psychopathyparalimbic.pdf

Psychiatry Research 142 (2006) 107–128

www.elsevier.com/locate/psychres

Review article

A cognitive neuroscience perspective on psychopathy:

Evidence for paralimbic system dysfunction

Kent A. Kiehl *

Olin Neuropsychiatry Research Center, Institute of Living, 200 Retreat Ave, Hartford, CT, 06106, USA

Departments of Psychiatry and Psychology, Yale University, New Haven, CT, USA

Received 18 May 2005; received in revised form 1 September 2005; accepted 12 September 2005

Abstract

Psychopathy is a complex personality disorder that includes interpersonal and affective traits such as glibness, lack of

empathy, guilt or remorse, shallow affect, and irresponsibility, and behavioral characteristics such as impulsivity, poor

behavioral control, and promiscuity. Much is known about the assessment of psychopathy; however, relatively little is

understood about the relevant brain disturbances. The present review integrates data from studies of behavioral and cognitive

changes associated with focal brain lesions or insults and results from psychophysiology, cognitive psychology and cognitive

and affective neuroscience in health and psychopathy. The review illustrates that the brain regions implicated in psychopathy

include the orbital frontal cortex, insula, anterior and posterior cingulate, amygdala, parahippocampal gyrus, and anterior

superior temporal gyrus. The relevant functional neuroanatomy of psychopathy thus includes limbic and paralimbic structures

that may be collectively termed d the paralimbic system T . The paralimbic system dysfunction model of psychopathy is discussed

as it relates to the extant literature on psychopathy.

D 2006 Published by Elsevier Ireland Ltd.

Keywords: Psychopathy; Cognitive neuroscience; Affective neuroscience; Review; fMRI; ERP

Contents

1. Introduction.................................................... 108

2. The construct and assessment of psychopathy .................................. 108

3. Neurology and psychopathy ........................................... 110

4. Neuropsychological test findings in psychopathy................................. 113

5. Abnormalities in neurocognitive function in psychopathy ............................ 113

6. Language processes and psychopathy ...................................... 113

* Tel.: +1 860 545 7385; fax: +1 860 545 7797.

E-mail address: kent.kiehl@yale.edu .

0165-1781/$ - see front matter D 2006 Published by Elsevier Ireland Ltd.

doi: 10.1016/j.psychres.2005.09.013

108

K.A. Kiehl / Psychiatry Research 142 (2006) 107–128

7. Attention and orienting processes in psychopaths ................................. 116

8. Affective processes in psychopathy ........................................ 120

9. Psychopathy as a disorder of the paralimbic system ............................... 122

Acknowledgements ................................................... 124

References ....................................................... 124

1. Introduction

psychotic symptoms or defects in intellectual func-

tion. In the 200 years that followed, the condition has

been through an evolution in terminology, but many

of the defining characteristics have remained un-

changed. These characteristics were most clearly

delineated, and the current diagnostic criteria estab-

lished, by the writings of the psychiatrist Hervey

Cleckley (1941) . In his 40 years of clinical work,

Cleckley came to narrow the syndrome he called

psychopathy to 16 characteristics. Affectively, psy-

chopaths are callous, shallow, and superficial, and

they lack insight and empathy for the effect their poor

behavior has on others; behaviorally, psychopaths are

impulsive, nomadic, and have weak behavioral

control.

In subsequent years, Hare and colleagues oper-

ationalized and transformed Cleckley’s characteristics

into items on the Hare Psychopathy Checklist ( Hare,

1980 ) and its successor, the Hare Psychopathy

Checklist-Revised (PCL-R; Hare, 1991, 2003 ) . The

PCL-R is now the most widely accepted diagnostic

instrument for psychopathy. There is a substantial

literature attesting to the reliability and validity of the

PCL-R as a measure of psychopathy in incarcerated

offenders, forensic patients, psychiatric patients, and

substance abuse patients (see Hare, 2003 , fora

review). The items on the PCL-R are listed in Table 1 .

