Neurocase (2006) 12, 164–178 Copyright © Taylor & Francis Group, LLC ISSN: 1355-4795 print DOI: 10.1080/13554790600611288
Divergent Patterns of Aggressive and Neurocognitive Characteristics in Acquired Versus Developmental Psychopathy NNCS
D.G.V. MITCHELL1, S.B. AVNY1,2 and R.J.R. BLAIR1 Acquired Versus Developmental Psychopathy
1
Mood and Anxiety Disorders Program, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA 2 Psychology Department, University of Maryland, College Park, MD, USA
An analogy is often drawn between patients with personality changes following orbitofrontal cortex lesions and individuals with developmental psychopathy. We present patient CL, who had acquired psychopathy following an orbitofrontal cortex lesion. Unlike previous studies, CL was assessed on a valid and reliable measure of psychopathy and was compared with controls and patients with developmental psychopathy on measures of instrumental (re)learning, extinction, emotional processing, and social cognition. The results provide further support for the notion that acquired and developmental forms of psychopathy are associated with dissociable neurocognitive deficits that leave each at different levels of risk for reactive and instrumental aggression.
Introduction Frontal lobe damage has been associated with profound changes in personality and emotional responding including increased irresponsibility, promiscuity, impulsivity and poor planning (Damasio, 1994). Lesions of the orbitofrontal cortex (OFC) are associated with disrupted occupational and social functioning, diminished regard for self and others, impulsivity, and reactive aggression (Burgess & Wood, 1990; Stuss et al., 1992; Damasio, 1994; Anderson et al., 1999). Accordingly, it has been suggested that such patients suffer from an acquired form of “psychopathy” (Blumer and Benson, 1975; Damasio, 1994; Anderson, 1999); developmental psychopathy is characterized by high rates of antisocial behavior and callousness that often manifest in childhood (Cleckley, 1967; Hare, 1983; 1991). However, we are aware of only one previous empirical investigation (Blair and Cipolotti, 2000) that included both patients with acquired and developmental psychopathy. The study presented here is an empirical investigation contrasting the neurocognitive correlates of acquired versus developmental psychopathy. Patients with OFC damage are at increased risk for deficits in decision-making (Bechara, et al., 1994; Damasio, 1994; Bechara et al., 1999), response reversal (Rolls et al., 1994; Rolls, 1996, 2004), extinction (Butter, 1969; Rolls et al., 1994), and emotional expression recognition (Hornak et al., Received 2 December 2005; accepted 1 February 2006. This research was supported by the Intramural Research Program of the NIH: NIMH. Address correspondence to Dr. D.G.V. Mitchell, Mood and Anxiety Disorders Program, National Institute of Mental Health, 15K North Drive, MSC 2670, Bethesda, Maryland, 20892. E-mail:
[email protected]
1996; Blair and Cipolotti, 2000). Similarly, individuals with developmental psychopathy show impaired decision-making (Blair et al., 2001a; Mitchell et al., 2002), response reversal (Mitchell et al., 2002), extinction (Newman et al., 1987), and emotional expression recognition (Blair et al., 2001a and b; Kosson et al., 2006). These similarities suggest neurocognitive parallels between OFC damage and developmental psychopathy. Despite the similarities between acquired and developmental psychopathy, important differences exist, particularly regarding the kind of aggression for which each is at risk. Reactive aggression is elicited by a frustrating or threatening event in the environment; it occurs without regard for any potential goal. Instrumental aggression is highly goaldirected aggression, usually aimed at material gain (e.g., obtaining the victim’s wallet), and need not occur with high levels of emotional arousal (Berkowitz, 1993). Acquired psychopathy is associated only with an increased risk for reactive aggression (Pennington and Ozonoff, 1996; Anderson et al., 1999; Blair, 2004). Developmental psychopathy, while associated with increased risk for reactive aggression, is particularly associated with heightened levels of instrumental aggression (Williamson et al., 1987; Cornell et al., 1996). The reactive aggression demonstrated by patients with acquired and developmental psychopathy may be related to a failure of orbital and ventrolateral prefrontal cortical regions to effectively regulate affective responding (Blair et al., 2001a; Mitchell et al., 2002; Blair, 2004). The instrumental aggression often seen in individuals with developmental psychopathy is thought to relate to difficulties with early socialization; it is argued that these difficulties result from disruption in the amygdala’s role in processing distress cues and in attaching emotional significance (positive or negative value) to stimuli in the environment (Blair, 2003). In support
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Acquired Versus Developmental Psychopathy of this position, individuals with developmental psychopathy show reduced startle reflex modulation (Patrick, 1994), impaired passive avoidance learning (Newman and Kosson, 1986), impaired extinction (Newman et al., 1987) or reversal (Mitchell et al., 2002), and impaired emotional expression recognition (particularly distress; Blair et al., 2001b; Blair et al., 2004b). Recent formulations suggest that dissociable cognitive functions relevant to emotional regulation are mediated by orbital and ventrolateral prefrontal cortex (Blair, 2004). Evidence suggests that separate systems for response reversal exist, which facilitate behavioral change to obtain abstract or unconditioned reward when reinforcement changes (Rolls, 1999). A second, social response reversal system modulates behavior when encountering disapproving social cues (Blair and Cipolotti, 2000) and in identifying and responding to socially inappropriate behavior (Berthoz et al., 2002). Dysfunction in either system can increase the risk for reactive aggression (Hornak et al., 1994; Blair, 2004); however, the systems may be dissociable on a neurocognitive level (Blair and Ciplotti, 2002; Blair, 2003; Blair et al., 2004). Here we present a case study involving patient CL. Following a severe penetrating head injury, CL showed evidence of a personality change consistent with “acquired” psychopathy. To our knowledge, this represents the first study in which psychopathy has been formally assessed in a case of acquired psychopathy using an empirically valid and reliable measure. His behavior is characterized by impulsivity, promiscuity, pathological lying, temper tantrums, and a callous disregard for the seriousness of his antisocial behavior. A series of experimental investigations were conducted to examine the cognitive dysfunction associated with his injury and explore how these deficits might relate to his profound social and emotional impairment. In light of the debate about the relationship between acquired and developmental psychopathy, the performance of CL was compared to an age-and IQ-matched healthy community sample, along with a small group of individuals with developmental psychopathy and a forensic control group. This enabled comparisons to be drawn between the neurocognitive deficits associated with acquired and developmental psychopathy. The tasks employed measured conditional learning (a form of stimulusresponse association formation), stimulus-reinforcement association learning and extinction, emotional expression recognition, and social cognition. “Theory of Mind” (ToM) is the ability to infer mental states such as thoughts, feelings, or intentions in others, and to predict and understand behavior on the basis of these mental states (Premack and Woodruff, 1978). In response to recent suggestions in the literature that ToM is compromised following lesions to the frontal lobes (Stone et al., 1998; Stuss and Anderson, 2004; ShamayTsoory et al., 2005), we also tested CL on two measures thought to be sensitive to ToM impairment. We predicted that CL and psychopathic individuals would show similar impairments on response reversal and extinction performance, but
dissociable instrumental acquisition and social response reversal impairments.
