ReviewDeficits in facial affect recognition among antisocial populations: A meta-analysis
Introduction
Processing facial affect is crucial for socialization and normal social interaction (Corden et al., 2006; Fridlund, 1991). Aggression and other maladaptive antisocial behaviors may result from failure to be appropriately guided by the social cues of others (Blair, 2003a; Montagne et al., 2005; Walker and Leister, 1994). Some have suggested that distress-related cues, particularly fearful expressions, play an important role in inhibiting antisocial behavior (Blair, 2001; Nichols, 2001; Price et al., 2004). Accordingly, many studies find impairments in processing distress-related cues among antisocial populations. However, not all studies find this impairment. It is unclear whether these inconsistencies result from disparate methodologies, sample populations, or analytic techniques, or, alternately, from the absence of a strong relationship between fearful affect processing and antisociality. Better understanding of facial affect recognition deficits associated with antisociality would permit more precise hypotheses to be formulated regarding neurocognitive correlates of antisocial behavior. We thus conducted this meta-analysis to assess associations between antisociality and facial affect recognition deficits. We hypothesized that, beyond any general facial affect recognition deficits, antisocial individuals show specific deficits in processing fearful expressions. We also hypothesized that such deficits are not solely attributable to task difficulty.
Emotional facial expressions play an important role in modulating interpersonal behavior. Given this, extensive research has assessed the relationship between facial affect recognition and psychiatric disorders characterized by interpersonal deficits. Generalized impairments in processing facial affect have been found in antisocial populations (Kropp and Haynes, 1987; Woodbury-Smith et al., 2005; Zabel, 1979). But such impairments have also been found in disorders like autism, schizophrenia and social anxiety disorder (Gross, 2004; Singh et al., 1998; Tremeau, 2006; Easter et al., 2005). Myriad factors, including general intelligence, age, attention, verbal ability, and task-specific motivation can be associated with reductions in facial affect recognition scores (Herba and Phillips, 2004; Moore, 2001). It is thus unsurprising that many clinical populations suffer facial affect recognition deficits. However, it means that little clinically or neuropsychologically specific information regarding a particular population's impairments can be extracted from general facial affect processing deficits.
More informative would be evidence for an association between antisocial behavior and a deficit in recognizing one or more specific expressions. Likely candidates include distress cues like fear and sadness because these expressions may inhibit or avert inappropriate behavior like aggression (Blair, 2003b; Blair et al., 1997; Marsh et al., 2005; Walker and Leister, 1994). Ethologists find similar aggression-inhibiting effects of distress cues in other primates and have speculated that distress cues evolved for this purpose (Preuschoft, 2000). Developmental, behavioral, and clinical research shows that distress cues elicit empathy in those who see them (Hoffman, 1987; Marsh and Ambady, 2007; Nichols, 2001; Preston and de Waal, 2002). Empathy is generally associated with decreased antisocial behavior (Eisenberg, 2000). It has been proposed that distress cues possess perceptual properties that elicit empathy and inhibit aggression (Marsh et al., 2005). It has also been proposed that fearful and sad expressions serve as social reinforcers that condition developing children to avoid engaging in the antisocial behaviors that elicit these expressions. This process is specified by the Integrated Emotion Systems (IES) model (Blair, 2005).
Facial affect processing relies on a distributed network of structures that includes occipitotemporal cortex (particularly fusiform gyrus and superior temporal gyrus), anterior cingulate cortex, amygdala, and ventromedial prefrontal cortex (Adolphs, 2006; Murphy et al., 2003). Evidence is accumulating, however, that beyond this general network partially separable neural systems process different expressions. Detection of fearful expressions relies disproportionately on the amygdala, and the detection of disgust on the insula and basal ganglia (Adolphs, 2002; Phillips et al., 2004; Murphy et al., 2003). Evidence that antisocial individuals are impaired in processing specific expressions like fear or disgust could facilitate targeted research into neurocognitive deficits underlying antisocial behavior.
