Impaired Reversal but Intact Acquisition: Probabilistic Response ReversalDeficits in Adult Individuals With Psychopathy

Salima Budhani, Rebecca A. Richell, and R. James R. BlairNational Institute of Mental Health

The performance of adult psychopathic individuals on a novel response reversal task involving 2reward–punishment contingencies (100–0 and 80–20) was investigated. In line with predictions, adultswith psychopathy presented with impairment on the response reversal component but not on theacquisition component of this task. This selective impairment for response reversal was seen for bothreward–punishment contingencies and was related to the tendency of individuals with psychopathy to beless likely to stay with a rewarded correct response to a stimulus on the subsequent presentation of thatstimulus. Results are discussed with reference to current models of the development of psychopathy.

Keywords: psychopathy, response reversal, integrated emotion systems model, fear dysfunction position

Adults with psychopathy and children with psychopathic tenden-cies are characterized by a distinct pattern of abnormal behavioral andemotional traits. These include callousness, a diminished capacity forremorse, superficial charm, impulsivity, and poor behavioral controls(Cleckley, 1967; Hare, 1991). Individuals with psychopathy commit adisproportionate amount of crime, habitually fail to fulfill societalobligations, respond badly to psychiatric interventions, and are proneto abnormally high rates of recidivism (Hare, 1993; Lykken, 1995). Inadulthood psychopathy is identified principally by use of the RevisedPsychopathy Checklist (PCL–R; Hare, 1991).

Classic response reversal tasks (e.g., the Intradimensional/Extra-dimensional [ID/ED] shift task) may be characterized as involvingtwo distinct phases: acquisition and reversal. The acquisition phase ofthe task requires the participant to learn an object discrimination to asatisfactory level (i.e., if presented with Pair A–B, then respond tostimulus A). The reversal phase requires that the participant alter thislearned discrimination (i.e., if presented with Pair A–B, then respondto stimulus B). Adults with psychopathy present with impairment onthe reversal phase of the ID/ED task. However, they do not presentwith impairment on the acquisition phase of this task.

This dissociation in performance between the acquisition andresponse reversal phases is potentially problematic to two of themain positions on psychopathy. First, the fear dysfunction positionsuggests that individuals with psychopathy are impaired in pro-cessing punishment-related information (Lykken, 1995; Patrick,1994). This suggests the prediction of impairment in both acqui-sition and reversal as both require appropriate learning on the basisof punishment-related information. Of course, it could be arguedthat because correct responses are rewarded, acquisition could be

achieved using reward-related information alone. Reversal mightbe more dependent on punishment information to correct thestimulus–response association. However, if this suggestion is cor-rect, it implies that participants should be relatively uninfluencedby punishment information during acquisition. Punishment of aresponse to a stimulus should be followed by the shift, by theparticipant, from the current response to an alternative response tothe stimulus. In other words, we can examine the probability thatthe participant shifts his or her response after punishment duringacquisition and reversal. If punishment does alter responding, thenparticipants should be more likely to shift their responses to stimuliafter punishment than to not shift their responses. Assuming par-ticipants do shift their responses after punishment during bothacquisition and reversal, the fear dysfunction position should pre-dict reduced response shifting during both acquisition and reversalin the individuals with psychopathy.

The second position is the response modulation hypothesis(Newman, 1998; Patterson & Newman, 1993). According to theauthors, response modulation involves “a rapid and relativelyautomatic (i.e., noneffortful or involuntary) shift of attention fromthe effortful organization and implementation of goal-directedbehavior to its evaluation” (Newman, Schmitt, & Voss, 1997, p.563). According to this hypothesis, the poor performance of indi-viduals with psychopathy on emotional learning tasks such aspassive avoidance and the one-pack card-playing tasks is related totheir inability to shift attention from their goal of responding togain reward to the peripheral punishment information. It could beargued that this position should predict impairment in both theacquisition and reversal phases of response reversal, as both re-quire, in the terms of this hypothesis, the participant to shiftattention from the goal to gain reward to process the punishmentinformation. Alternatively, it could be argued that response mod-ulation is only impaired when individuals with psychopathy arerequired to alter a dominant response set after punishment infor-mation. This would suggest that individuals with psychopathywould only show significant response modulation impairment afterpunishment during the reversal phases of the study.

