Elsevier

Acta Psychologica

Volume 123, Issue 3, November 2006, Pages 312-336
Acta Psychologica

Aging and visual search: Automatic and controlled attentional bias to threat faces

https://doi.org/10.1016/j.actpsy.2006.01.008Get rights and content

Abstract

Using a visual search paradigm, we investigated how age affected attentional bias to emotional facial expressions. In Experiments 1 and 2, participants searched for a discrepant facial expression in a matrix of otherwise homogeneous faces. Both younger and older adults showed a more effective search when the discrepant face was angry rather than happy or neutral. However, when the angry faces served as non-target distractors, younger adults’ search was less effective than happy or neutral distractor conditions. In contrast, older adults showed a more efficient search with angry distractors than happy or neutral distractors, indicating that older adults were better able to inhibit angry facial expressions. In Experiment 3, we found that even a top–down search goal could not override the angry face superiority effect in guiding attention. In addition, RT distribution analyses supported that both younger and older adults performed the top–down angry face search qualitatively differently from the top–down happy face search. The current research indicates that threat face processing involves automatic attentional shift and a controlled attentional process. The current results suggest that age only influenced the controlled attentional process.

Introduction

There clearly is an evolutionary advantage to a species that can respond rapidly to danger or a threat in the environment. If an animal waited to identify an object before taking action, the chances of survival would be reduced. Thus, it is not surprising that neurophysiological studies have suggested a direct pathway from the sensory thalamus to the amygdala, which allows automatic responses to a potential threat (LeDoux, 1996). A facial expression would qualify as a biologically-critical stimulus with the potential to indicate danger or a threat. Öhman (2002) suggested that facial expressions rapidly access the amygdala through a “quick and dirty” analysis via a simple subcortical network rather than a complete visual analysis in the cortical network. Previous studies reported that individuals with bilateral amygdala damage show an impaired social judgment based on facial expressions, particularly those expressing threat-related emotions (Adolphs, Tranel, & Damasio, 1998). The special status of threatening facial expressions to guide attention was even observed when the face was presented outside an individual’s awareness (Dimberg et al., 2000, Mogg and Bradley, 1999, Morris et al., 1999).

The special status of threat faces was also supported by studies using a visual search paradigm. Previous research found that faces expressing negative facial emotions guide visual search more efficiently than faces expressing happy or neutral emotions (Eastwood et al., 2001, Fox et al., 2000, Hansen and Hansen, 1988, Öhman et al., 2001, Vuilleumier and Schwartz, 2001). Some facial expressions used in these studies expressed sad rather than threatening emotions (Eastwood et al., 2001), though other studies reported that effective visual search was more specific to threatening rather than generally negative faces (Öhman et al., 2001).

Processing of threat stimuli could be modified within an individual’s lifetime. Studies suggested that older adults were more proactive in avoiding negative affect (Carstensen, 1992, Lawton, 1989, Mroczek, 2001). For instance, Mather and Carstensen (2003) showed that older adults were slower at responding to the location previously occupied by emotionally negative faces. According to the socio-emotional selectivity theory (Carstensen, 1992, Carstensen et al., 1999), a changing priority in life would guide older adults to focus on emotional goals, developing better emotional regulation. The idea that older adults selectively inhibit emotionally negative stimuli appears to be inconsistent with cognitive aging research that suggested an age-related deficit in inhibitory processing (Hasher and Zacks, 1988, Kane et al., 1994). However, research suggested that age-related inhibitory deficits were selective, not unitary (Kramer, Humphrey, Larish, Logan, & Strayer, 1994). Recently, Kramer et al. (in press) showed that older adults maintain better memory for already inspected objects as compared to younger adults, making fewer re-fixations on the previously examined distractors. Research has also demonstrated a greater inhibition-of-return effect for older adults (Langley, Fuentes, Hochhalter, Brandt, & Overmier, 2001) as compared to younger adults. These results suggest that some of the inhibitory processes that support visual search are improved for older adults. In a recent review article (Mather & Carstensen, 2005), it was argued that older adults often show better inhibition of negative information than younger adults because they are more likely to have a currently activated goal to try to regulate emotion. Thus, it is plausible to hypothesize a special status for threat stimuli regarding inhibitory processing of older adults.

Selectively inhibiting negative affect is not the only account to explain age differences in facial expression processing. Older adults may be less accurate at recognizing facial expressions (Calder et al., 2003, McDowell et al., 1994, Moreno et al., 1993, Phillips et al., 2002, Sullivan and Ruffman, 2004). Interestingly, studies reported older adults’ deficit in recognizing facial expressions mostly for negative facial expressions. For instance, McDowell et al. (1994) found deficits from older participants in recognizing sadness, anger, and fear from photographs, with no difference between the age groups in identifying happiness. Sullivan and Ruffman (2004) showed that elderly adults were poor at recognizing angry, sad, or fearful facial expressions, but were not impaired at judging other emotions. Phillips et al. (2002) showed that older adults were less able to identify some aspects of emotion from faces, particularly anger and sadness. Calder et al. (2003) found that older adults were impaired at recognizing some facial expressions, primarily fear and sadness, but unimpaired in recognizing disgust. This age-related decline in the recognition of some negative emotions appeared to be independent of changes in perceptual ability or processing speed (Sullivan & Ruffman, 2004).

Neuropsychological studies also supported age-related differences in facial processing. Older adults recruit different cortical pathways to process emotions than younger adults. Gunning-Dixon et al. (2003) examined brain activation of facial emotion processing using fMRI. Younger adults activated the amygdala and surrounding temporo-limbic regions during emotional face processing, whereas older adults showed increased activation in parietal, temporal and frontal regions. Iidaka et al. (2002) showed a significant age difference in the left amygdala during the perception of negative facial expressions, with reduced activity for older participants.