Methods Participants Case Report CL is a 51 year-old, right-handed male, who suffered a penetrating head injury at the age of 14 in a cycling accident. The injury required a series of operations to remove necrotic tissue and reconstruct the right frontal bone. A radiology report following a CAT scan was available for the year that the current study took place. It indicated two wedge-shaped low density lesions involving the frontal lobes bilaterally, suggesting bi-frontal infarcts. The left-sided lesion was of a lower density and appeared to be older in origin than the right-sided lesions. No other significant intra cerebral or extra axial lesions were noted. Figure 1 shows a Computerized Axial Scan of CL’s head and indicates the bilateral lesions involving the orbitofrontal cortex impinging on BA 10 and 11 and extending to BA 9 and 46. Prior to the accident, CL led a relatively unremarkable childhood without notable behavioral problems other than “minor truancy.” After his injury, however, he was reported to have become socially isolated. He left school without obtaining any qualifications and began to work. His work history thereafter was sporadic, and he was routinely dismissed from jobs within weeks or even days. He was first arrested as a young adult when he sexually assaulted and murdered a middle-aged woman. Psychiatric evaluations found no evidence of mental illness, but noted the patient’s striking disregard for the seriousness of his offense. After a few months of observation, the diagnosis “post-traumatic psychopathic disorder” was made by a psychiatrist, and CL was described as being a danger both to himself and to others. During periods in custody, reports indicate that CL lacked insight into his offense (offering conflicting versions of the offense, ranging from a full admission to complete denial that the murder even took place), had an unrealistically high self-opinion, and behaved in an abrasive, domineering, and confrontational manner.
Fig 1. Computerized Axial Tomography (CAT) scan of patient CL. The scan shows signs of severe necrosis in the frontal cortex. A radiology report concerning a CAT scan of the head reveals wedgeshaped low density lesions involving the frontal lobes bilaterally suggestive of frontal infarcts.
166 CL was discharged as an outpatient after being detained for approximately 15 years. Despite several allegations of serious aggressive behavior, CL’s only conviction in the first years following his release was of impaired driving. Individuals responsible for his care, however, felt that their safety was being threatened. Eventually, after several years as an outpatient, CL was again convicted of a sexual offense and was incarcerated. Specialists reported that his intake period was characterized by an impoverished sense of remorse. Again, it was suggested that CL suffered from psychopathy; however, details about the criteria used to reach this diagnosis were not available. Psychopathy Assessment CL was assessed using the Psychopathy Checklist-Revised (PCL-R; Hare, 1991). To our knowledge, this study is the first report of an individual with acquired psychopathy formally assessed on the PCL-R. The PCL-R is a reliable and valid instrument for assessing psychopathy in a prison population (Hare, 1991). The measure consists of 20 behavioral items that are scored using both file reviews and a semi-structured interview. Factor analyses reveal two distinct factors; factor 1 includes callous and unemotional characteristics while factor 2 refers to characteristics associated with antisocial behavior and lifestyle (Hare, 1991). Scores range from a possible 0 to 2 for each item (based on established criteria), thereby allowing for a maximum total score of 40. In North America, threshold for meeting criteria for psychopathy is a score of 30. CL’s total PCL-R score of 26.3 (77th percentile) indicates significant psychopathic characteristics. CL’s psychopathic characteristics were most pronounced on factor 1 (emotional component); he scored in the 90th percentile for male forensic patients. On factor 2, the antisocial lifestyle component, he showed less characteristics (41st percentile for male forensic patients). CL’s total score of 26.3 was therefore primarily driven by his affective characteristics; his interpersonal relations are characterized by high rates of poor behavioral controls, sexual promiscuity, grandiosity, glibness, and shallow affect. Neuropsychological Assessment CL received an extensive test of intellectual and executive functioning. The Wechsler Adult Intelligence Scale-Revised (WAIS-R), a subset of the Ravens Advanced Matrices, and the National Adult Reading Test all reveal an above average IQ (range from 114 to 124). He showed intact recognition memory as measured by the Recognition Memory Task for words but impaired recognition of faces (less than the 5th percentile). CL showed intact levels of executive functioning as measured by several indices including the Wisconsin Card Sorting Task and the Hayling Task. Table 1 shows CL’s performance on the measures of intelligence and the standardized neuropsychological test battery of memory and executive function.
D.G.V. Mitchell et al. Comparison Groups CL’s neurocognitive performance was contrasted with three comparison groups: five age-and IQ-matched community controls, five male prison inmates with developmental psychopathy, and five non-psychopathic control residents of the same forensic institutions. The community sample was matched on age and IQ; however, due to the demographics of the forensic institution accessed, it was not possible to obtain age-and IQ-matched forensic groups. Consequently, comparisons were primarily between CL and his community controls versus individuals with psychopathy and their forensic control group. Impairment was defined in each sample as the mean score falling outside the range of a 95% confidence interval (CI) constructed from the distribution of scores of the respective comparison groups. However, for descriptive purposes, we highlight instances in which significant differences exist between CL and the forensic samples. Psychopathy was assessed in the forensic samples using the PCL-R (Hare, 1991). All participants were pre-screened to exclude individuals who were older than 60 or whose psychiatric reports revealed a diagnosis of psychosis, organic brain damage, or neurological disorder. The Raven’s Advanced Progressive Matrix (Set I) was administered to provide an estimate of intelligence. There were no significant differences between the two forensic groups in either age (F(1,8) = 1.11, ns) or Raven’s score (F(1,8) = 0.68). Participant details are shown in Table 2.