A third position on psychopathy, the Integrated Emotion Sys-tems (IES) m odel (Blair, 2004), in contrast, would predict thedissociation. The IES model can be considered an extension and

Salima Budhani, Rebecca A. Richell, and R. James R. Blair, Mood andAnxiety Disorders Program, National Institute of Mental Health.

This work was supported by a Medical Research Council studentshipgrant to Salima Budhani.

Correspondence concerning this article should be addressed to R.James R. Blair, Chief, Unit on Affective Cognitive Neuroscience, Moodand Anxiety Disorders Program, National Institute of Mental Health,15K North Drive, Room 206, MSC 2670, Bethesda, MD 20892-2670,E-mail: blairj@intra.nimh.nih.gov

Journal of Abnormal Psychology Copyright 2006 by the American Psychological Association2006, Vol. 115, No. 3, 552–558 0021-843X/06/$12.00 DOI: 10.1037/0021-843X.115.3.552

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development of the earlier fear (Lykken, 1995; Patrick, 1994) andempathy (Blair, 1995) positions. The IES model has been devel-oped in detail elsewhere (Blair, 2004). Only the details related tothe current study will be discussed here. The IES model followsthe distinction drawn by Baxter and Murray (2002) between twoforms of instrumental learning: instrumental learning based onstimulus–reinforcement associations (e.g., passive avoidance) andinstrumental learning based on stimulus–response associations(e.g., object discrimination). Considerable data suggests that al-though instrumental learning based on stimulus–reinforcement as-sociations requires the integrity of the amygdala, instrumentallearning based on stimulus–response associations does not (Baxter& Murray, 2002). According to the IES model, adult individualswith psychopathy present with amygdala and orbital frontal cortexdysfunction. The IES model would not therefore expect that indi-viduals with psychopathy would present with difficulties in theacquisition (object discrimination) stage of paradigms such as theID/ED task as, following Baxter and Murray (Baxter & Murray,2002), object discrimination does not recruit the amygdala. However,orbital frontal cortex is known to play a role in the modification ofbehavior based on stimulus–response associations after contingencychange; lesions of orbitofrontal cortex disrupt response reversal inobject discrimination tasks in humans (Swainson et al., 2000) andother primates (Dias, Robbins, & Roberts, 1996). In addition, imagingdata particularly implicates Brodmann’s Area 47 (also referred to asventrolateral cortex) in response reversal (Cools, Clark, Owen, &Robbins, 2002). The IES model, by suggesting orbital frontal cortexdysfunction in psychopathy, would therefore predict that individualswith psychopathy would show impairment on the response reversalcomponent of these paradigms. In short, the IES model would expectthe observed dissociation in the performance of individuals withpsychopathy between the acquisition and response reversal phases ofthe ID/ED task.

Unfortunately, however, data provided by the ID/ED task doesnot allow an adequate test of the contrasting potential predictionsof the fear–response set modulation hypothesis and the IES model.The object discrimination phases of the ID/ED task are consider-ably easier than the two response reversal phases. Failure to findgroup differences for object discrimination might therefore simplyreflect a floor effect; the task was too easy for both groups. For thisreason, we wished to examine the performance of individuals withpsychopathy on a more difficult object discrimination–responsereversal paradigm. By manipulating the salience of the contin-gency change, it is possible to manipulate the ease of difficulty ofobject discrimination–response reversal (Cools et al., 2002;O’Doherty, Critchley, Deichmann, & Ddan, 2003; Swainson et al.,2000). Thus, a response to the “correct” stimulus in a pair with an80–20 probabilistic reinforcement contingency is rewarded ononly 8 out of 10 presentations and punished on 2 out of 10presentations (the opposite reinforcement contingency is true ofthe “incorrect” stimulus). The acquisition and reversal of thiscontingency is more difficult than the acquisition and reversal of a100–0 probability reinforcement contingency.