The PCL-R assessment is performed by reviewing

the participant’s institutional records, including intake

assessments, social worker assessments, and reports

of institutional adjustment and transgressions. A semi-

structured interview covering school adjustment,

employment, intimate relationships, family, friends,

and criminal activity is conducted. Explicit criteria

detailing each item are reviewed from the PCL-R

manual, and each item is scored on a three point scale:

0—does not apply, 1—applies somewhat, and 2—

definitely applies, to the individual. The resulting

scores range from 0 to 40, and the recommended

diagnostic cutoff for psychopathy is 30 ( Hare, 1991,

2003 ). Interviews are typically video taped so that an

Psychopathy is a serious mental health disorder.

Psychopathy is believed to affect approximately 1%

of the general population, 15–25% of the male and

female prison population ( Hare, 1991, 2003 ) , and 10–

15% of substance abuse populations ( Alterman and

Cacciola, 1991; Alterman et al., 1993, 1998 ). Over the

last 20 years, much has been learned about the

assessment and characterization of the forensic and

legal aspects of psychopathy. However, compared

with other psychiatric disorders of similar prevalence,

relatively little is known about the neural systems

implicated in psychopathy. This review will draw on

information from multiple disciplines, including

neurology, psychiatry, psychology, cognitive neuro-

science, psychophysiology, and epileptology. The

literatures will be integrated and a new model of the

functional neuroanatomy underlying psychopathy will

be presented. The review is offered in several parts.

First, the assessment and classification of psychopathy

is reviewed. The second part of the review will draw

upon indirect evidence from studies of how insults or

damage to regions of the brain may lead to symptoms

and cognitive abnormalities consistent with those

observed in psychopathy suggesting that these latter

circuits may be implicated in the disorder. The third

part of the review focuses on the cognitive and

affective neuroscience studies of psychopathy. Finally,

a new model of the functional neuroanatomy under-

lying psychopathy will be presented.

2. The construct and assessment of psychopathy

The modern concept of psychopathy can be traced

back to the psychiatrist Pinel (1792 as cited in

Cleckley, 1941 ) , who labeled the condition d madness

without delirium T . This term was used to denote the

lack of morality and behavioral control in these

individuals that occurred despite the absence of any

K.A. Kiehl / Psychiatry Research 142 (2006) 107–128

109

Four-factor

model

1 Glibness/superficial charm 1 1

2 Grandiose sense of self-worth 1 1

3 Need for stimulation 2 3

4 Pathological lying 1 1

5 Conning/manipulative 1 1

6 Lack of remorse or guilt 1 2

7 Shallow affect 1 2

8 Callous/lack of empathy 1 2

9 Parasitic lifestyle 2 3

10 Poor behavioral controls 2 4

11 Promiscuous sexual behavior – –

12 Early behavioral problems 2 4

13 Lack of realistic, long-term goals 2 3

14 Impulsivity 2 3

15 Irresponsibility 2 3

16 Failure to accept responsibility 1 2

17 Many marital relationships – –

18 Juvenile delinquency 2 4

19 Revocation of conditional release 2 4

20 Criminal versatility – 4

The items corresponding to the early two-factor conceptualization

of psychopathy ( Harpur et al., 1988, 1989 ) and current four-factor

model are listed ( Hare, 2003 ) . The two-factor model labels are

Interpersonal/Affective (Factor 1) and Social Deviance (Factor 2)

and the four-factor model labels are Interpersonal (Factor 1),

Affective (Factor 2), Lifestyle (Factor 3), and Antisocial (Factor 4).

Items followed by a dash did not load on any factor.

grounds of specificity in forensic populations ( Hart

and Hare, 1996 ). Nearly 80–90% of inmates in a

maximum security prison fulfill the criteria for ASPD,

while only 15–25% score above the diagnostic

criteria for psychopathy. In addition, the diagnostic

confusion of psychopathy as putatively measured by

ASPD and the complex relationships of these con-

structs with substance disorders have led to consid-

erable confusion and hampered research efforts. It is

important to stress that proper psychometric assess-

ment of a condition is crucial, particularly when

trying to relate it to psychophysiological or cognitive

neuroscience data. The review below will largely be

constrained to studies that employed psychometric

measures consistent with the classic conceptualization

of psychopathy. That is, the preferred conceptualiza-

tion of psychopathy is a disorder that includes both

interpersonal and affective characteristics and deviant

behavior.