Experimental Investigation The following experiments were conducted over a period of one year. The tasks were introduced to all patients as part of an investigation of the cognitive correlates of antisocial behavior. For each experiment, significant impairment was defined as the individual or mean score falling outside of the range of a 95% confidence interval of their respective control group (community controls for CL and forensic controls for participants with psychopathy). Stimulus-Response Learning and Reversal Task 1: The Ask for Money Task (Fine, 2000) This task involves making conditional discriminations to reference stimuli. Conditional learning is a form of stimulusresponse learning, which requires individuals to associate an individual reference with a motor response (Baxter and Murray, 2002). Procedure This task is described more fully by Fine (2000). In brief, participants attempt to borrow money from their “relatives.” Digital representation of four relatives and two response options (buttons) for each stimulus (hint or beg) were shown. Two relatives
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Acquired Versus Developmental Psychopathy Table 1. General cognitive and executive function test scores CL
Score
IQ WAIS Verbal IQ WAIS Performance IQ WAIS Full Scale IQ Raven’s Advanced Matrix NART Recognition Memory (Warrington, 1984) RM Words RM Faces Verbal Graded Naming Test Concrete Word Synonyms Abstract Word Synonyms Proverbs Verbal Fluency (FAS) Unrestricted nouns Animals Executive Function Object Decision Cube Analysis Cognitive Estimates Wisconsin Card Sorting Speed of Information Processing Adult Memory and Information Processing Battery Form I (AMIPB)* Motor Speed Cognitive Speed A Cognitive Speed B Accuracy A Accuracy B
Normative result
115 113 114 9/12 45/50
84th percentile 80th percentile 82nd percentile 75th percentile Premorbid IQ estimated at 124
46/50 33/50
62nd percentile 50th
Note. WAIS = Wechsler Adult Intelligence Scale. RM = Recognition memory. NART = National Adult Reading Test.
Table 2. Characteristics of the comparison groups Individuals with psychopathy (n = 5)
Participant characteristics Ravens Score Age PCL-R Factor 1 Score PCL-R Factor 2 Score PCL-R Total
Forensic Controls (n = 5)
Community Controls (n = 5)
M
SD
Range
M
SD
Range
M
SD
Range
7.80 41.40 11.07 15.00 31.07
1.92 6.66 2.17 1.87 1.37
5 to 10 37 to 53 9.00 to 14.00 12.00 to 17.00 30.00 to 33.35
7.60 43.60 4.40 5.59 11.92
2.70 3.36 3.90 3.59 7.28
5 to 11 39 to 48 1.50 to 10.00 1.30 to 10.15 3.30 to 20.00
9.60 50.40 – – –
2.07 6.88 – – –
7 to 12 44 to 59 – – –
Note. M = mean; SD = standard deviation; PCL-R = Psychopathy Checklist Revised (Hare, 1991).
yielded a favorable response to hinting, and two were more favorable to begging. In the first phase, participants learn the stimulus-response associations. The second phase measures conditional reversals; for half of the stimuli the responses change
value so that the alternative response becomes optimal. Acquisition consisted of 32 trials, followed by 24 trials of reversal. The dependent measure was the number of correct selections in the acquisition and reversal phase.
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Results CL showed impaired conditional learning relative to the community controls based on the acquisition phase and in the second phase for non-reversed stimuli. In contrast, individuals with developmental psychopathy showed intact conditional discrimination acquisition, but impaired reversal performance. The results of the task are shown in Table 3. Task 2: The Intradimensional-Extradimensional Shift Task (ID/ED; Dias et al., 1996) The ID/ED Task assesses object discrimination, response reversal (RR) and extradimensional (ED) shift performance. A previous study incorporating the same procedure reported deficits in adults with psychopathy (Mitchell et al., 2002). Procedure This task is described more fully by Dias and colleagues (1996). Participants select between two stimuli based on response feedback (the words “correct” or “incorrect”). The stimuli have two dimensions: object and shape. With one exception, the correct stimulus for each pair is always specified by its shape. Object discrimination involves learning which of two shapes to select. RR involves selecting the previously punishing stimulus after contingency change. Following the ED shift, the previously relevant stimulus dimension (shape) became irrelevant and selections were made on the basis of a superimposed line rather than the shape. The dependent measure is the number of errors made before successfully completing the phase (with success defined as 8 consecutive correct selections). Results CL’s performance was at or near ceiling on each component of the task. In contrast, the RR performance of the individuals
with psychopathy was selectively impaired. Table 4 shows the performance of each group on the ID/ED Task. Task 3: The Iowa Gambling Task (Bechara et al., 1994; Bechara et al., 1999) Previous reports suggest that this task, designed to assess real-life decision-making, reveals impaired performance in patients with acquired (Bechara et al., 1994; Bechara et al., 1999) and developmental psychopathy (Mitchell et al., 2002; Van Honk et al., 2002). Procedure The gambling task was administered in computerized format with a schedule of reinforcement described in detail by Bechara and colleagues (1999). Participants make selections from four decks of cards. Two high-risk, net-loss decks yield high magnitude reward, but even higher punishment. The remaining two low-risk, net-gain decks yield low magnitude reward, but even lower punishment. The dependent measure was the number of high-risk selections. Results CL’s total number of risky selections (Decks A/B) was significantly greater than the comparison group. Similarly, individuals with developmental psychopathy made significantly more errors than the forensic comparison group. Table 5 presents the results of this task. Summary of Stimulus-response Learning and Reversal Tasks The results of the stimulus-response and reversal tasks reveal a double dissociation: CL showed deficient stimulusresponse learning, but intact object reversal learning;
Table 3. Ask for Money Task results Conditional acquisition correct CL Controls M SD Range CI Psychopathic M SD Range CI Forensic controls M SD Range CI
Phase 2 reversed stimuli
Phase 2 Non-reversed stimuli
13
4
3
23.00 5.61 15 to 30 16.0 to 30.0
5.80 2.86 1 to 8 2.2 to 9.4
9.60 1.67 7 to 11 7.5 to 11.7
18.20 4.32 13 to 24 12.8 to 23.6
4.60 1.14 3 to 6 3.2 to 6.0
6.00 1.87 4 to 9 3.7 to 8.3
15.80 4.44 8 to 19 10.3 to 21.3
5.80 0.84 5 to 7 4.8 to 6.8
4.40 2.51 0 to 6 1.3 to 7.5
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Acquired Versus Developmental Psychopathy Table 4. ID/ED task results Object discrimination
ED set shifting
CL 0 Controls M 0.00 SD 0.00 Range – CI – Psychopathic M 1.40 SD 0.89 Range 0 to 2 CI 0.29 to 2.5 Forensic controls M 1.20 SD 0.84 Range 0 to 2 CI 0.16 to 2.2
Object reversal
1
0
7.00 7.45 0 to 15 0 to 16.3
0.53 0.51 0 to 1 0 to 1.2
9.40 6.80 2 to 15 0.95 to 17.8
7.60 8.14 1 to 17 0 to 17.7
5.00 5.67 1 to 15 0 to 12.0
1.40 1.34 0 to 3 0 to 3.1
Procedure The passive avoidance task used was described by Blair and colleagues more fully (2004a). In the task, 8 different numbers were presented to the participant once per block, for 10 blocks. Four of the stimuli yielded reward when selected, and four yielded punishment. The dependent variables were the number of passive avoidance errors (responding to negative stimuli) and omission errors (failing to respond to positive stimuli). Results CL showed no evidence of impairment in passive avoidance learning. Individuals with psychopathy were within the confidence interval of their forensic control group; however, their mean score for passive avoidance errors was more than 1.5 standard errors above the control mean. CL made significantly less errors than individuals with psychopathy. No significant differences existed for number of omission errors. Table 6 shows the results of this experiment.