In addition, the IES position makes specific predictions withrespect to the participant’s response during reversal after rewardsand punishments. Orbital–ventrolateral frontal cortex appear to beimportant in responding to rewards and punishments after thereversal of previously learned contingencies. Patients with lesionsof orbital–ventrolateral prefrontal cortex are less likely to stay witha rewarded correct response and less likely to shift away from a

punished incorrect response during reversal than comparison indi-viduals (Berlin, Rolls, & Kischka, 2004; Hornak et al., 2004). TheIES position thus predicts that individuals with psychopathyshould be less likely to stay with a rewarded correct response andless likely to shift away from a punished incorrect response duringreversal than comparison individuals.

Our goal was to investigate the performance of adult individualswith psychopathy on a modified version of the probabilistic re-sponse reversal task previously used with children with psycho-pathic tendencies (Budhani & Blair, 2005). On the basis of the IESmodel, we predicted that the individuals with psychopathy wouldnot show impairment in the acquisition phases of the task butwould show impairment in the reversal phases. In addition, wepredicted that individuals with psychopathy should be less likely tostay with a rewarded correct response and less likely to shift awayfrom a punished incorrect response during reversal than compar-ison individuals.

Method

Participants

The sample was made of up 37 men from a pool of 200 men incarceratedin a Category B (high security) forensic institution in the London area. Ofthe participants, 29 were Caucasian, 1 was Asian, and 8 were Afro-Caribbean (1 Asian and 2 Afro-Caribbean participants were in the com-parison group, and 6 Afro-Caribbean participants were in the psychopathicgroup). Files were prescreened to exclude individuals whose psychiatricreports revealed a diagnosis for psychosis, organic brain damage, orneurological disorder. Written consent was obtained from each inmate whoparticipated in the study. All of the participants were informed that par-ticipation was voluntary and would not affect individual status or recordwithin the institution. Participants did not receive any financial or othergain for their participation or performance on the task.

In accordance with the literature and the guidelines of the PCL–R (Hare,1991), individuals with a score of 30 or above on the PCL–R were assigned tothe psychopathic group (n � 20), whereas those with a score of 20 or less wereassigned to the control group (n � 17).1 The Raven’s Advanced ProgressiveMatrices, Set I (Raven, 1976) was administered to provide an estimate of fullscale IQ. There were no significant group differences in either age or Raven’sscore. Participant details by group are presented in Table 1.

Design

Participants were split into two groups according to PCL–R scores(individuals with psychopathy and comparison individuals). The within-subjects factors comprised (a) the two phases (acquisition of the discrim-ination and reversal of the discrimination) and (b) the two reinforcementcontingencies (100–0 and 80–20). Thus the design involved 2 (group:individuals with psychopathy and comparison individuals) � 2 (phase:acquisition, reversal) � 2 (reinforcement contingency: 100–0 and 80–20)mixed-model design. The dependence variable was errors to criterion.

1 Please note that participants scoring �30 on the PCL–R in this samplewere approximately 15% of our forensic population available to us. Par-ticipants scoring �20 on the PCL–R were approximately 20% of ourforensic population. Also, note that some of these participants had beeninvolved in other studies from our group. For example, 5 of the individualswith psychopathy and 6 of the comparison individuals had also performedthe differential reward–punishment task (Peschardt, Leonard, Morton, &Blair, in press), and 7 of the individuals with psychopathy and 5 of thecomparison individuals had also performed the emotional interrupt task(Mitchell, Richell, Leonard, & Blair, in press).

553RESPONSE REVERSAL AND PSYCHOPATHY

Measures

Raven’s Advanced Progressive Matrices, Set I. Set I of the Raven’sAdvanced Progressive Matrices (Raven, 1976) was used to provide anestimation of full scale IQ. This measure is not dependent on the partici-pant’s ability to read.

Psychopathy Checklist–Revised (PCL–R). The PCL–R (Hare, 1991)consists of 20 behavioral items that are scored on the basis of a file reviewand, where possible, a semistructured interview. High interrater reliabilitycoefficients for total scores (not less than 0.83) and high Cronbach’s alphacoefficients and iteritem correlations provide support that the PCL–R is areliable index of psychopathy in forensic settings (Hare, 1991).

