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 deficits in antisocial samples do not simply reflect differences in factors that alter facial affect recognition broadly, such as general intelligence, attention, task-specific motivation, or perceptual processing deficits. Rather, they suggest that antisocial behavior may be associated with deficits in neurocognitive mechanisms that specifically underlie processing of fearful expressions. These results reinforce that meta-analyses can reveal latent but consistent data patterns across multiple studies (Rosenthal and DiMatteo, 2001
). Although the results of many of the studies we assessed showed fear recognition deficits, often the authors did not emphasize or discuss these deficits. And in aggregate, they yielded a consistent relationship between fear deficits and antisociality, although they contained samples with heterogeneous age and gender distributions and diverse specific classifications.
Fear is indisputably more difficult for even healthy individuals to recognize than expressions such as happiness and sadness (Russell, 1994
; Elfenbein and Ambady, 2002
). Accuracy rates for this expression are typically around sixty to seventy percent in healthy populations. It has been suggested that fear recognition deficits in some clinical populations may result from the general difficulty of recognizing fearful expressions. Rapcsak and colleagues (2000)
found that fear recognition deficits in individuals with large temporal or parietal cortex lesions were statistically related to healthy individuals' difficulty in processing fearful expressions. When task difficulty was accounted for, subjects with lesions were not disproportionately impaired in fear recognition. By contrast, our results show that fear recognition deficits in antisocial populations are proportionally greater than in comparison populations, indicating that these deficits are not attributable solely to task difficulty (see Adolphs, 2002
). It should also be noted that our comparison samples showed nearly equivalent accuracy for fear and disgust expression recognition, as has been found previously (Calder et al. 2003
; Camras and Allison, 1985
; Ekman et al. 1987
). However, antisocial individuals showed no recognition deficits for disgust.
Fear recognition deficits may instead indicate consistent neurocognitive dysfunctions among antisocial populations. Recent reviews indicate that fear recognition relies disproportionately on the amygdala (Adolphs, 2006
; Murphy et al. 2003
). Clinical studies find that amygdala lesions lead to specific impairments in recognizing fearful expressions (Adolphs et al. 1999
; Papps et al. 2003
). Neuroimaging studies find larger increases in amygdala activation to fearful expressions than other expressions. The results of a recent meta-analysis (Murphy et al. 2003
) indicated that amygdala activity is “remarkably selective” (p. 225) for fear-related processing. This conclusion was based on results showing that over 60% of studies assessing fear expression processing show enhanced amygdala activation, compared to fewer than 20% of studies assessing emotional processing relevant to disgust, anger, happiness, or sadness. Several studies have shown enhanced amygdala activity across multiple expressions; however, the largest increase in amygdala activity still may be found to fearful expressions (Winston et al. 2003
; Fitzgerald et al. 2006
). Finally, sampling participants on the basis of their fear recognition ability shows that reduced ability to identify fearful expressions is associated with amygdala hyporesponsivity (Corden et al. 2006
). Together, this evidence supports the association between specific fear recognition deficits and amygdala dysfunction.
Extensive indirect and direct evidence supports the existence of amygdala dysfunction in antisocial populations. Patrick was the first to consider that amygdala dysfunction might be linked to the development of psychopathy (Patrick, 1994
). Subsequent neurocognitive testing to probe functions subserved by the amygdala has found consistent deficits in antisocial individuals. Individuals with psychopathy show impairment on tasks that assess the generation of autonomic responses to anticipated threat (Hare, 1982
; Ogloff and Wong, 1990
), the augmentation of the startle reflex following visually presented threat primes (Levenston et al. 2000
), passive avoidance learning (Lykken, 1957
; Newman and Kosson, 1986
), and affective priming (Blair et al. 2006
). Individuals with antisocial personality disorder and children with conduct disorder have similarly shown reduced autonomic responding to aversive stimuli (Dinn and Harris, 2000
; Herpertz et al. 2001
). Children who show antisocial behavior report reduced arousal to aversive stimuli (Sharp et al. 2006
). The results of more recent imaging studies have confirmed that amygdala activation is reduced during affective processing tasks in psychopathic adults (Birbaumer et al. 2005
; Kiehl et al. 2001
) and children with conduct disorder (Sterzer et al. 2005
). Behavioral data cannot conclusively settle questions relevant to neuroanatomical substrates. However, the current data are consistent with existing neuroanatomical data that suggest amygdala impairment to be associated with both antisociality and specific impairments in fearful expression processing.