Note. ED = Extradimensional.
conversely, individuals with psychopathy showed intact stimulusresponse learning, but impaired object reversal learning. It is interesting to note that CL showed impairment on one form of stimulus-response learning (conditional learning), yet showed intact performance on the second stimulus-response task (object discrimination in the ID/ED task). This can be explained by task difficulty and sensitivity of the task. Stimulus-reinforcement Learning, and Extinction Task 4: The Passive Avoidance Task (Blair et al., 2004a) In this task, participants associate a specific stimulus to a specific level of reinforcement, which is referred to as stimulusreinforcement learning (Baxter and Murray, 2002). Individuals with psychopathy have shown deficits on this form of learning (Newman and Kosson, 1986; Newman et al., 1987; Newman and Schmitt, 1998; Blair et al., 2004a).
Task 5: The One-Pack Card Playing Task (Newman et al., 1987) This task requires participants to update the incentive value of a stimulus to guide responding and extinguish a stimulusreinforcement association, which is reported to be impaired in adults with psychopathy (Newman et al., 1987). A previous study reported intact performance in a case of acquired psychopathy (Blair and Cipolotti, 2000). Procedure This task is described more fully by Newman and colleagues (1987). Participants make selections from a single deck of cards. Initially, all selections from the deck are rewarded with 10 points; however, the number of punishments steadily increases by 10% for every 10 cards played. The task continues until the participant elects to stop. The dependent measure is the number of cards played.
Table 5. Iowa Gambling Task results Community controls CL
M
SD
Range
Individuals with psychopathy CI
Total disadvantageous selections Block 1 15 9.00 8.31 0 to 16 0 to 19.3 Block 2 8 5.40 3.65 0 to 10 0.9 to 9.9 Block 3 7 6.20 3.42 1 to 10 2.0 to 10.4 Block 4 15 8.00 6.63 2 to 18 0 to 16.2 Block 5 9 4.80 3.03 3 to 10 1.0 to 8.6 Totals by decks Decks A/B 54 33.40 10.48 22 to 46 20.4 to 46.4 Decks C/D 46 66.60 10.48 54 to 78 53.6 to 79.6
M
SD
Range
10.60 8.80 10.40 12.40 9.80
1.34 2.17 3.71 4.83 5.93
9 to 12 6 to 11 5 to 13 8 to 18 6 to 20
CI
Forensic controls M
8.9 to 12.3 13.60 6.1 to 11.5 7.60 5.8 to 15.0 6.00 6.4 to 18.4 2.00 2.4 to 17.2 3.00
SD
Range
CI
4.45 4.39 4.53 3.94 4.24
8 to 19 2 to 13 0 to 11 0 to 9 0 to 9
8.1 to 19.1 2.1 to 13.1 0.4 to 11.6 0 to 6.9 0 to 8.3
52.00 12.49 39 to 67 36.5 to 67.5 32.20 11.58 20 to 50 17.8 to 46.6 48.00 12.49 33 to 61 32.5 to 63.5 67.80 11.58 50 to 80 53.4 to 82.2
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Table 6. Passive Avoidance Task results Passive Avoidance errors CL Controls M SD Range CI Psychopathic M SD Range CI Forensic controls M SD Range CI
8
Emotional Expression Processing Omission errors 7
9.40 4.28 5 to 16 4.1 to 14.7
10.80 7.82 0 to 20 1.1 to 20.5
24.40 9.45 10 to 36 12.7 to 36.1
11.00 5.24 5 to 19 4.5 to 17.5
18.00 8.09 7 to 28 8.0 to 28.0
13.00 7.45 4 to 24 3.7 to 22.3
Results CL’s performance was not significantly different than his comparison group. The mean number of cards played by the psychopathic inmates was very near the upper limit, but not outside the confidence interval of the forensic controls. CL played significantly less cards than the individuals with developmental psychopathy. The results are shown in Table 7. Summary of Stimulus-reinforcement Learning, and Extinction CL showed no evidence of stimulus-reinforcement learning deficits. He performed within the CI of the community and forensic controls and better than individuals with developmental psychopathy. Table 7. One-pack Card Playing Task results Cards selected CL Controls M SD Range CI Psychopathic M SD Range CI Forensic controls M SD Range CI
Task 6: The Emotional Expression Multimorph Task This task is identical to the task described by Blair and colleagues (2004b) and is used to assess sensitivity to emotional facial expression. Neuroimaging and lesion studies indicate that at least partially dissociable neural substrates specialize in processing distinct emotional expressions. Previous studies have reported limited expression recognition deficits in patients with psychopathy (Kosson et al., 2006), particularly for fear (Blair et al., 2001b; Blair et al., 2004b). Procedure The stimuli used are taken from the cross-culturally validated Pictures of Facial Affect Series (Ekman and Friesen, 1976) depicting the six basic emotional facial expressions (happiness, surprise, fear, sadness, disgust, and anger). Individual stimuli were prepared by blending photographs of prototypical emotional expressions in varying proportions with neutral expressions. For each continuum, the participant viewed each face as it gradually changed through 20 morphed sequences in 5% increments (each stage lasting 3 seconds) into one of six prototypical expressions. The participants were presented with 18 test stimuli in random order. The dependent variable was the number of stages required before successful recognition. Errors were coded one point greater than the highest possible score (21 + 1) as a conservative estimate of impairment. Results CL showed impaired performance for each category of emotion with the exception of sad and surprised expressions. In contrast, psychopathic individuals were impaired only in the recognition of fearful facial expressions. CL was significantly impaired relative to individuals with psychopathy for happy and angry facial expressions. The results are shown in Table 8.