Recent psychometric analyses, using Item Re-

sponse Theory (IRT), of PCL-R scores from large

diverse multicultural samples have revealed a two-

factor four-facet model (see Table 1 ; Hare, 2003 ) .

This model includes facets labeled, Interpersonal

(Factor 1), Affective (Factor 2), Lifestyle (Factor 3),

and Antisocial (Factor 4) (but see also Cooke and

Michie, 1997 , for a three-factor model). There have

been few studies that have examined the neuro-

cognitive correlates of the factor models of psychop-

athy ( Patrick et al., 1993, 1994; Raine et al., 2004;

Soderstrom et al., 2002; Sutton et al., 2002 ).

However, as in complex disorders such as schizo-

phrenia, relating specific symptom clusters to patterns

of cerebral activity may clarify the relevant brain

disturbances and help reconcile discrepant findings

( Liddle, 2001 ) . It may be fruitful therefore to relate

psychophysiological and cognitive neuroscience

measures to the factors of psychopathy. A potential

problem with this method, however, is that the factors

of psychopathy are often strongly correlated, making

it difficult to relate neural correlates to the symptom

profiles.

In summary, research over the last 20 years has

made great strides in characterizing the psychometric

assessment and classification of psychopathy. The

classic conceptualization of psychopathy is a disorder

that includes both interpersonal and affective charac-

teristics and behavioral traits.

independent rating can be obtained. The total assess-

ment time typically ranges from 2 to 5 h, it is rigorous,

and training is required.

Early factor analyses of the PCL-R items revealed

two correlated factors (see Table 1 ; Harpur et al.,

1988, 1989 ). Factor 1 included items related to

emotional and interpersonal relationships. Factor 2

items reflected impulsive and antisocial behaviors.

This latter factor is most closely related to the

Diagnostic and Statistical Manual of Mental Disorders

(DSM-IV) classification of Antisocial Personality

Disorder (ASPD; American Psychiatric Association,

1994 ). It is important to note that ASPD has been

criticized for overly relying on antisocial behaviors,

while excluding many of the affective and interper-

sonal characteristics considered to be central to the

construct of psychopathy ( Alterman et al., 1998; Hare,

1996; Hare et al., 1991; Hart and Hare, 1996; Widiger

et al., 1996 ). ASPD also has been questioned on

Table 1

The 20 items listed on the Psychopathy Checklist-Revised ( Hare,

1991, 2003 )

Item

Two-factor

model

110

K.A. Kiehl / Psychiatry Research 142 (2006) 107–128

3. Neurology and psychopathy

aggression — a cardinal feature of psychopathy ( Blair,

2001; Hare, 1993 ). Orbital frontal patients also do not

typically exhibit the callousness commonly observed

in psychopathic individuals. Similarly, patients with

d acquired sociopathy T , unlike psychopathic individu-

als, are characterized by lack of motivation, hoarding

behavior, mood disturbances, incontinence, and fail-

ure or inability to make long-term plans ( Blumer and

Benson, 1975 ). Psychopathic individuals, on the other

hand, often enjoy making grandiose life plans — they

just fail to follow through with them.

Patients with orbital frontal lesions show impair-

ment on affective voice and face expression identifi-

cation tasks ( Hornak et al., 1996, 2003 ) , response

reversal or extinction ( Blair and Cipolotti, 2000; Rolls

et al., 1994 ), and decision-making ( Bechara et al.,

2000 ). The animal literature shows that lesions to

orbital frontal cortex impair inhibitory performance on

No Go trials of Go/No Go paradigms ( Iversen and

Mishkin, 1970 ). Psychopaths have problems with

processing certain aspects of affective speech and face

stimuli ( Blair et al., 1997; Kosson et al., 2002; Louth

et al., 1998 ). Psychopaths, under certain contextual

demands, also show poor response inhibition ( Kiehl,

2000; Lapierre et al., 1995 ), response modulation

( Newman and Kosson, 1986; Newman et al., 1987,

1992; Newman and Schmitt, 1998 ) and more recently

response reversal ( Mitchell et al., 2002 ) . Boys with

psychopathic tendencies and adult psychopaths tend

to show impairments on the Bechara gambling test of

decision making ( Blair, 2001; Mitchell et al., 2002 ) ,

though not all studies have found this effect ( Schmitt

et al., 1999 ).