After consent was obtained, the participants were interviewed. Partici-pants who declined an interview, but were willing to participate in theexperiment, were scored according to file notes (N � 4, split evenlybetween groups). Evidence suggests that the PCL–R can be scored reliablyand validly if detailed file information is available (Hare, 1991; Wong,1988). Interrater reliability was established by means of a Spearman rankcorrelation conducted on 33 inmates who were scored independently bytwo raters. The correlation, rranks � 0.89, p � .001, is comparable with thatpresented in the literature (Hare, 1991).

Probabilistic reversal learning task. The probabilistic reversal learn-ing task was programmed in Visual Basic (6.0) and was presented on a DellLaptop computer. Stimuli comprised 12 line drawings of animals(Snodgrass & Vanderwart, 1980) that had each been shaded in a differentcolor. Stimuli measured 4 cm � 4 cm and were presented on a graybackground.

Stimuli were assigned into pairs randomly at the beginning of the taskand remained in the same pairs throughout the task. On each trial, stimuliwere presented in pairs on the screen. Stimulus locations were assignedrandomly on each trial (there were 16 possible locations). The participanthad to choose one of the stimuli by clicking on it with the mouse. Uponchoosing they would receive either positive (“you win 100 points”) ornegative (“you lose 100 points”) feedback on the basis of the reinforcementcontingency of that pair. One of the animals in each pair was always morelikely than the other to be rewarded rather than punished. Participantsbegan the task with 0 points. A running total of points was always visibleat the bottom of the screen. Trials were self-paced.

The reinforcement contingencies were probabilistic such that the “cor-rect” pair was not always rewarded and the “incorrect” pair was not alwayspunished. The “correct” stimulus in each pair was always the one with thegreater ratio of reward–punishment. For example the “correct” stimulus ina pair with a 80–20 reward–punishment contingency would be rewardedon 8 out of every 10 trials and punished on 2 out of every 10 trials.Conversely, the “incorrect” stimulus would be punished on 8 out of every10 trials and rewarded on 2 out of every 10 trials. The order of probabilisticfeedback was randomized within the program.

There were six different pairs of stimuli: two test pairs that changedcontingency (reversing pairs: R) and four “dummy” pairs that did not(nonreversing pairs: NR; see Figure 1). The two reversing pairs hadcontingencies 100–0 and 80–20. The reinforcement contingency of thereversing pairs remained constant for 40 trials (Phase 1: acquisition of thediscrimination). Upon completing 40 trials of the reinforcement contin-

gency, the reversing pairs were reversed (Phase 2: reversal of the discrim-ination). Thus the previously correct stimulus became the incorrect stim-ulus and the previously incorrect stimulus now became the correctstimulus. Three of the four nonreversing dummy pairs had the contingency100–0, the fourth 80–20. The contingencies of the nonreversing pairsremained the same for the entire 40 trials that they were presented for.

Rather than learn about pairs of stimuli serially (e.g., all 80 trials of100–0 contingency and then all 80 trials of the 80–20 contingency),participants had experience with two different pairs of stimuli at any phaseof the study. One of these pairs was always a test pair in which thecontingencies reversed, the other a dummy pair in which the contingenciesdid not reverse. As can be seen in Figure 1, participants received a test pairon 66% of trials and the dummy pair on 33% of trials. This was done inorder to increase task difficulty; serial presentation might have allowed theparticipant to more easily calculate that after a set amount of trials, manyof the pairs changed contingency. In addition, because there were nonre-versing pairs, the participant could not be sure that all pairs would reverse.All of the participants received 270 trials, regardless of performance. Theorder of test pair presentation was randomized.

For the purposes of analysis a learning criterion of eight consecutivecorrect responses was imposed in both phases. Thus participants had tochoose the correct stimulus in each pair eight times consecutively beforethey had successfully passed that phase of the task. If participants did notmeet the learning criterion, total errors made were analyzed.

