Neurocognitive Function in Antisocial Personality Disorder
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Psychiatry Research 97Ž. 2000 173᎐190 Neurocognitive function in antisocial personality disorder Wayne M. DinnU, Catherine L. Harris Department of Psychology, Boston Uni¨ersity, 64 Cummington Street, Boston, MA 02215, USA Received 20 March 2000; received in revised form 6 September 2000; accepted 22 September 2000 Abstract Recent neuroimaging studies and neuropsychological test ®ndings support the contention that prefrontal dysfunc- tion is associated with psychopathic personality traits and antisocial behavior. However, con¯icting results have arisen regarding performance on measures of frontal executive function. We administered a neuropsychological test battery consisting of measures sensitive to frontal lobe dysfunction and a battery of personality questionnaires and clinical scales sensitive to antisocial personality disorderŽ. APD subjects presenting with prominent psychopathic personality features and matched control subjects. We also monitored the subjects' electrodermal activity during the presentation of emotionally charged stimuli. APD subjects showed greater neuropsychological de®cits on measures sensitive to orbitofrontal dysfunction in comparison to control participants. Moreover, APD subjects were electroder- mally hyporesponsive to aversive stimuli relative to control group members. APD subjects did not demonstrate performance de®cits on classical tests of frontal executive function. Participants also underwent clinical assessment. As expected, APD subjects were less conscientious, self-reproaching, guilt-prone, and socially anxious than matched control subjects. Moreover, the scores indicated that APD subjects were more venturesome and uninhibited relative to control subjects. Contrary to expectations, APD subjects and community control subjects did not differ on a self-report measure of sensitivity to speci®c phobic situations. ᮊ 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Psychopathy; Frontal lobe; Orbitofrontal; Dorsolateral᎐prefrontal; Neuropsychological; Electrodermal U Corresponding author. 42 Washington Terrace, Whitman, MA 02382, USA. Tel.: q1-617-353-1362. E-mail address: [email protected]Ž. W.M. Dinn . 0165-1781r00r$ - see front matter ᮊ 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 5 - 1 7 8 1Ž. 0 0 00224-9 174 W.M. Dinn, C.L. Harris rPsychiatry Research 97() 2000 173᎐190 1. Introduction function de®cits are associated with antisocial personalityŽ. APD . Morgan and Lilienfeld Ž. 2000 1.1. Prefrontal dysfunction and psychopathy found a signi®cant relationship between executive function de®cits and antisocial behavior. Recent neuroimaging studies and neuropsycho- In response to Gorenstein's study, HareŽ. 1984 logical test ®ndings support the contention that assigned inmates to low-, medium-, and high-psy- prefrontal dysfunctionŽ. particularly orbitofrontal chopathy groups and administered the aforemen- is associated with psychopathic personality traits tioned frontal executive function tasks. No sig- and antisocial behaviorŽ Davidson et al., 2000; ni®cant group differences were observed. Hare Raine et al., 1998, 2000; Lapierre et al., 1995. was unable to replicate Gorenstein's ®ndings. However, con¯icting results have arisen regarding Sutker and AllainŽ. 1987 also found that psycho- the performance of psychopathic subjects on pathic subjects and control subjects performed measures of frontal executive function. similarly on measures of concept formation, ab- Several studies suggest that a select de®cit in- straction, and planning. How can we account for volving the orbitofrontal system may underlie psy- these con¯icting ®ndings? One possibility is that chopathy and antisocial behavior. Lapierre et al. the executive function de®cits among psycho- Ž.1995 found that incarcerated psychopathic sub- pathic subjects are associated with the presence jects were signi®cantly impaired on tasks con- of comorbid psychiatric conditions, while the core sidered sensitive to orbitofrontalrventrome- interpersonal and affective characteristics associ- dial᎐prefrontal dysfunction including a visual ated with psychopathyŽ e.g., egocentricity, callous- gorno᎐go discrimination task, Porteus Maze Q- ness, manipulativeness, guile, lack of empathy scoresŽ. i.e., rule-breaking errors , and an odor and remorse. may result from orbitofrontal dys- identi®cation task in comparison to matched con- function. trol subjectsŽ. non-psychopathic inmates . Lapierre et al.Ž. 1995 also found that psychopathic subjects 1.2. Executi¨e function and APD did not display performance de®cits on measures sensitive to dorsolateral᎐prefrontalŽ. DLPF and Several studies examining neurocognitive func- posterorolandic functionŽ i.e., the Wisconsin Card tion in psychopathy and APD reveal broadly Sorting TestŽ. WCST and the Mental Rotation frontal de®cits, but if the prefrontal cortex can be Task.