Points
38
260
53.40 19.46 23 to 73 29.2 to 77.6
262.00 55.86 170 to 310 192.6 to 331.4
78.40 18.53 58 to 98 55.4 to 101.4
232.00 85.53 120 to 320 126.1 to 337.9
56.80 21.42 26 to 85 30.2 to 83.4
260.00 43.01 200 to 300 206.6 to 313.4
Task 7: Audio Emotion Recognition (Scott et al., 1997) This task indexes sensitivity to vocal expressions of emotion. Previous studies report impaired vocal affect recognition in children with psychopathic tendencies (Blair et al., 2001a) and adults with psychopathy (Blair et al., 2004b). Procedure The test consists of 65 digitalized bi-syllabic words of neutral denotation (e.g., carpet) spoken by native English speakers (3 male and 3 female). The emotions conveyed were those of happiness, disgust, anger, sadness and fear (12 examples of each emotion). Participants were asked to detect the likely emotion that the speaker was feeling based on how the word was spoken. The dependent measure was the number of errors made for each emotion.
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Acquired Versus Developmental Psychopathy Table 8. Multimorph Expression Recognition Task number of stages required for recognition Fearful CL 17.33 Controls M 13.80 SD 2.30 Range 11.33 to 16.67 CI 10.9 to 16.7 Psychopathic M 17.80 SD 3.02 Range 13.33 to 21.67 CI 14.0 to 21.6 Forensic controls M 12.93 SD 1.79 Range 10.67 to 15.67 CI 10.7 to 15.2
Sad
Happy
15.00
Surprised
14.33
Disgusted
Angry
Total
15.00
21.33
21.00
17.32
13.93 2.92 9.33 to 17.33 10.3 to 17.6
6.73 2.42 4.33 to 10.33 3.7 to 9.7
16.07 4.59 12.00 to 22.00 10.37 to 21.76
14.20 4.68 8.67 to 21.67 8.39 to 20.0
13.93 4.02 8.67 to 17.33 9.0 to 16.4
13.11 2.62 9.17 to 16.28 9.9 to 16.4
15.27 1.94 12.67 to 17.33 12.9 to 17.7
9.40 3.42 5.33 to 14.33 5.2 to 13.6
14.67 4.28 9.00 to 19.67 9.4 to 20.0
16.80 4.69 10.00 to 22.00 11.0 to 22.0
14.27 4.11 7.33 to 17.67 9.2 to 19.4
14.70 2.44 11.39 to 17.00 11.7 to 17.7
15.27 1.94 12.67 to 17.33 8.5 to 19.0
8.73 3.01 5.00 to 13.33 5.0 to 12.5
12.07 3.59 9.00 to 19.67 7.6 to 16.5
15.73 4.46 10.00 to 22.00 10.2 to 21.3
11.93 4.21 7.33 to 17.33 6.7 to 17.2
12.52 2.39 9.28 to 15.72 9.6 to 15.5
Results CL showed no evidence of impaired auditory emotional expression processing. In contrast, individuals with developmental psychopathy were impaired in the recognition of fearful and sad vocal affect relative to forensic controls. The results are shown in Table 9.
Summary of Emotional Expression Processing CL showed near-global impairment in the recognition of facial expressions and intact recognition of vocal expressions of emotion. In contrast, participants with psychopathy
showed a selective fearful facial recognition deficit and impaired recognition of fearful and sad vocal affect.
Social Cognition Task 8: The Joke Comprehension Test (Corcoran et al., 1997) The Joke Comprehension Test (Corcoran et al., 1997) is a set of 20 cartoon drawings. Half of the cartoons are thought to index ToM because they are only understood with reference to mental states; the remainder can be appreciated through physical and semantic analysis (Corcoran et al., 1997). The task is sensitive to ToM impairments in schizophrenic patients (Corcoran et al.,
Table 9. Auditory Emotional Expression Recognition Task results (errors) Fearful CL Controls M SD Range CI Psychopathic M SD Range CI Forensic controls M SD Range CI
Sad
Happy
Disgusted
Angry
Total
0
1
7
2
3
2.60
1.60 1.67 0.00 to 4.00 0 to 3.7
1.20 0.84 0.00 to 2.00 0.2 to 2.2
5.00 2.55 3.00 to 9.00 1.8 to 8.2
3.60 2.19 1.00 to 7.00 0.9 to 6.3
2.20 1.79 0.00 to 4.00 0.0 to 4.4
2.72 1.24 1.40 to 4.40 1.2 to 4.3
5.00 2.00 3.00 to 8.00 2.5 to 7.5
4.20 1.48 2.00 to 6.00 2.4 to 6.0
4.20 2.58 1.00 to 8.00 1.0 to 7.4
2.80 2.95 0.00 to 7.00 0.0 to 6.5
3.80 2.17 2.00 to 7.00 1.1 to 6.5
4.00 1.57 2.20 to 5.40 2.1 to 5.9
1.80 1.10 0.00 to 3.00 0.44 to 3.2
2.60 1.15 1.00 to 4.00 1.2 to 4.0
4.60 3.36 1.00 to 10.00 0.4 to 8.8
2.00 0.71 1.00 to 3.00 1.1 to 2.9
2.60 1.52 1.00 to 4.00 0.7 to 4.5
2.72 0.30 2.40 to 3.20 2.3 to 3.1
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Table 10. Performance on the Joke Comprehension Test ToM comprehension (max = 10) CL Controls M SD Range CI
ToM comic rating (max = 10)
9.00
4.50
9.00 1.00 8 to 10 7.8 to 10.2
4.76 1.86 2.30 to 6.70 2.4 to 7.1
Physical comprehension (max = 10) 10.00 9.20 1.79 6.00 to 10.00 7.0 to 11.4
Physical comic rating (max = 10) 5.60 4.58 1.93 1.90 to 6.40 2.2 to 7.0
Note. ToM = Theory of mind.