Procedure

Each participant was tested individually in a quiet room allocated by theinstitution. Subsequent to the administration of the Raven’s ProgressiveMatrices by the experimenter, the participants completed the responsereversal task (PCL–R interviews were conducted on a separate occasion).The experiment was described without informing the participant of theinvestigation’s specific objectives and expectations. After Swainson et al.(2000), the following instructions were presented on the computer screenand read aloud by the experimenter: Pairs of animals will appear on thescreen. On each go you have to choose one of these animals and thecomputer will tell you if your choice was correct or wrong. If it is correctyou will win 100 points. If it is incorrect you will lose 100 points. Eachanimal will sometimes be correct and sometimes be incorrect, but one ofthe animals will tend to be correct more often than the other one. Find outwhich animal is usually correct, and choose that animal every time. Stickwith it even if it is occasionally wrong. At some point it may change so thatthe other animal is usually correct, in which case you should choose thatone every time. Press “begin” to start the experiment.

Results

All of the participants reached the learning criterion for theacquisition of the 100–0 contingency. However, 1 comparison

Figure 1. A diagrammatic representation of the probabilistic responsereversal task. The orders presentation of Pairs 1–4 was randomized. Ineach segment trials from pairs were presented alternately.

Table 1Mean Age, (Standard Deviation), PCL–R Rating, and Raven’sScores for Adult Individuals With Psychopathy and Control

Group Age PCL–R Raven’s

Psychopathic (n � 20) 37.80 (7.64) 32.24 (1.95)* 8.05 (1.99)Control (n � 17) 34.53 (10.59) 7.45 (4.72) 8.00 (1.66)

Note. PCL–R � Psychopathy Checklist–Revised (maximum score � 40);Raven’s � Raven’s Progressive Matrices (maximum score � 12).* p � .001

554 BUDHANI, RICHELL, AND BLAIR

individual and 3 individuals with psychopathy failed to reach thecriterion for the acquisition of the 80–20 contingency. Given thatit is unclear that these participants sufficiently learned thestimulus–response association so that reversal could be assessed,we excluded these participants from analysis. One additional com-parison individual and 2 individuals with psychopathy failed toreach the criterion for the reversal of the 80–20 contingency.

Initially, errors were analyzed using a 2 (group: psychopathy/control) � 2 (contingency: 100–0/80–20) � 2 (phase: acquisition/reversal) repeated measures analysis of variance (ANOVA). Errorsto criterion were defined as all errors made prior to reaching thecriterion of eight consecutive correct responses. If this criterionwas not met, total errors were analyzed. This revealed a maineffect of group, F(1, 31) � 4.14, p � .05; the individuals withpsychopathy made more errors that comparison individuals, M(in-dividuals with psychopathy) � 5.74, SE � 0.81; M(comparisonindividuals) � 3.40, SE � 0.84, respectively. There was also ahighly significant main effect of contingency, F(1, 31) � 17.20,p � .001; the participants made less errors for the 100–0 contin-gency than the 80–20 contingency, M(100–0 contingency) �2.60, SE � 0.60; M(80–20 contingency) � 6.50, SE � .88,respectively. In addition, there was also a highly significant maineffect of phase, F(1, 31) � 23.97, p � .001; the participants madefewer errors during acquisition than reversal, M(acquisition) �1.76, SE � 0.30; M(reversal) � 7.33, SE � 1.11, respectively.Crucially, the group by phase interaction was significant, F(1,31) � 6.00, p � .05. Whereas the groups did not differ in theirnumber of errors during acquisition, F(1, 31) � 1, ns, the groupsdid differ in their number of errors during the reversal phase, F(1,31) � 5.38, p � .05; see Figure 2.

Acquisition in Comparison to Response Reversal

Specific analyses showed that the comparison individuals foundthe 80–20 acquisition more difficult than the 100–0 reversal, F(1,16) � 5.02, p � .05; M(80–20 acquisition) � 4.18, SD � 5.634;M(100–reversal) � 2.65; SD � 0.86, respectively. However, asreported above, there was no significant group difference for the80–20 acquisition, F(1, 37) � 1, ns, but there was a significantgroup difference in the 100–0 reversal, F(1, 36) � 3.11, p � .05,one-tailed. In short, the dissociable pattern of impairment betweenacquisition and reversal shown by the individuals with psychopa-thy cannot be attributed to a task difficulty effect.