In the current study, we further explored how age influences attentional processing of facial expressions. In particular, we investigated how different components of the attentional network are affected by aging. Research has supported the independence of attentional networks that involve alerting, orienting, and executive function (Corbetta et al., 2000, Fan et al., 2002, Posner and Peterson, 1990), with the orienting network consisting of engagement, shift, and disengagement components (Posner and Cohen, 1984, Posner et al., 1982). The special status of threatening facial expression during visual search may be associated with a shift of visual attention toward threatening stimuli (Mogg and Bradley, 1999, Öhman et al., 2001). However, recent studies characterized anxiety as a failure to rapidly disengage visual attention away from the threat-related facial expressions (Fox et al., 2002, Georgiou et al., 2005), suggesting that a selective component of the attentional network can be identified during facial expression search. Research also reported that age affected attentional networks selectively during emotional stimuli processing. For instance, Rösler et al. (2005) showed that age did not influence the initial saccade to negative or positive emotional scenes, but older adults showed a shorter dwell time on the emotionally negative scenes than positive or neutral scenes. This result indicates that older and younger adults may not be different at shifting attention toward affective stimuli, but older adults may be better able to disengage from emotionally negative stimuli.

Our objective in this study is first to investigate how age modulates a shift of visual attention toward threat-related facial expressions, and second to determine how age affects the disengagement of visual attention from threat-related facial expressions. In the current study, younger and older adults conducted a visual search task with neutral, angry, and happy schematic faces. We examined the shift of visual attention and disengagement of visual attention by using different facial expressions as targets or as non-target distractors. For instance, if the task is to search for an angry facial expression, search performance would reflect an attentional shift toward an angry face. On the other hand, if the task is to search for a neutral or happy facial expression, angry faces in the display would serve as non-target distractors that must be inhibited or rapidly disengaged.

According to the socioemotional selectivity theory, which supports a selective inhibition of negative affect by older adults, age should influence the disengagement or ignoring of the threat face. Therefore, if the task is to search for an angry facial expression, performance should not be influenced by age. However, if the task is to ignore an angry facial expression (i.e., when angry faces serve as non-target distractors), older adults should show an advantage. Note that studies reporting age-related deficits at recognizing emotional facial expression showed age differences mainly for emotionally negative faces (Calder et al., 2003, McDowell et al., 1994, Phillips et al., 2002, Sullivan and Ruffman, 2004). Therefore, it is plausible to hypothesize that selective avoidance of negative affect leads to a deficit in recognizing facial expressions, which is a prediction that the socioemotional selectivity theory would also make. Age would influence only the disengagement process, with older adults’ showing an advantage when angry faces serve as non-target distractors.

Note that neuropsychological studies showed age-related differences in brain activation responding to facial expressions (Gunning-Dixon et al., 2003, Iidaka et al., 2002). Research suggested that older adults recruit brain areas including the parietal and frontal cortices to respond to facial expressions, while younger adults showed mostly temporo-limbic activation (Gunning-Dixon et al., 2003). We speculate that older adults might utilize more controlled attentional processes when responding to threat-related facial expressions, recruiting prefrontal and parietal pathways, in addition to automatic vigilance mediated by the amygdala. Presumably, this adaptive and goal-driven attentional control of older adults would contribute to better inhibitory processing on threat-related facial expressions.

In the current studies, by using a visual search paradigm, we predicted that both younger and older participants would show smaller search slopes when the search target is expressing angry rather than happy or neutral emotions. We also hypothesized that older adults would be more effective at disengaging attention from threatening facial expressions than younger adults. For instance, when angry facial expressions serve as non-target distractors (i.e., searching for a neutral face among an angry crowd), older adults may show better search performance, effectively inhibiting or disengaging from the angry distractors.

Section snippets

Experiment 1

In Experiment 1, we examined the efficiency of attentional guidance to emotional faces using a visual search. Younger and older adults viewed a number of schematic faces on a computer screen and located a discrepant face by touching the touchscreen display. If an angry face is more effective at attracting visual attention than a happy face (Fox et al., 2000, Hansen and Hansen, 1988, Öhman et al., 2001), we would expect smaller search slopes for the angry than the happy face search. We

Experiment 2

In Experiment 2, we investigated whether age influences attentional disengagement from facial expressions. In Experiment 1, the task was to locate a discrepant facial expression, and thus did not address whether attentional disengagement from facial expressions (particularly threat-related facial expression) was influenced by age. If older adults selectively inhibit negative affect as suggested by socioemotional selectivity theory (Carstensen et al., 1999, Mather and Carstensen, 2003), older

Experiment 3

The objective of Experiment 3 was to investigate whether a specific search goal for a facial expression (i.e., looking for only a happy face or only an angry face) would overcome the special status of an angry face for guiding attention towards it. In addition, we investigated whether the presence of a happy or angry face in the display, which would be opposed to the task goal, would influence the visual search. In the experiment, participants viewed a number of schematic faces on a computer

General discussion

Using a visual search task, we investigated younger and older adults’ attentional bias while searching for facial expressions. Both younger and older adults showed a smaller search slope when the search target was angry rather than happy or neutral. However, when the angry faces served as non-target distractors, younger adults’ search was less effective than happy or neutral distractor conditions. In contrast, older adults showed a more efficient search with angry distractors than happy or

Acknowledgements

We thank Johan Wagemans, Mara Mather, and an anonymous reviewer for their helpful comments on the manuscript.

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    We did not include the inverted face condition in the main analyses because we included the condition to examine a secondary question: whether the angry face superiority effect was due to an artifact of the schematic face stimuli. Despite inverting distractor and target faces, we still observed an angry face superiority effect, although the size of the effect was reduced.

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