Attention to the eyes and fear-recognition deficits in child psychopathy

The ability to recognise fear is impaired in people with damageto the amygdala and, interestingly, in adult psychopathy. Herewe confirm that deficits in recognising fear exist in childrenwith psychopathic traits. We show for the first time that,as with patients with amygdala damage, this deficit can betemporarily corrected by simply asking them to focus on the eyes of other people. These data support models of psychopathythat emphasise specific dysfunction of the amygdala and suggestan innovative approach for intervening early in the developmentof psychopathy.

INTRODUCTION

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INTRODUCTION

Deficits in fear recognition occur in both psychopathy (Hare, 1995; Blair, 2003) and patients with amygdala damage (Davis & Whalen, 2001;Adolphs et al, 2005) suggesting a role for amygdala dysfunctionin psychopathy. Recently, Adolphs et al (2005) showed thatdeficits in fear recognition associated with amygdala dysfunctionare driven by lack of attention to other people's eyes, andcould be overcome by instructing subjects to attend to theeyes. No study has tested whether these attentional processesoccur in the fear-recognition problems characteristic of psychopathy.A positive finding might have enormous potential for understandingthe development of the most severe forms of antisocial behaviour.

Whereas it may be naïve naive to think that deficits infear recognition could account for antisocial behaviour seenin adult psychopathy, such deficits could have a powerful influenceduring critical periods of child development. Fear recognitionnecessitates understanding that other people are sentient,typically described as a theory of mind (Skuse, 2003), in orderto discern the source of threat from the direction of the other'sgaze (Emery, 2000). A theory of mind is necessary for thedevelopment of empathy; amygdala damage is associated withdeficits in theory of mind development (Shaw et al, 2004); and children lacking this skill are less likely to develophealthy emotional connections or to benefit from the subtletiesof caregiver discipline associated with the development ofa conscience (Hughes et al, 2000). Thus, we were particularlyinterested in testing whether fear-recognition deficits occurand could be modified in children with psychopathic traits.

METHOD

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METHOD

This study tested the relationships of fear recognition andeye gaze to psychopathic traits (callous-unemotional traitsand antisocial behaviour) in community samples of childrenand adolescents. Psychopathic traits measured in these samplesare prognostic of negative outcomes (Dadds et al, 2005), havehigh genetic loadings (Viding et al, 2005), and have the advantageof not being confounded by comorbidity problems that characteriseclinical and forensic samples. We hypothesised that:

callous-unemotional traits would be uniquely associated withpoorer recognition of fear in a free-gaze condition;
highlycallous-unemotional children would improve to normallevelswhen instructed to attend to the eyes;
in a mouth-gaze condition,the highly callous-unemotional childrenwould return to theirprevious levels.

The studies were conducted in schools in Sydney, Australia.The first experiment included 33 boys, ranging in age from8 to 15 years (mean 12.07, s. d.=1.91); the second included65 boys, ranging in age from 9 to 17 years (mean 13.2, s. d.=1.87).Both samples were from middle- to upper-middle-class backgrounds.Means and standard deviations for callous-unemotional and antisocialbehaviour were consistent with normative samples from Australia (Dadds et al, 2005).

Callous-unemotional traits and antisocial behaviour were measuredas described in Dadds et al (2005). Parent and child scores were combined using a highest-score counts method. Accuracyof emotion recognition was measured using the University ofNew South Wales Facial Emotion Task (Dadds et al, 2004), inwhich happiness, sadness, anger, disgust, fear or a neutralexpression is displayed by four adult faces. Testing occurredin school classes. Emotions were presented in a random orderfor 2 s each. Participants recorded the emotion portrayed froma list of six emotions. In study 2, the faces were repeatedin two further blocks. In blocks 2 and 3, participants wereinstructed to focus on the eyes and the mouth, respectively, of the display faces. The order of the blocks was chosen becausefree gaze needed to be first in order to avoid contaminationby the later instructions. The look-at-the-eyes condition wasscheduled next and the look-at-the-mouth condition last, sothat any practice effects producing an improvement in accuracyover time would run counter to the experimental hypothesis thateye gaze would produce the highest accuracy.

RESULTS

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RESULTS

Partial correlations of callous-unemotional traits and antisocialbehaviour to accuracy of emotion recognition are shown in Fig. 1a.Antisocial behaviour was associated with poorer recognitionof neutral faces (r=-0.43, P<0.004), where neutral faceswere most often mistakenly rated as angry. This finding isconsistent with the hostilitybias model in which antisocialpeople are thought to over-interpret hostility in other people (Dodge & Pettit, 1993). As hypothesised, callous-unemotionalscores were uniquely associated with poor recognition of fearfulfaces (r=-0.52, P<0.0001). The most common errors were torate fear as neutral emotion or disgust. In the second experimentin the free-gaze condition, we replicated the finding that callous-unemotionalscores were negatively correlated with fear accuracy (r=-0.36,P<0.01). The correlation dropped to r=0.05 in the eye-gazecondition, but was again significant in the mouth-gaze condition,r=-0.24, P<0.05. Thus, high callous-unemotional scores wereassociated with poorer fear recognition except when participantswere instructed to look at the eyes. The mean accuracy scoresof fear recognition for boys across the three gaze conditionsfor the sample split into high callous-unemotional (top 25%)and low-average callous-unemotional groups are shown in Fig. 1b.Clearly, highly callous-unemotional children are substantiallypoorer at recognising fear unless specifically instructed tolook at the eyes. Direction of gaze made no difference to accuracyrates in low callous-unemotional children.

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Fig. 1. (a) Partial correlations of antisocial (controlling for callous-unemotional (CU) traits) and CU traits (controlling for antisocial) with accuracy of recognition of the six emotions for boys in study 1. (b) Mean accuracy for facial fear recognition for boys high and low on CU traits under three gaze conditions: no instruction, instruction to focus on eyes, instruction to focus on mouth. Significant interaction between gaze and CU category, F (2,55)=5.149, P=0.009. Error bars represent standard errors of the means.

DISCUSSION

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DISCUSSION

These results show that antisocial behaviour and callous-unemotionaltraits are associated with very different emotion-recognitionproblems in young males. Specifically, antisocial behaviouris uniquely associated with a tendency to oversee hostility,and callous-unemotional traits, the affective aspect of psychopathy,are uniquely related to poor recognition of fearful expressions.The current study shows that this deficit in fear recognitionis in part owing to visual neglect of the eye region of otherpeople's faces, as with amygdala-damaged patients (Adolphs et al, 2005),and can be temporarily reversed by directing attentional focusto the eye region of other people. Although this study is thefirst to demonstrate this effect, we note that Richell et al(2003) found that psychopathic individuals could identify facialemotions using stimulus faces that were truncated to includeonly information from the eye region.

Although they require replication in larger samples containingmore extremes of the psychopathy traits, these findings indicatethat emotion-recognition emotion-recognition problems in psychopathyare owing in part to a failure to direct attention to the emotionallysignificant aspects of the environment. This may have wide-reachingimplications for understanding and intervening with high-riskchildren at developmentally sensitive periods. We argue thatthese attentional processes will be of critical importance in the early years of life, when responsiveness to normal disciplinepractices will depend in part on the ability to recognise theemotional states of caregivers. Further, the ability to recognisefear in other people may be a specific marker of the abilityto develop theory of mind during the developmental stage thatis critical for learning that other people are sentient, feelingorganisms: a skill that is needed in order to treat others accordingly.

ACKNOWLEDGMENTS

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ACKNOWLEDGMENTS

This research was supported by a National Health and MedicalResearch Council of Australia Project Grant to M. D.

REFERENCES

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