Win–Stay, Lose–Shift Analysis

Finally data were recoded to allow analysis of win–stay, lose–shift strategies. Specifically, we examined (a) The participant’sresponse to receiving a reward having made the correct response;that is, would they stay with this correct response on the subsequenttrial (win–stay) or inappropriately shift their response? As participantsmade different numbers of correct responses, a win–stay percentagewas calculated: no. of win–stay/(no. of wins–stay � no. of win–shift) � 100. (b) The participant’s response to receiving a punishmenthaving made the incorrect response; that is, would this shift awayfrom the incorrect response (lose–shift) or inappropriately stay withtheir response? As participants made different numbers of incorrectresponses, a lose–shift percentage was calculated: no. of lose–shift/(no. of lose–shift � no. of lose–stay) � 100.

The IES model predicted that individuals with psychopathyshould be less likely to stay with a correct response after a rewardduring the reversal phase than comparison individuals. This pre-diction was confirmed, F(1, 31) � 3.75, p � .05, one-tailed,M(individuals with psychopathy) � 89.8%, SE � 2.78%; M(com-parison individuals) � 95.92%, SE � 1.58%, respectively. TheIES model predicted that individuals with psychopathy should beless likely to shift away from an incorrect response after a pun-ishment during the reversal phase than comparison individuals.This prediction was not confirmed, F(1, 31) � 1, ns. However, thiswas principally because punishment during the reversal phases ofthe paradigm had no predictive power with respect to the partici-pant’s subsequent response; participants were at chance as towhether they would make the same incorrect response or thealternative correct response after a punished incorrect response,M(individual with psychopathy) � 53.22%, SE � 5.28%; M(com-parison individuals) � 49.1%, SE � 3.48%, respectively.

There were no significant group differences during acquisition.The individuals with psychopathy were as likely to stay with acorrect response after a reward as the comparison individuals, F(1,31) � 1, ns; M(individuals with psychopathy) � 93.0%, SE �2.86%; M(comparison individuals) � 94.0%, SE � 2.50%, respec-tively. Similarly, the individuals with psychopathy were as likelyto shift away from an incorrect response after a punishment as thecomparison individuals, F(1, 31) � 1, ns; M(individuals withpsychopathy) � 81.9%, SE � 4.73%; M(comparison individu-als) � 86.2%, SE � 5.13%, respectively.

Discussion

This study examined the ability of adult individuals with psy-chopathy to perform a novel probabilistic response reversal task.As expected, the individuals with psychopathy performed compa-rably with control participants in the acquisition phase of the task.Also, in line with predictions, individuals with psychopathy pre-sented with impairment relative to comparison individuals in thereversal phase of the task. The salience of the contingency had acomparable impact on both groups in both acquisition and re-sponse reversal.

This study is in line with previous experiments using adultindividuals with psychopathy that have found intact acquisition butimpaired reversal/extinction in response reversal and extinctionparadigms (Mitchell, College, Leonard, & Blair, 2002). This dis-sociation is of importance particularly as the current results cannotbe attributed to a task difficulty effect. The individuals with

Figure 2. Errors to criterion made by adults in the acquisition andreversal phases (standard error bars). Maximum errors � 40.

555RESPONSE REVERSAL AND PSYCHOPATHY

psychopathy showed no impairment, relative to the comparisonindividuals, in the 80–20 acquisition condition but did showimpairment in the 100–0 reversal condition. However, for thecomparison individuals, the 80–20 acquisition was significantlymore difficult than the 100–0 reversal. In other words, the indi-viduals with psychopathy showed impairment relative to the com-parison individuals on the condition that was easier for the com-parison individuals. This dissociation in impairment between theacquisition and reversal phases is problematic for positions stress-ing either a general impairment in processing punishment-relatedinformation (Lykken, 1995; Patrick, 1994) or an inability to shiftattention away from the goal of responding to gain reward to theperipheral punishment information (Newman, 1998; Patterson &Newman, 1993).