The role that the amygdala plays in the correct identification of fearful expressions is not yet clear. Several possibilities have been proposed. One is that perception of an emotion causes the viewer to simulate the perceived emotional experience. A viewer may draw on information from an amygdala-based fear simulation to reconstruct and identify the expresser's emotional state (Goldman & Sripada, 2005
; Lawrence & Calder, 2004
). This explanation specifies that reduced fear responding will be associated with impaired fearful expression recognition. As has been discussed, some antisocial populations (particularly psychopaths) show just this pattern: both limited fearful responding (Patrick, 1994
) and limited fearful expression recognition (Blair et al. 2004
). Another proposed mechanism is that activity in the amygdala facilitates retrieval of semantic labels for facial expressions like fear. In this view, expression recognition impairments represent impairments in the ability to generate a verbal label for an expression like fear (Adolphs, 2006
; Blair et al. 2005
). Empirical support exists for both of these models of facial affect recognition; this meta-analysis cannot provide conclusive evidence in support of one over the other.
This meta-analysis also cannot clarify whether deficits in the recognition of fear expressions are specific to antisocial populations or extend to other clinical populations. However, the available evidence does not suggest that specific deficits in fear expression recognition are characteristic of all clinical samples. There is no theoretical support of which we are aware for fear recognition deficits in disorders such as depression, anxiety, or borderline personality disorder. Some data even suggest that individuals with these disorders show enhanced sensitivity to fearful expressions (Bhagwagar et al. 2004
; Le Masurier et al. 2007
; Surcinelli et al. 2006
; Wagner and Linehan, 1999
). Indications of amygdala dysfunction in autism have led to suggestions of fear recognition impairment in this population (Howard et al. 2000
). However, individuals with autism are typically found to show equivalent impairments in the recognition of multiple expressions (Castelli, 2005
; Humphreys et al. 2007
; Sasson, 2006
). This suggests broader face processing deficits in autism in accordance with the broad social dysfunction characteristic of this disorder.
It should be emphasized that identifying any emotional expression, including fearful expressions, is a complex task that requires visual scanning, perceptual processing, effortful attention, working memory, and semantic processing. Accordingly, such processing relies on a large, distributed network of neural structures. At the most basic level, intact functioning of occipitotemporal visual cortex is required to process the geometric configuration of the features of the face (Allison et al. 1999
). The superior temporal gyrus and fusiform gyrus (part of inferior temporal cortex) play central roles in processing faces (LaBar et al. 2003
). Once configural features have been assessed, intact functioning of structures in the temporal lobes is required to link the configural properties of facial expressions with stored knowledge about what those properties represent (Haxby et al. 2002
). Dysfunction in any of these structures may characterize individuals who show generalized impairments in processing facial emotion.
Low levels of impairment were found across expressions in the antisocial samples in this meta-analysis. This suggests that dysfunction in one or more structures in this network may be associated with antisocial behavior. Dysfunction in superior temporal sulcus has been implicated in antisocial populations (Kiehl, 2006
). In addition, regions involved in general emotional processing that are functionally connected to the amygdala may be associated with deficits in processing facial expressions, particularly fearful expressions (Murphy et al. 2003
). Such regions include the dorsal anterior cingulate cortex (Stein et al. 2007
) and the ventromedial prefrontal cortex, a region that has extensive functional connections with the amygdala and that is often found to be impaired in antisocial individuals (Birbaumer et al. 2005
; Kiehl et al. 2001
). Lesions to these regions, and disrupted connections between these regions and the amygdala, appear to affect processing of multiple emotional expressions rather than of fearful expression specifically (Hornak et al. 2003
). Finally, subcortical routes that involve the thalamus and superior colliculus appear to be involved in processing emotional expressions, particularly fearful expressions (Luo et al. 2007
; Morris, et al. 1999
). Dysfunction in these regions could also exist among antisocial populations.