Ž. Moreover, Deckel et al. 1996 reported fractionated into separate frontal subsystems, that performance on tests assessing frontal execu- these may be differentially engaged in APD sub- tive functioningŽ e.g. the WCST, controlled oral types. One possibility is that APD subjects de- word ¯uency test, and trail-making test. failed to monstrating core psychopathic traits and a lack of predict antisocial personality disorder classi®ca- foresightŽ e.g., dif®culty anticipating negative con- tions. These tasks are considered sensitive indica- sequences. , planning, and goal-directed behavior tors of DLPF dysfunctionŽ i.e., tasks which re- Ž.e.g., disorganized offending will show greater quire the employment of organizational strategies neuropsychological de®cits on tasks considered for ef®cient performance. These ®ndings suggest sensitive to orbitofrontal dysfunction and on mea- that a select orbitofrontal de®cit may be associ- sures of frontal executive function. Speci®cally, ated with psychopathy. core psychopathic personality characteristics may However, GorensteinŽ. 1982 reported that psy- result from orbitofrontal dysfunction. The addi- chopathic subjects demonstrated performance tional involvement of DLPF dysfunction may lead de®cits on tests of frontal executive function in- to antisocial behavior that combines core psycho- cluding the WCSTŽ. i.e., perseverative errors , pathic characteristics with poor planning and or- Necker cube task, and a sequential matching me- ganization, and dif®culty keeping in mind diverse mory task. A recent meta-analytic review of 39 future consequences. Motivation for this hypothe- studies by Morgan and LilienfeldŽ. 2000 lends sis is that the DLPF cortex mediates executive strong support to the contention that executive functionsŽ. Smith and Jonides, 1999 , while the W.M. Dinn, C.L. Harris rPsychiatry Research 97() 2000 173᎐190 175 orbitofrontal cortex mediates sensitivity to dy- cation Test to investigate olfactory function. Ol- namically changing reinforcement contingencies, factory identi®cation tasks have been used to and thus may be particularly important for modu- assess the functional integrity of orbitofrontal lating individuals' response to the social world cortex. The orbitofrontal region plays a major and other threat-laden situations. role in odor discrimination, and olfactory agnosia has been reported in patients with damage to the 1.3. Is orbitofrontal dysfunction the key to orbitofrontal aspect of the prefrontal cortex. psychopathy? Jones-Gotman and ZatorreŽ. 1988 reported that patients with focal surgical brain lesions involving Numerous case reports describe the emergence orbitofrontal cortex were impaired on an odor of psychopathic behavior following orbitofrontal identi®cation task. damage. Striking alterations in personality have The fact that orbitofrontal lesion patients un- been well-documented. These patients demon- dergo a dramatic personality changeŽ alterations strate social disinhibition, shallow affect, de- which strongly resemble primary psychopathy. is creased empathy, and impulsive, antisocial behav- an intriguing line of evidence which lends support iorŽ Blumer and Benson, 1975; Cummings, 1993; to the contention that orbitofrontal dysfunction is Damasio, 1994; Damasio and Van Hoesen, 1983; associated with psychopathy. However, we are not Grattan et al., 1994; Martzke et al., 1991; Meyers suggesting that an orbitofrontal lesion is an etio- et al., 1992; Stuss et al., 1992. Meyers et al. logic factor in psychopathy or APD. Rather, we Ž.1992 reported post-operative behavioral changes support the hypothesis that orbitofrontal hypoac- which ``strongly resembled'' APD in a 33-year-old tivity, in the absence of gross lesions, underlies male with left orbitofrontal damage following primary psychopathyŽ. Lapierre et al., 1995 . Neu- surgery for a pituitary tumor. It is noteworthy ropsychological test performance patterns and that cognitive abilities are generally preserved in atypical electrodermal responses among psycho- these patients, suggesting a highly selective dis- pathic subjects are consistent with the notion that ruption. orbitofrontal hypometabolism may underlie psy- A signi®cant body of research suggests that the chopathy. orbitofrontal system plays a major role in regulat- ing the individual's emotional response to aver- 1.4. Psychophysiological testing, psychopathy, and sive stimuli. CummingsŽ. 1993 described the the orbitofrontal hypothesis emergence of a disinhibition syndrome following damage to the orbitofrontal region. Moreover, he Although atypical electrodermal responses is noted that damage to subcortical structuresŽ e.g., associated with damage