As the fear positions suggest that individuals with psychopathyare impaired in processing punishment-related information(Lykken, 1995; Patrick, 1994), it should be predicted that individ-uals with psychopathy should show impairment in both acquisitionand reversal as both require appropriate learning on the basis ofpunishment-related information. However, the individuals withpsychopathy showed no significant impairment during acquisition.Of course, it could be argued that because correct responses arerewarded, acquisition could be achieved using reward-related in-formation alone and that punishment information is less relevantduring acquisition. However, this argument appears incorrect. Apunished incorrect response during acquisition was, for bothgroups on over 80% of occasions, followed by a correct responseon the subsequent presentation of the stimulus. Indeed, if anything,punishment information was less relevant during reversal. A pun-ished incorrect response during reversal was, for both groups, aslikely to be followed by a correct response as an incorrect responseon the subsequent presentation of the stimulus.

Of course, the fear dysfunction accounts (Lykken, 1995; Patrick,1994) can be adapted. The original fear dysfunction positionsassumed that fear was mediated by a unitary cognitive entity, forexample, the Behavioral Inhibition System (Gray, 1987). How-ever, the empirical literature now strongly suggests that there is nosingle fear system but rather that there are a series of at leastpartially separable neural systems that are engaged in specificforms of processing that can be subsumed under the umbrella termfear. For example, dissociable neural systems mediate respondingto social threats, aversive conditioning, and specific forms ofinstrumental learning (Amaral, 2001; Baxter & Murray, 2002;Killcross, Robbins, & Everitt, 1997; Prather et al., 2001). Propo-nents of fear dysfunction accounts have made reference to amyg-dala dysfunction (Patrick, 1994). Indeed, the IES account (Blair,2004) can be considered an extension of the fear dysfunctionpositions and also refers to amygdala dysfunction (and dysfunctionin orbital and ventrolateral frontal cortex). Amygdala dysfunctionis not associated with impairment in the object discriminationnecessary for the acquisition stage of the current paradigm (Baxter& Murray, 2002). In short, the current data constrains the feardysfunction positions. Specifically, it suggests that the processingof punishment information is only impaired in the context of tasksreliant on the amygdala (cf. Blair, 2004).

The current results also suggest that the response modulationposition needs adaptation. This position might predict impairmentin both the acquisition and reversal phases of response reversal asboth require in the terms of this hypothesis (Newman, 1998;Patterson & Newman, 1993), the participant to shift attention from

the goal to gain reward to process the punishment information.Alternatively, it could be argued that response modulation predictsthat individuals with psychopathy should only show impairmentwhen they are required to alter a dominant response set followingpunishment (i.e., to shift their incorrect responses following pun-ishment during the reversal phase). However, none of these po-tential predictions were confirmed. Individuals with psychopathyonly showed impairment during the reversal phase of the study.However, this was not due to reduced shifting away from the nowincorrect dominant response after punishment. Their impairmentwas far more related to the tendency of individuals with psychop-athy to be less likely to stay with a rewarded correct response.

The results of the current study are compatible with the IES(Blair, in press). As noted above, according to the IES model, adultindividuals with psychopathy present with amygdala and orbitalfrontal cortex dysfunction (in particular Brodmann’s Area 47).Following Baxter and Murray (2002), it is suggested that theamygdala is crucial for the formation of stimulus–punishmentassociations. Individuals with psychopathy should present withimpairment on instrumental leaning tasks known to be reliant onthe formation of stimulus–reinforcement associations (such aspassive avoidance learning) but intact on instrumental learningtasks known to be reliant on the formation of stimulus–responseassociations. Individuals with psychopathy present with severedifficulties on passive avoidance learning tasks (Blair et al., 2004;Newman & Kosson, 1986) but are intact on object discriminationtasks such as the acquisition phase of the current study. Orbital andventrolateral frontal cortex are known to be involved in responsereversal and extinction (Butter, 1969; Cools et al., 2002; Dias etal., 1996; Rolls, Hornak, Wade, & McGrath, 1994; Swainson et al.,2000). According to the IES model (Blair, 2004), it is suggestedthat Brodmann’s Area 47 is particularly involved in the detectionof contingency change and the gating of motor responding withreference to that contingency change. It is argued that individualswith psychopathy may be impaired in one or both of these pro-cesses. In short, the intact performance of individuals with psy-chopathy even on the relatively difficult (for comparison individ-uals) acquisition of the 80–20 contingency in the context ofimpaired performance on particularly the relatively easy (for com-parison individuals) acquisition of the 100–0 reversal, is highlycompatible with the IES model.