Most of the populations in the studies included in this meta-analysis had clinical diagnoses, were incarcerated, or were in other secure settings (e.g., camps or schools for children with behavior problems). These populations presumably posessed serious functional impairments. Only three studies (Blair & Coles, 2000
; Dadds, 2006; Montagne et al, 2005
) drew from community samples. It is thus difficult to infer how the observed relationship between antisociality and fear recognition would vary as a function of functional impairments. We speculate that increasingly severe antisocial behaviors and traits such as callousness would be associated with increasingly impoverished fear recognition abilities. Thus, any two samples that differ in antisociality will also differ in fear recognition skills, but the greater the disparity in antisocial traits and behavior, the greater the disparity in facial affect recognition.
This meta-analysis included populations characterized as psychopathic, conduct disordered, aggressive, unsocialized, abusive, and criminal. These classifications all are primarily defined by persistent behavior that violates the rights and welfare of others or breaks important normative rules—i.e., antisocial behavior. Unlike the other classifications, a classification of psychopathy indicates particular antisocial personality traits (e.g., lack of empathy and remorse) in addition to antisocial behaviors such as criminal offenses. The remaining classifications do not specify what personality or environmental variables (such as impulsiveness, substance abuse, physical abuse, or trauma) are associated with observed antisocial behavior. Psychopathic individuals thus represent a more homogenous group, and evidence of impaired amygdala functioning in this group is accordingly more consistent (Birbaumer et al. 2005
; Blair et al. 2006
; Herpertz et al. 2001
; Kiehl et al. 2001
; Mitchell et al. 2006
). This may be because amygdala dysfunction is most pertinent to callous and unemotional personality traits and instrumental antisocial behavior, which are characteristic of psychopaths but may or may not be present in other antisocial individuals (Blair, 2001
). However, the consistency of our results among psychopathic and non-psychopathic samples, as well as frequent findings of reduced amygdala functioning among other antisocial samples, suggest a high degree of overlap among these samples.
Our analyses found sadness recognition deficits were also associated with antisociality. This is theoretically consistent in that sadness, like fear, is a distress cue (Blair et al. 1997
; Decety and Chaminade, 2003
). In addition, similar neural structures, including the amygdala, are associated with processing sadness expressions (Adolphs and Tranel, 2004
; Blair et al. 1999
). It is unclear why antisociality is more reliably linked to fear recognition than sadness recognition; perhaps recognition deficits are less evident for expressions that possess identifiable markers such as the downturned mouth of sadness. Comparing correlates of fear and sadness recognition might be facilitated by examining patterns of errors during identification of these expressions. Only three studies we assessed provided error information (Blair et al. 2004
; Matheson et al. 2005; Walz and Benson, 1996
), and examination of these data did not reveal clear error patterns for fear or sadness. More consistent provision of such data might improve the interpretation of the results of future studies.
Distress cues such as fearful or sad expressions have been theorized to stabilize social interactions among healthy individuals by eliciting affective responses that reduce the likelihood of continued aggression against the victim (Blair, 1995
; Marsh and Ambady, 2007
). Such affective response may include empathy and remorse. Both of these responses are elicited by the perception and correct interpretation of distress cues such as fear expressions (Blair, 1995
; Hoffman, 1987
; Marsh and Ambady, 2007
). That antisociality is associated with a lack of empathy and remorse again supports the conclusions that antisocial individuals do not respond appropriately to distress cues (Eisenberg, 2000
). The Integrated Emotion Systems model provides one explanation for this process, specifying that distress cues are social reinforcers that enable conspecifics to convey the societal valence of objects and behaviors to the developing individual (Blair, 2001
). Because the amygdala is involved in the formation of stimulus-reinforcement associations, it is theorized that amygdala dysfunction impairs the learning that typically results following distress cues. This prevents moral socialization and increases the likelihood of antisocial behavior (Blair, 2005
). Another mechanism by which fearful expressions may elicit empathy is via infantile appearance cues (e.g., wide, round eyes) that stimulate caring, non-aggressive responses in perceivers (Marsh et al. 2005
Relatively few studies were included in this analysis. However, the consistency of the results of the various analyses we conducted strengthens our conclusions. Our file-drawer analysis indicates that our findings did not likely result from sampling bias, which in meta-analyses usually results from the exclusion of unpublished or “file drawer” studies that do not show significant results. The nature of the meta-analysis we conducted minimized such biases because facial affect recognition studies do not typically test a single effect relevant to the null hypothesis. Rather, they test the recognition of multiple separate expressions individually and in aggregate. Thus, a study need not have demonstrated fear recognition deficits in order to be published (and indeed, several did not).
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.