, Lazeyras, & Vuilleumier, 2006
). Naturally, as we do not know the developmental time course of amygdala maturation, its structural and functional connectivity with mechanisms implicated in emotion processing (e.g., orbitofrontal and anterior cingulate cortices) and visual processing of faces (inferotemporal cortex), or the role of the amygdala in emotional face perception in human infants, caution should be warranted in relating the adult model of emotional attention (Vuilleumier, 2005
) to early development.
The present findings indicate that infants’ stronger attentional responses to fearful faces can not be interpreted simply as responses to enlarged fearful eyes. Consistent with previous data (e.g., Adolphs et al., 2005
), results from our scanning task showed that infants focused primarily on the eye region of all faces, however, this bias was not strengthened in response to fearful faces or neutral faces with fearful eyes. In the overlap task, the latency to disengage attention from the neutral face with fearful eyes was indifferent from happy and neutral faces, with only full fearful faces resulting in longer disengagement latencies. Postulating that the effects of threat-related stimuli on attention are contingent on enhanced amydgala activity(Vuilleumier, 2005
), the results seem to be partially at odds with previous findings of comparable amygdala responses to fearful faces and fearful eyes alone in adults (Morris et al., 2002
; Whalen et al., 2004
). However, more recent evidence suggests that the perception of fearful eyes is not solely responsible for the enhanced amygdala reactivity to fearful faces. With fMRI, Asghar et al. (2008)
found amygdala responses of similar magnitude to whole fearful faces, fearful eyes alone, and fearful faces with the eye region masked. With similar stimulus conditions, Leppänen et al. (2008)
found enhanced visual ERP responses to fearful as compared to neutral faces both when the eyes were covered and presented in isolation. However, in Leppänen et al. (2008)
, behavioral and ERP differentiation of fearful and neutral expressions occurred at a shorter latency when the whole face instead of the eye region alone was visible. This suggests that although adults may respond to the eyes per se
and the eye region may provide sufficient information for classifying faces as fearful vs. non-fearful, whole face expressions provide additional diagnostic cues that permit faster and more accurate discrimination performance (e.g., cues in the mouth region). Collectively, these findings seem to suggest that adults flexibly utilize information from multiple sources to recognize fearful expressions whereas infants, in turn, seem to require the whole face in order to detect the face as fearful. As a limitation, it should be noted that the design of the present study does not permit an answer to the question of whether a fearful mouth embedded in an otherwise neutral face would yield similar results in infant participants as a stimulus with fearful eyes in a neutral face.
In conclusion, the present study provides evidence that by 7 months of age, infants show enhanced sensitivity to facial signals of threat as measured by the latency to disengage attention from centrally presented facial expression stimuli. It also seems that low-level visual information consisting of wide-open eyes is not sufficient to account for infants’ attentional biases for fearful faces. The results contribute to the growing research area of emotion-attention interactions in infancy which aims to elucidate the ontogenetic mechanisms of the processing of emotional significance in environmental stimuli (Leppänen & Nelson, 2009
). Finally, it remains to be determined how the differential disengagement from different emotional stimuli contributes to other measures of infant attention such as looking times and attention-sensitive ERPs.