In summary, damage to the orbital frontal cortex

appears to be associated with some symptoms and

cognitive impairments that may also be found in

psychopaths. However, despite these apparent similar-

ities, no studies have actually explicitly investigated

how orbital frontal patients score on psychopathy

measures. Similarly, many of the studies of cognitive

function in psychopathy and orbital frontal patients

have used different cognitive tests, making inferences

between studies problematic. It is only recently that

identical tasks (i.e., response reversal) have been

examined in both orbital frontal patients and in

samples of psychopathic individuals ( Mitchell et al.,

2002 ). Nevertheless, it appears that lesions to orbital

frontal cortex appear to elicit behaviors that most

One way to examine the possible neural regions

implicated in psychopathic behavior is to draw from

studies of behavioral changes and cognitive impair-

ments associated with damage to specific brain circuits.

It is important to recognize that this method provides

only indirect evidence of the possible regions impli-

cated in psychopathic symptomatology; nevertheless,

some interesting and compelling data have accumulat-

ed. The most notable neurological case study is that of

the railroad worker Phineas Gage ( Harlow, 1848 ) .

Gage suffered penetrating trauma to the prefrontal

cortex ( Damasio et al., 1994 ) . He was transformed by

this accident from a responsible railroad manager to an

impulsive, irresponsible, sexually promiscuous, ver-

bally abusive individual ( Harlow, 1848 ) . Many of

Gage’s symptoms are consistent with those classically

associated with psychopathy.

Subsequent studies of patients with prefrontal lobe

damage suggest that the orbital frontal cortex plays a

role in mediating some behaviors related to psychop-

athy ( Blumer and Benson, 1975; Damasio, 1994 ) .

Damage to the orbital frontal cortex leads to a

condition termed d pseudopsychopathy T ( Blumer and

Benson, 1975 )or d acquired sociopathic personality T

( Damasio, 1994 ) characterized by problems with

reactive aggression, motivation, empathy, planning

and organization, impulsivity, irresponsibility, insight,

and behavioral inhibition ( Malloy et al., 1993; Stuss et

al., 1983 ). In some cases, patients may become prone

to grandiosity ( Blumer and Benson, 1975 ) and

confabulation ( Malloy et al., 1993; Schnider, 2001 ) .

Recent studies suggest that bilateral damage to orbital

frontal cortex is necessary to elicit changes in social

behavior ( Hornak et al., 2003 ) . Moreover, patients with

gross, extensive damage due to stroke or closed head

injury are more likely to exhibit d acquired sociopathic T

symptomology than are patients with focal, circum-

scribed surgical lesions to orbital frontal cortex

( Hornak et al., 2003 ) . These data suggest that some

aspects of psychopathic symptomatology may map

onto the (dys)function of orbital frontal cortex and

adjacent regions. However, the d pseudopsychopathy T

or d acquired sociopathy T model does not appear to fully

account for the constellation of symptoms observed in

psychopathy. For example, patients with orbital frontal

damage rarely show instrumental or goal-directed

K.A. Kiehl / Psychiatry Research 142 (2006) 107–128

111

consistently map onto the Affective (Factor 2) and

Lifestyle (Factor 3) factors of the four-factor psychop-

athy model. These factors of psychopathy include

symptoms of impulsivity, irresponsibility, and stimu-

lation seeking as well as a general lack of empathy. In

some cases, orbital frontal patients’ symptomatology

may be similar to the Interpersonal items (Factor 1),

which include superficial charm, grandiose sense of

self-worth, and pathological lying. Thus, while the

d pseudopsychopathy T or d acquired sociopathy T model

appears to mimic some features of psychopathy, the

two disorders differ in many respects. This raises the

possibility that disturbances in brain regions other than

orbital frontal cortex may contribute to psychopathy.

