The interplay of attention and emotion: top-down attention modulates amygdala activation in psychopathy

Abstract

Psychopathic behavior has long been attributed to a fundamental deficit in fear that arises from impaired amygdala function. Growing evidence demonstrates that fear potentiated 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 attention-related 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 non-psychopaths, and this increased LPFC activation mediated psychopathy’s association with decreased amygdala activation. In contrast, when explicitly attending to threat, amygdala activation in psychopaths did not differ from non-psychopaths. 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.

Functional Neuroimaging in Psychopathy

“…The authors reported that differences in amygdala activation in subjects with psychopathy are a function of goal-directed attention (for example, focus of attention can moderate amygdala dysfunction in psychopathy). The same study reported that regions of lateral PFC (relatives to top-down attention) mediate the correlation between psychopathy and amygdala activation [44]. This can confirm the central role of top-down attention in regulating bottom-up emotion and inhibitory cues in psychopathic offenders.…”

“…Larson et al [44] conducted an fMRI study with an instructed fear task, mainly focusing on attention-related circuitry in psychopathic offenders. The authors reported that differences in amygdala activation in subjects with psychopathy are a function of goal-directed attention (for example, focus of attention can moderate amygdala dysfunction in psychopathy).…”

“…This study also showed a tendency of people with psychopathy to focus on primary goals and tasks, excluding goal-irrelevant information. The activation of the mid-vlPFC can be a neural functional correlate of such inflated selective attention in psychopathic offenders [44]. …”

Dissociable relations between amygdala subregional networks and psychopathy trait dimensions in conduct‐disordered juvenile offenders

“…One may for instance speculate that the hyperconnectivity we document could reflect top‐down overregulation of BLA neurons by the frontoparietal control system, which might ostensibly deprive this system of negative affective salience (i.e., threat/punishment cues) and thus hinder optimum control of actions. Excessive frontoparietal control of BLA neurons and diminished BLA responding have been tentatively theorized in relation to impulsive and antisocial psychopathic traits [Blair, 2010; Blair, 2013b; Blair and Mitchell, 2009; Glenn et al, 2009; Larson et al, 2013; Moul et al, 2012], and subsumed to underpin the executive dysfunction and behavioral disinhibition that lie at the heart of these traits [Dolan and Anderson, 2002; Morgan and Lilienfeld, 2000; Racer et al, 2011; Sadeh and Verona, 2008; Sellbom and Verona, 2007; Zeier et al, 2012]. However, given the bidirectional flow of information between the BLA and frontoparietal structures [Barbas et al, 2003; Ghashghaei and Barbas, 2002; Sah et al, 2003; Selemon and Goldmanrakic, 1988], our finding may also reflect exaggerated bottom‐up signaling of motivational salience, potentially at the expense of negative emotional information.…”

The Psychopath Next Door: How Similar Are They to Those Behind Bars? Criminality, Executive Functioning, and Emotion Processing in 'Noncriminal' Psychopathy

“…While the IES model can accommodate the findings of emotional impairment, it cannot account for findings that demonstrate that redirection of attention to emotional information ameliorates the emotion impairment (Dadds, El Masry, Wimalaweera, & Guastella, 2008;Larson et al, 2013;Newman, Curtin, Bertsch, & Baskin-Sommers, 2010). …”