1997); however, to our knowledge, it has not been tested on a patient with acquired psychopathy. Procedure The Joke Comprehension task is described in more detail by Corcoran et al. (1997). Forensic groups were not available to complete this task due to inmate transfers and wing closures. CL and his comparison group were asked to describe and rate the comic value of each on an ascending scale of 1 to 10. Dependent measure was the number of mental state and physical situation jokes explained correctly. Results CL comprehension of both sets of jokes was not significantly different from that of the controls. Table 10 shows the results of this task. Task 9: The Reading the Mind in the Eyes Task (Advanced ToM; Baron-Cohen et al., 2001). The Eyes Task investigates an individual’s ability to infer mental states on the basis of social information conveyed from photos depicting a person’s eyes. It is considered a sensitive index of ToM (Baron-Cohen et al., 1997). A previous study using this task indicated equally good performance between psychopathic and nonpsychopathic individuals, suggesting intact ToM in individuals with psychopathy. Procedure This task is presented in more detail by Baron-Cohen and colleagues (2001). Participants were presented with 36 photographs depicting only the facial area around the eyes. Four complex mental state descriptors (e.g., dispirited, bored) were printed around the photo, one at each corner. One of these words (the target) correctly identified the mental state of the person in the photo, whereas the others were included as foils (e.g., annoyed or hostile). Participants chose the word that best described what the person in the picture was thinking or feeling. Word definitions were available and the dependent measure was the number of correct identifications.
Results Neither CL nor individuals with developmental psychopathy showed evidence of impaired task performance. CL’s score of 30 was within the CI of his comparison group (M 29.40; SD 4.16; Range 23 to 33; CI 24.2 to 34.6). Similarly, individuals with psychopathy (M 25.20; SD 4.71; Range 19 to 31; CI 19.3 to 31.1) performed within the CI of their comparison group (M 25.00; SD 4.30; Range 20 to 31; CI 19.7 to 30.3). Task 10: The Social Situations Task (Dewey, 1991) The Social Situations Task indexes an individual’s ability to detect transgressions for which no formal societal prohibitions exist, but which may provoke anger or aggression in observers. It is thought to be a sensitive measure of social response reversal, which has been implicated in modulating behavior when encountering disapproving social cues (Blair and Cipolotti, 2000). The study includes nine short stories depicting socially normative behavior, and nine stories depicting social violations. By examining the frequency with which social norms and their violations are identified, the task provides an estimate of an individual’s ability to detect socially inappropriate behavior. A previous study found impairment in individuals with psychopathy in recognizing social violations, whereas the case study of acquired psychopathy showed intact performance (Blair and Cipolotti, 2000). Procedure The procedure is described in more detail by Dewey and colleagues (1991). Scenes describing social situations were presented to the participants on a computer screen and read aloud. At specified points in the stories, participants were asked to verbally rate the behavior described in the story according to how most witnesses would judge that behavior on an ascending scale of inappropriateness. Mean ratings for these two types of behavior were calculated. Results CL performed significantly worse than forensic, psychopathic and community groups in both the identification and
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Acquired Versus Developmental Psychopathy Table 11. Social Situations Task results Social violations correctly identified (0 to 11) CL Controls M SD Range CI Psychopathic M SD Range CI Forensic controls M SD Range CI
Normal behaviors labelled violations (0 to 11)
Inappropriateness rating for violations (0 to 33)
5
1
8
9.80 1.30 8 to 11 8.2 to 11.4
2.40 2.30 0 to 6 0 to 5.3
18.80 5.45 12 to 27 12.0 to 25.6
8.40 1.14 7 to 10 7.0 to 9.8
2.00 1.87 0 to 5 0 to 4.3
13.20 3.70 10 to 19 8.6 to 17.8
8.40 0.55 8 to 9 7.7 to 9.1
2.20 1.64 0 to 4 0.2 to 4.2
14.80 0.84 14 to 16 13.8 to 15.8
severity ratings of socially inappropriate behavior. This contrasts with his above-average performance on the ToM tasks. Participants with developmental psychopathy showed no deficits in identifying or rating inappropriate social behavior. Summary of Social Cognition Tasks CL showed no evidence of ToM impairments as indexed by the ToM cartoons or the reading the mind in the eyes task. Despite his intact ToM, CL showed impairment in identifying violations of social norms. Individuals with psychopathy showed no evidence of impairment on the reading the mind in the eyes task.
