Elsevier

Biological Psychiatry

Volume 50, Issue 9, 1 November 2001, Pages 677-684
Biological Psychiatry

Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging

https://doi.org/10.1016/S0006-3223(01)01222-7Get rights and content

Abstract

Background: Psychopathy is a complex personality disorder of unknown etiology. Central to the disorder are anomalies or difficulties in affective processing.

Methods: Functional magnetic resonance imaging was used to elucidate the neurobiological correlates of these anomalies in criminal psychopaths during performance of an affective memory task.

Results: Compared with criminal nonpsychopaths and noncriminal control participants, criminal psychopaths showed significantly less affect-related activity in the amygdala/hippocampal formation, parahippocampal gyrus, ventral striatum, and in the anterior and posterior cingulate gyri. Psychopathic criminals also showed evidence of overactivation in the bilateral fronto-temporal cortex for processing affective stimuli.

Conclusions: These data suggest that the affective abnormalities so often observed in psychopathic offenders may be linked to deficient or weakened input from limbic structures.

Introduction

Psychopathy is a personality disorder believed to affect approximately 1% of the general population and approximately 15%–25% of incarcerated offenders (Hare 1991). Compared with other inmates, psychopathic offenders commit a disproportionate amount of repetitive, often violent, criminal acts Hare and McPherson 1984, Hart et al 1994. Central to the disorder is a complex of features—glibness; superficiality; and lack of empathy, guilt, or remorse—that appear to be associated with difficulties or anomalies in the processing and production of affective material Cleckley 1976, Hare 1993. Although the clinical symptomology of criminal psychopathy is well characterized (Hare 1991), relatively little is known regarding the neural systems mediating its affective abnormalities.

Most empirical research on the affective processes of psychopathic criminals has used behavioral methods or peripheral measures of neural activity (Patrick 1994). One of the most consistent findings from these studies is that criminal psychopaths fail to experience or appreciate the emotional significance of stimuli in the way that nonpsychopaths do Christianson et al 1996, Day and Wong 1996, Kiehl et al 1999, Louth et al 1998, Patrick et al 1993, Patrick et al 1994, Williamson et al 1991. For example, data from our laboratory has shown that criminal psychopaths fail to show normal behavioral facilitation and event-related potential (ERP) differentiation between emotional and neutral words (Williamson et al 1991). Subsequent research has confirmed the presence of affective abnormalities in criminal psychopaths (Kiehl et al 1999). These deficits appear to be most prominent in response to negatively valenced emotional stimuli Day and Wong 1996, Patrick et al 1993, Patrick et al 1994. Although ERPs have provided valuable information regarding the temporal features of these abnormalities, their limited spatial resolution has left the neural sources poorly characterized. One functional imaging study, using Single Photon Emission Computed Tomography (SPECT), found that psychopathic individuals show greater activation for affective than for neutral stimuli bilaterally in temporo-frontal cortex (Intrator et al 1997). These latter data have been interpreted as supporting the notion that psychopathic individuals require more cognitive resources to process and evaluate affective stimuli than do comparison subjects. We note however that this latter study was limited in that it only assessed function in a 13.5 mm axial slice of cortex.

Researchers have suggested that a number of neural structures and systems may be implicated in psychopathic behavior. These regions include orbital frontal cortex (Damasio et al 1990), prefrontal cortex Anderson et al 1999, Bechara et al 1994, Raine et al 2000, ventro-medial frontal cortex (Bechara et al 1999b), and limbic structures such as the amygdala Bechara et al 1999b, Patrick et al 1993, Patrick et al 1994, Tranel and Damasio 1994 and cingulate Dikman and Allen 2000, Tranel and Damasio 1994. Unfortunately, very little is known about the possible involvement of these structures in criminal psychopathy.

The purpose of the present study was to use whole brain functional magnetic resonance imaging (fMRI) to examine the neural systems underlying emotional processing in psychopathic offenders during performance of an affective memory task. The affective memory task consisted of eight repetitions of three phases (encoding, rehearsal, and recognition) plus rest. Unknown to the participants, four of the repetitions contained stimuli that were negative in affect, while in the remainder of the repetitions the stimuli were neutral in affect. Prior pilot research with this task revealed that affective stimuli elicit greater activation than do neutral stimuli in both limbic and neocortical brain regions, including the amygdala, hippocampal formation, and temporal and frontal cortex (see Table 1) (Kiehl et al 1998). In light of the substantial evidence indicating impaired processing of affect in psychopathy, we hypothesized that psychopaths would show less activation than healthy controls and criminal nonpsychopaths when processing affective words compared with neutral words, at those cerebral sites where healthy controls had exhibited significant activation for affective words compared with neutral words in the pilot study.

Section snippets

Methods and materials

Criminal psychopaths (n = 8) and criminal nonpsychopaths (n = 8) were inmates from a maximum-security prison located in Abbotsford, British Columbia, Canada. Inmates were escorted to the University of British Columbia Hospital’s magnetic resonance imaging (MRI) unit by the Correctional Services of Canada Regional Escort Team. Matched healthy control participants (n = 8) were recruited from the general population. All participants were free from any documented history of serious head injury

Behavioral Data

Consistent with previous research, negative words were recalled more accurately than were neutral words (main effect of Word, F (1, 21) = 20.01, p < .000097). There were no group differences in affective processing, relative to neutral processing (Group × Word interaction, F (2, 21) = 4.82, p = .59); however, the effect of word type was most pronounced in the criminal nonpsychopaths (F (1, 21) = 9.44, p < .006; percentage correct for neutral 83.60 (SD 4.91) and negative 90.63 (SD 5.10) words)

Discussion

This study was designed to elucidate and characterize the abnormal functional architecture underlying affective processing in psychopathic offenders in the context of a memory task. The results support the hypothesis that criminal psychopathy is associated with abnormalities in the function of structures in the limbic system and frontal cortex while engaged in processing of affective stimuli. These structures primarily included anterior and posterior cingulate, inferior frontal gyrus,

Acknowledgements

This research was supported by grants from the Medical Research Council (MRC) of Canada. The first author was supported by the Michael Smith Graduate Scholarship, Medical Research Council of Canada. We would like to thank Drs. Alex MacKay and Ken Whittall for their assistance. We gratefully acknowledge the programming assistance of Tim Duty, Adrien Desjardins, and Krish Singh (mri3dX) and MR technicians Trudy Shaw, Sylvia Renneberg, and Karen Smith. This research could not have been performed

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