The interplay of attention and emotion: top-down attention modulates amygdala activation in psychopathy (original) (raw)

2013, Cognitive, Affective, & Behavioral Neuroscience

Psychopathic behavior has long been attributed to a fundamental deficit in fear that arises from impaired amygdala function. Growing evidence has demonstrated that fearpotentiated startle (FPS) and other psychopathy-related deficits are moderated by focus of attention, but to date, no work on adult psychopathy has examined attentional modulation of the amygdala or concomitant recruitment of relevant attentionrelated circuitry. Consistent with previous FPS findings, here we report that psychopathy-related differences in amygdala activation appear and disappear as a function of goal-directed attention. Specifically, decreased amygdala activity was observed in psychopathic offenders only when attention was engaged in an alternative goal-relevant task prior to presenting threat-relevant information. Under this condition, psychopaths also exhibited greater activation in selective-attention regions of the lateral prefrontal cortex (LPFC) than did nonpsychopaths, and this increased LPFC activation mediated psychopathy's association with decreased amygdala activation. In contrast, when explicitly attending to threat, amygdala activation did not differ in psychopaths and nonpsychopaths. This pattern of amygdala activation highlights the potential role of LPFC in mediating the failure of psychopathic individuals to process fear and other important information when it is peripheral to the primary focus of goal-directed attention. Keywords Attention. Emotion. Amygdala. Prefrontal cortex Psychopathy is a common and severe psychopathological disorder affecting approximately 1 % of the general population and 15 %-25 % of incarcerated male offenders (Hare, 1996; Neumann & Hare, 2008). Despite psychopathic individuals' good intelligence and an absence of Axis I psychopathology (aside from substance abuse; Hart & Hare, 1989), they display an inability to form genuine relationships with parents, teachers, friends, or lovers; limited and superficial affective processing, especially with respect to anticipatory anxiety and remorse; an impulsive behavioral style involving a general failure to evaluate anticipated actions and inhibit the inappropriate ones; and a chronic antisocial lifestyle that entails great costs to society as well as for the affected individual (e.g., incarceration; Cleckley, 1941). Although both affective and behavioral characteristics are important elements of psychopathy, the affective deficits have traditionally been considered the root cause of the psychopath's problems. Affective deficits in psychopathy have most often been understood in the context of the low-fear model (Lykken, 1957), which posits that the psychopath's deficit is mediated by an amygdala-based deficiency (Blair, 2003; Marsh & Cardinale, in press; Patrick, 1994; Viding et al., 2012). In adult samples, whereas some neuroimaging evidence has suggested that psychopathic individuals display less amygdala activation than controls during aversive conditioning, moral decision-making, social cooperation, and memory for emotionally salient words (