Antisocial behaviors are those that violate the rights or welfare of other individuals. Multiple studies have shown specific impairments in fearful expression processing in populations who engage in these behaviors (e.g., Blair et al., 2004; Blair and Cipolotti, 2000; Carr and Lutjemeier, 2005; Walker and Leister, 1994; Woodbury-Smith et al., 2005). These populations include those primarily classified by the presence of antisocial behaviors (e.g., aggressive, criminal, externalizing, abusive) and those classified on the basis of both antisocial behaviors and personality traits such as a lack of empathy and remorse (e.g., psychopaths). However, not all of these studies find fearful expression recognition impairments (Kosson et al., 2002). Many studies that find fear recognition deficits assess children (Blair and Coles, 2000; Blair et al., 2001; Stevens et al., 2001). This leaves questions remaining, such as whether apparently specific deficits in recognizing fearful expressions stem from task difficulty rather than fear-specific neuropsychological deficits.
Even in healthy populations, fearful expressions are more often misidentified than other expressions. It is important to determine whether task difficulty can fully account for the link between fear recognition deficits and antisociality. If it can, it suggests the deficits can be accounted for by general facial affect processing impairments. Such deficits may simply be more obvious for expressions that are more difficult to recognize. If, however, fear-recognition deficits cannot be explained by task difficulty, this suggests dysfunction in neural structures or systems, such as the amygdala, that are particularly important to fearful expression processing (Adolphs, 2002; Rapcsak et al., 2000).
Prior research supports the contention that fearful expression recognition deficits may be associated with both amygdala dysfunction and antisocial behavior. Patients with amygdala lesions show deficits in recognizing fearful expressions (Adolphs et al., 1999; Papps et al., 2003). Neuroimaging studies also support the role of the amygdala in processing fearful expressions (Corden et al., 2006; Murphy et al., 2003; Phillips et al., 2004; Whalen et al., 1998). Considerable recent work has implicated impaired amygdala functioning in antisocial populations during affective tasks (Levenston et al., 2000; Patrick, 1994; Blair, 2003a, Blair, 2003b). And recent neuroimaging research has supported the existence of amygdala dysfunction in antisocial individuals (Birbaumer et al., 2005; Kiehl et al., 2001; Sterzer et al., 2005). This body of evidence is consistent with the hypothesis that across studies, antisocial individuals show a consistent and specific deficit in the recognition of fearful expressions. However, this hypothesis has not yet been tested.
The goal of this meta-analysis was to assess the existing literature that has measured facial expression recognition abilities in individuals with disorders or behaviors that are defined by antisociality. Such individuals include those classified as psychopathic, aggressive, criminal, delinquent, or externalizing. We investigated whether (a) individuals with antisocial behavior show impairments in recognition of each of the six expressions; (b) whether this deficit is greater for fearful expressions than for other emotional expressions; and (c) whether deficits in fear recognition are attributable to task difficulty.
Section snippets
Method
A variety of strategies were used to find relevant articles. Once located, several criteria were applied to determine whether a study could be included in the meta-analysis:
Do antisocial populations show deficits in recognizing the six emotional expressions?
For each analysis addressing this question, we compared accuracy for recognizing the six basic expressions among antisocial individuals to accuracy for controls. We used both single-sample t-tests and their non-parametric equivalent to calculate these comparisons. In all cases, threshold significance was set at P<0.05; only results that survive correction for multiple comparisons via the Bonferroni method are presented.
Discussion
We found a consistent, robust link between antisocial behavior and impaired recognition of fearful facial affect. Relative to comparison groups, antisocial populations showed significant impairments in recognizing fearful, sad, and surprised expressions. They were not reliably impaired in recognizing happiness, anger, or disgust expressions. Deficits for recognizing fear were significantly greater than deficits for any of the other expressions. This specificity suggests that fear recognition
Conclusions
Antisocial populations across 20 studies showed specific deficits in recognizing fearful facial affect. The perception and recognition of fearful expressions have been previously linked to intact amygdala function, which may be impaired in individuals who exhibit persistent antisocial behaviors. The results of this meta-analysis may assist researchers in developing more precise hypotheses regarding the neural correlates and causes of antisocial behavior.
Acknowledgments
This research was supported by the Intramural Research Program of the NIH:NIMH.
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