Short communicationTheta phase coherence in affective picture processing reveals dysfunctional sensory integration in psychopathic offenders
Introduction
Prominent models of psychopathy attribute these offenders’ failures of conscience, antisocial behavior, and insensitivity to affective information to a core emotion deficit. However, substantial evidence indicates that experimental context moderates these emotion deficits. Baskin-Sommers, Curtin, and Newman (2011) propose that this context specificity is associated with an early attention bottleneck that filters multidimensional information in serial, rather than simultaneously, thus hindering the fluid processing of information. Across experimental contexts, psychopathic offenders display normal responses to affective information when it is part of their goal-directed task or embedded in a perceptually simple display, yet their reactions to the same stimuli are deficient when their attention is allocated to an alternative goal or complex aspect of the situation (Baskin-Sommers, Curtin, & Newman, 2013; Decety, Chen, Harenski, & Kiehl, 2013; Meffert, Gazzola, den Boer, Bartels, & Keysers, 2013; Newman, Curtin, Bertsch, & Baskin-Sommers, 2010; Newman and Kosson, 1986, Sadeh and Verona, 2012).
Arguably the strongest evidence for the emotion deficit in psychopathy comes from research examining startle responses during picture viewing. In contrast to non-psychopathic offenders, who display startle potentiation during unpleasant pictures and startle inhibition during pleasant pictures, the startle potentiation to unpleasant pictures appears to be lacking in psychopathic offenders, particularly in offenders high on interpersonal-affective (Factor1) traits (Vaidyanathan, Hall, Patrick, & Bernat, 2011). However, Baskin-Sommers et al. (2013) demonstrated that by manipulating picture familiarity, psychopathic offenders displayed the classic deficit in emotion-modulated startle during novel pictures, but no deficit in emotion-modulated startle during familiar pictures.
Using explicit instruction or condition manipulations, previous work provides strong evidence of dysfunctional attention-emotion processing in psychopathy. It is possible, though, that an attention bottleneck can also affect perceptual and sensory processing (Kastner & Ungerleider, 2000). Previous research shows that the phase coherence of theta, particularly in parietooccipital and primary sensory cortices, represents a neural index of readiness to perceive and integrate sensory inputs, both across and within sensory modalities (Buzsaki, 2005, Lakatos et al., 2009). Moreover, theta phase coherence is modulated by familiarity, possibly indicating greater dynamic coordination in familiar conditions across sensory domains (Miyakoshi, Kanayama, Iidaka, & Ohira, 2010).1 The present study measured theta phase coherence, as an index of readiness to perceive and integrate sensory information, during the picture-viewing paradigm used by Baskin-Sommers et al. (2013). If readiness to perceive and integrate sensory information affects the efficient processing of affective information among offenders with psychopathy, then their theta inter-trial coherence (ITC), much like their defensive startle reactivity, should be impacted by the familiarity manipulation.
Section snippets
Participants
Ninety-nine incarcerated males between the ages of 18 and 45, with an IQ greater than 70, no clinical diagnoses of schizophrenia, bipolar disorder, or psychosis, and who were not currently using psychotropic medications were assessed for psychopathy and its related traits with the Psychopathy Checklist-Revised (PCL-R) (Hare, 2003) (see Table S1).
Task
Thirty-six pictures (12 unpleasant, 12 neutral, 12 pleasant) were selected from the International Affective Picture System (Lang, Bradley, & Cuthbert,
Psychopathy
Data were examined in a 2 (familiar, novel) by 3 (pleasant, neutral, unpleasant) General Linear Model (GLM) with PCL-R (z-score) as a continuous factor. Interaction contrasts were used to examine valence (unpleasant vs. pleasant) and affect (unpleasant/pleasant vs. neutral) effects.
Consistent with prior research, there was a significant familiarity main effect, F(1,97) = 4.71, p = 0.032, ηp2 = 0.046, with familiar pictures eliciting greater theta phase coherence than novel pictures. There were no
Discussion
The present study used time-frequency analysis to examine whether sensory processing and integration affects the core affective deficits characteristic of psychopathy. Psychopathic offenders, and offenders high on Factor1, showed enhanced emotion-modulation of theta ITC to familiar, but not novel pictures. In contrast, theta coherence for offenders high on Factor2 was greater for both types of affective novel stimuli. These results suggest that the psychopathy and Factor-related dysregulation
Acknowledgement
This work was supported by grant 5R21DA030876 from NIDA.
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