Discussion Following bilateral trauma to the frontal region involving the OFC, CL showed severe disturbance in affect and interpersonal functioning. While CL did not meet the traditional diagnostic threshold for psychopathy on the PCL-R, his score was notably elevated (Hare, 1991; 2003). In particular, his affective disturbances were similar to those reported in individuals with psychopathy (corresponding to Factor 1 on the PCL-R; Hare, 1991). We compared CL’s neuropsychological performance with the performance of psychopathic, forensic control, and control groups on the same tasks. Both CL and cases of developmental psychopathy showed similar deficits in decision-making; however, they showed a different pattern of impairment in conditional learning, reversal learning, stimulusreinforcement learning, extinction, emotional expression recognition, and in the identification of socially inappropriate behaviors. Table 12 provides a summary of these results. We suggest that CL’s deficient performance on facial expression and inappropriate social behavior recognition tasks are symp-
tomatic of dysfunction in the social response reversal system and that this dysfunction contributes to his reactive aggression. In contrast, he did not show clear evidence for neurocognitive risk factors of instrumental aggression, such as stimulus-reinforcement association deficits as measured by the passive avoidance task. We suggest that for individuals with developmental psychopathy, deficient vocal and facial expression recognition and poor stimulus-reinforcement association formation are symptomatic of dysfunction in the amygdala, and that this dysfunction contributes to their instrumental aggression (Blair, 2003). Individuals with psychopathy also showed deficits on response reversal and decision-making performance, which we suggest contribute to increased levels of frustration and greater risk for reactive aggression. Together, these findings are compatible with suggestions that acquired psychopathy is associated with neurocognitive deficits that increase the risk for reactive, but not instrumental aggression, whereas developmental psychopathy is associated with neurocognitive deficits that increase the risk for both reactive and instrumental aggression (Blair, 2004). Acquired psychopathy does not follow all ventral or orbital frontal lesions, but it is associated with greater risk for the disorder than other neurological conditions (Grafman et al., 1996). Evidence for this association comes from studies involving frontotemporal dementia (Mendez et al., 2005), acquired pedophilia (Burns and Swerdlow, 2003), and patients with bilateral (Barrash et al., 2000) or right-sided (but not left) OFC lesions (Tranel et al., 2002). Each of these studies report heightened levels of reactive aggression: frustration intolerance, social inappropriateness, sex offenses, irritability, and lability (Barrash et al., 2000; Burns and Swerdlow, 2003). However, they show no evidence for elevated levels of instrumental antisocial behavior or characteristics such as “dependence” and “manipulativeness” (Barrash et al., 2000; Blair and Cipolotti, 2000). These studies do not explain
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D.G.V. Mitchell et al.
Table 12. Summary of task performance C.L Instrumental learning/decision-making Ask For Money ID/ED Iowa Gambling Passive Avoidance One-Pack Card Playing Emotional expression processing Emotional Expression Multimorph Audio Emotion Recognition Social cognition Joke Comprehension Test Reading the Mind in the Eyes Social Situations
Controls
Δ Acquisition
√
√ Δ √ √
√ √ √ √
√: SD, SR, Δ: F, H, D, A, T √
√
√ √ Δ
Psychopathic √ Acquisition Δ Reversal Δ Selective RR Δ Δ (Trend) Δ (Trend)
Forensic controls √ √ √ √ √ √
√
√: SD, SR, D, A, T Δ: F, H Δ: F, SD
√ √ √
– √ √
– √ √
√
Note. * √ = Intact; Δ = Impaired; SD = Sad; SR = Surprised; F = Fearful; H = Happy; D = Disgusted; A = Angry; T = Total mean expression score.
why neurocognitive deficits associated with OFC damage give rise to risk for reactive aggression, such as assaults and sexual offenses, but not instrumental antisocial offenses, such as armed robbery. The present investigation included measures of ToM. The neural structures implicated in ToM are the amygdala, superior temporal sulcus, anterior paracingulate, and the OFC (Baron-Cohen et al., 1994; Baron-Cohen et al., 2000; Gallagher et al., 2000; Fine et al., 2001; Rilling et al., 2004). Some work has reported ToM dysfunction following frontal lobe damage (Stone et al., 1998; Stuss and Anderson, 2004; Shamay-Tsoory et al., 2005). However, these suggestions rely on results from the ‘social faux pas’ test, which requires the identification of socially inappropriate behavior (Stone et al., 1998; Shamay-Tsoory et al., 2005). Furthermore, studies investigating ToM performance in adults reliably assessed for psychopathy have consistently failed to uncover evidence of impairment (Blair et al., 1996; Blair and Cipolotti, 2000; Richell et al., 2003). Similarly, we found no evidence of ToM deficits in any of our samples and therefore do not support suggestions that the increased risk for reactive aggression seen in CL and in individuals with developmental psychopathy is related to ToM functioning. Frustration is thought to occur when operant behavior fails to precipitate the expected level of reinforcement (Berkowitz, 1993). The failure to flexibly adapt behavior to changes in reinforcement contingencies will lead to (possibly chronically) increased levels of frustration, and subsequently, increased risk for reactive aggression. Previous studies have found reversal learning deficits in patients with OFC lesions (Rolls et al., 1994; Fellows and Farah, 2003; Hornak et al., 2004). However, CL showed no evidence of response reversal or extinction deficits (see Tasks 2 and 5). This implies that his elevated risk for reactive aggression was not due to an inability to flexibly adapt to changes in reinforcement contingency.
A caveat to this suggestion is that CL did show impoverished decision-making, which is thought to be an important feature of acquired psychopathy (Bechara et al., 1994; Damsio, 1994; Bechara et al., 2000). One possibility is that the gambling task is a more sensitive index of both response reversal and of the ability to update the incentive value of stimuli. Despite the fact that CL did not show all risk factors associated with reactive aggression (he showed intact response reversal), the poor decision-making performance in CL and in our sample with developmental psychopathy, may contribute to heightened levels of frustration. In contrast to CL, but consistent with the previous literature, individuals with psychopathy showed difficulty with both response reversal and extinction (Newman et al., 1987; Lapierre et al., 1995; Mitchell et al., 2002; Budhani and Blair, 2005). We believe that the elevated risk for reactive aggression seen in individuals with psychopathy may be due to increased levels of frustration resulting from an impoverished ability to adapt responding to changes in reinforcement contingency (Manes et al., 2002; Blair, 2004). However, as yet, we are not aware of any studies that have examined the ability of response reversal performance to predict risk for reactive aggression in a population of individuals with psychopathy. Difficulties adapting behavior to changes in reinforcement (response reversal) have been linked with aberrant social behavior (Rolls et al., 1994; Blair, 2004). In addition, we have argued that an increased risk of reactive aggression is seen following dysfunction to a proposed social response reversal system. This system is thought to have evolved for the resolution of hierarchy interactions (including aggression) between conspecifics (Blair, 2004). Neuro-imaging and patient studies suggest that lateral OFC/ ventrolateral prefrontal cortex plays a role in monitoring social cues in the environment and identifying inappropriate or embarrassing