Other brain regions that may be implicated in

psychopathy include the anterior cingulate. The ante-

rior cingulate is a multifaceted complex structure that is

commonly divided into at least two distinct functional

regions ( Devinsky et al., 1995 ) . The rostral aspect,

often termed the d affective T division, is known to be

involved in pain perception and affect regulation ( Bush

et al., 2000 ). The caudal region, termed the d cognitive T

division, is known to be involved with response

conflict, error monitoring, and task switching, among

other processes ( Kiehl et al., 2000a ) . Selective lesions

to the anterior cingulate are rare, but when they do

occur, they tend to be related to emotional unconcern

( Mesulam, 2000 ) , hostility, irresponsibility, and dis-

agreeableness ( Swick, 2003 ) . Recently, Hornak and

colleagues have shown that selective lesions to bilateral

anterior cingulate cortex produce disturbances in

personality functioning similar to those observed in

patients with orbital frontal lesions ( Hornak et al.,

2003 ). In humans, anterior cingulate lesions lead to

perseveration ( Mesulam, 2000 ) , difficulties in affective

face and voice identification ( Hornak et al., 2003 ) , error

monitoring ( Swick and Jovanovic, 2002; Swick and

Turken, 2002; Turken and Swick, 1999 ) and response

inhibition abnormalities ( Degos et al., 1993; Tekin and

Cummings, 2002 ). Psychopathy has long been associ-

ated with perseveration (see review by Newman,

1998 ), apathy ( Cleckley, 1941; McCord and McCord,

1964 ), difficulties in identifying some affective face

stimuli ( Blair et al., 1997; Kosson et al., 2002 ) , and

more recently, error monitoring ( Bates et al., submitted

for publication ) and response inhibition abnormalities

( Kiehl et al., 2000b; Lapierre et al., 1995 ) . Studies also

have shown that the volume of the right anterior

cingulate is positively correlated with harm avoidance

( Pujol et al., 2002 ) . Psychopaths are known to score

low on harm-avoidance measures ( Hare, 1991 ) . Thus,

it would appear that bilateral damage to the anterior

cingulate and/or orbital frontal cortex may lead to

symptoms and cognitive impairments similar to those

observed in psychopathy. The facets of psychopathy

that appear to map onto anterior cingulate dysfunction

include the Affective (Factor 2) and Lifestyle (Factor 3)

factors of the four-factor psychopathy model ( Hare,

2003 ). These latter facets include symptoms of lack of

empathy, shallow affect, impulsivity, and irresponsi-

bility. These symptoms appear to be prevalent in

patients with anterior cingulate damage ( Mesulam,

2000; Swick, 2003 ).

In addition to regions of the frontal cortex, regions in

the temporal lobe may be linked to some symptoms of

psychopathy. Damage to the medial temporal lobe in

general ( Kluever and Bucy, 1938, 1939 ) , and neural

tracts that pass through the amygdala in particular

( Aggleton, 1992 ) , have long been associated with

emotional and behavioral changes in monkeys. These

changes include an unnatural propensity for approach

behavior or fearlessness and unusual tameness. Medial

temporal lobe lesioned monkeys also show excessive

fascination with objects, often placing them in the

mouth, and general hyperactivity and hypersexual

activity. This collection of behaviors has been termed

the Kluever–Bucy syndrome. Only a small minority of

humans with damage to bilateral amygdala exhibit the

full manifestation of the Kluever–Bucy syndrome,

while the majority developed less severe emotional

changes ( Adolphs and Tranel, 2000 ) . One case study

reported that bilateral amygdala damage due to

calcification associated with Urbach–Wiethe disease

may be related to mild antisocial behavior, including

rebelliousness, disregard for social convention, and

lack of respect for authorities ( Adolphs and Tranel,

2000 ).

Detailed psychological and personality assess-

ments of patients with temporal lobe epilepsy suggests

a high incidence of psychopathic-like behavior.

Indeed, some studies have reported that pre-opera-

tively the prevalence of psychopathic-like behaviors is

as high as 70% of patients with anterior temporal lobe

epilepsy ( Blumer, 1975; Hill et al., 1957 ) . Structures

that are commonly implicated in temporal lobe

epilepsy include the amygdala, hippocampus, para-

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