Theta phase coherence in affective picture processing reveals dysfunctional sensory integration in psychopathic offenders

Abstract

Psychopathic offenders are described as emotionally cold, displaying deficits in affective responding. However, research demonstrates that many of the psychopathy-related deficits are moderated by attention, such that under conditions of high attentional and perceptual load psychopathic offenders display deficits in affective responses, but do not in conditions of low load. To date, most studies use measures of defensive reflex (i.e., startle) and conditioning manipulations to examine the impact of load on psychopathy-related processing, but have not examined more direct measures of attention processing. In a sample of adult male offenders, the present study examined time-frequency EEG phase coherence in response to a picture-viewing paradigm that manipulated picture familiarity to assess neural changes in processing based on perceptual demands. Results indicated psychopathy-related differences in the theta response, an index of readiness to perceive and integrate sensory information. These data provide further evidence that psychopathic offenders have disrupted integration of sensory information.

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.