Acquired Versus Developmental Psychopathy social behaviors (Blair and Cipolotti, 2000; Berthoz et al., 2002). We believe that failures within this system can increase the risk for reactive aggression in two main ways. First, a failure to recognize disapproving social cues will compromise the ability to adjust behavior in real-time to dynamic social demands. Second, the formation of unrealistic expectations of social reception (receiving reduced respect and affiliation rather than the opposite) can lead to increased frustration, and therefore increased risk for reactive aggression. The present study indexed the social response reversal system through tasks examining the recognition of emotional expressions and violations of social norms. Similar to a previous case of acquired psychopathy (Blair and Cipolotti, 2000), CL demonstrated significant and generalized impairment in recognizing emotional facial expressions and in identifying socially inappropriate behavior. In contrast, we found no evidence of social response reversal deficits in individuals with developmental psychopathy; individuals with developmental psychopathy were able to correctly identify depictions of anger, disgust, and socially inappropriate behavior. Given CL’s impaired performance on both the facial expression recognition task and the facial recognition memory task, it is tempting to speculate that his difficulties on the former might be attributable to a more global visuo-spatial face processing deficit rather than to an affective processing deficit. However, this explanation is unlikely given his exceptional performance on the theory of mind (Eye Gaze) task, which also requires visuo-spatial processing of faces. In conjunction with CL’s deficits in identifying socially inappropriate behavior in the Social Situations Task, a social response reversal deficit is the most parsimonious explanation of his selective affective expression recognition deficit. In short, we believe that for CL (but not the individuals with psychopathy) the increased risk for reactive aggression and potentially sexual offending, may reflect social response reversal dysfunction. Instrumental aggression is associated with developmental, but not acquired psychopathy. We have previously argued that two functional processes are necessary for successful moral socialization and the emergence of care-based morality. Dysfunction in either process can increase the risk for instrumental aggression. The first functional process is involved in facilitating distress cue processing. If the aversive quality of distress cues is reduced, as it is in psychopathy, the individual will not find actions associated with a victim’s distress aversive and so have less reason to avoid those actions. The second process involves the ability to form stimulus-reinforcement associations. Even with intact distress cue processing, difficulties forming stimulus-reinforcement associations will result in a weaker association between a moral transgression and victim distress. The data suggest that individuals with psychopathy show deficits in both processing distress cues, and in making stimulus-reinforcement associations (Newman and Kosson, 1986; Newman and Schmitt, 1998). Both stimulus-reinforcement association formation (Baxter and Murray, 2002) and distress cue processing (Phillips et al., 1998; Blair et al., 1999; Breiter et al., 1996; Morris
175 et al., 1996) are associated with amygdala function. Disruption to these processes reduces the efficacy of standard socialization practices and can lead to increased risk for instrumental aggression and the development of the full syndrome of psychopathy (Blair, 2004). Our sample of individuals with developmental psychopathy showed deficient recognition of fearful and sad expressions (as did CL). However, individuals with psychopathy, but not CL, also showed impairment in stimulus-reinforcement learning (see task 4). The impairments seen here were milder than expected, but were consistent with previous reports of passive avoidance learning impairment in psychopathy (Newman and Kosson, 1986; Newman and Schmitt, 1998). Like patients with developmental psychopathy, CL shows little evidence of empathy for his victims or concern about his actions before, during, or after his offenses. Following Schoenbaum and colleagues (Gallagher et al., 1999; Pickens et al., 2003), we have suggested that the amygdala transmits information about the expected reinforcement associated with a particular object or action to medial OFC (Kosson et al., in press). Using this information, medial OFC initiates approach or withdrawal responses to the object or action. We, and others, have argued that distress cues in others act as punishing stimuli, and that through conditioning, the individual also finds aversive the actions associated with producing the distress cues (Mineka and Cook, 1993; Blair, 2004). Accordingly, once the individual has learned about a moral transgression, representation of the action will lead to an aversive expectation; at the neural level, this is thought to involve a signal from the amygdala to medial OFC. This integrated amygdala-medial OFC formulation of an aversive expectation constitutes an individual’s “moral attitude” to the situation (Luo et al., in press). In line with this position, recent neuro-imaging studies of morality using different methodologies such as in a morality-based Implicit Association Test (Luo et al., in press), making moral decisions based on text descriptions of ethical dilemmas (Greene et al., 2001; Greene et al., 2004), passive viewing pictures of moral violations (Moll et al., 2002b), judging sentence descriptions of behaviors as moral or immoral (Moll et al., 2002a; Heekeren et al., 2005) and making moral decisions (morally appropriate or not) versus semantic decisions (semantically correct or not) on sentences (Heekeren et al., 2003) have implicated both the amygdala and medial regions of OFC. Patient and imaging data implicate ventromedial regions (Eslinger and Damasio, 1985; Damasio, 1994; Anderson et al., 1999; Blair and Cipolotti, 2000; Takahashi et al., 2004) and the amygdala (Moll et al., 2002; Greene et al., 2004; Heekeren et al., 2005) in moral emotions. In short, according to this position, damage to either the amygdala or medial OFC could lead to the affective deficits seen in individuals with psychopathy and CL respectively. Although the conclusions that can be drawn from a case study are limited, the results raise questions about the analogy frequently drawn between acquired and developmental psychopathy. Due to CL’s above-average IQ, we were not able to
176 acquire forensic groups matched in this respect. Consequently, CL’s performance was primarily defined with respect to his age-and IQ-matched controls. It would be ideal if future work matched the developmental groups and individuals with acquired personality disturbances in this domain to increase the strength of the results. Despite its limitations, these results underscore the value of investigations that reliably and validly assess psychopathy in both acquired and developmental forms. To our knowledge, the current study is the first to use the PCL-R to assess psychopathy in a patient with an acquired form of the disorder. With respect to instrumental learning, a double dissociation was found. CL showed conditional learning deficits, but intact stimulus-reinforcement learning. In contrast, individuals with developmental psychopathy showed stimulus-reinforcement learning deficits, but intact conditional learning. Furthermore, CL showed intact response reversal, but impaired social response reversal, whereas individuals with developmental psychopathy showed intact social response reversal, but impaired response reversal. Contrary to OFC accounts of ToM, CL showed no evidence of impairment on two sensitive measures of mental state representation, which supports the idea that social response reversal deficits can be associated with reactive aggression in the absence of ToM or RR dysfunction. Together, these results provide further evidence that acquired and developmental psychopathy is dissociable at a neurocognitive level. The divergent neurocognitive impairments may underlie the two different forms of aggression, reactive versus instrumental, that primarily characterize each disorder.
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