On the basis of previous human neuropsychological work (Ber-lin et al., 2004; Hornak et al., 2004), the IES position predicted thatindividuals with psychopathy should be less likely to stay with arewarded correct response and less likely to shift away from apunished incorrect response during reversal than comparison indi-viduals. The first of these predictions was confirmed. However, thesecond was not; it is surprising that both groups were as likely toshift away from, as to stay with, a punished incorrect responseduring reversal. Currently, the reason for this absence of groupdifferences remains unclear.

The results of the current study were broadly in line with thedata from our previous study with boys with psychopathic tenden-cies (Budhani & Blair, 2005). In this study, the boys with psycho-pathic tendencies showed no impairment in acquisition for any ofthe contingencies tested (100–0, 90–10, 80–20, or 70–30). How-ever, they showed progressively greater reversal impairment, rel-ative to the comparison boys, as the contingency became lesssalient. In contrast to the adults with psychopathy in the currentstudy, the boys with psychopathic tendencies presented with no

556 BUDHANI, RICHELL, AND BLAIR

reversal learning impairment for the 100–0 contingency but weresignificantly impaired, relative to the comparison boys, for theother three contingencies. In short, the current study and the earlierstudy using a very similar paradigm with boys with psychopathictendencies (Budhani & Blair, 2005) echo the results of our earlierwork with the ID/ED task and the Bechara gambling task (Blair,College, & Mitchell, 2001; Mitchell et al., 2002). Both adults withpsychopathy and children with psychopathic tendencies presentwith impairment in response reversal but the impairment found inadults is significantly more pronounced relative to that seen inboys with psychopathic tendencies. Moreover, the reversal impair-ment seen in adults with psychopathy is present even for salientcontingencies (100–0). Children with psychopathic tendenciesshow no impairment for these salient contingency changes (Blairet al., 2001; Budhani & Blair, 2005).

One interesting feature of the current results was there was nosignificantly greater impact of reduced contingency salience onreversal learning in the individuals with psychopathy than thecomparison individuals. Within the IES model, we follow thecomputational modeling work of Dayan and colleagues who havestressed the importance of temporal difference calculations(O’Doherty et al., 2004; Schultz, Dayan, & Montague, 1997;Sutton & Barto, 1981). The temporal difference error is the dif-ference between the expected value associated with a stimulus/action and the actual value currently received with respect to thatstimulus/action. In other words, unexpected rewards induce largepositive temporal difference errors (initiating rapid learning). Ab-sent highly expected rewards induce large negative temporal dif-ference errors (initiating response reversal/extinction). For salient100–0 contingency changes, the previous action has always beenrewarded and now is always punished; that is, the initial negativetemporal difference errors after contingency change will be verylarge, a strong impetus for response reversal/extinction. For lesssalient 80–20 contingency changes, the expected reward valueassociated with the old action will be less (because it was onlyrewarded 80% of the time) and the current values are less likely tobe punishments (because these are also only received 80% of thetime); that is, the initial negative temporal difference errors aftercontingency change will be smaller. The current data indicating nodifferential impact of contingency salience on reversal learning inthe individuals with psychopathy, relative to the comparison indi-viduals, suggests that whatever the magnitude of negative temporaldifference error, individuals with psychopathy are impaired withtheir initiation of reversal learning. Whether this is due to aninability to successfully generate negative temporal differenceerrors or an inability to use these errors to successfully initiateresponse reversal is a matter under current empirical enquiry.

It is unclear why there is greater response reversal impairment inadults with psychopathy than in children with psychopathic ten-dencies. However, there are several possibilities. First, the geneticanomalies associated with psychopathy might affect the develop-ment of the amygdala and orbital frontal cortex independently ofone another. The genetic contribution might affect the functioningof the amygdala at an early age but progressively affect thefunctioning of orbital/ventrolateral frontal cortex functioning pro-gressively with age. Second, it is known that the amygdala andorbital frontal cortex are massively interconnected (Amaral, Price,Pitkanen, & Carmichael, 1992; Carmichael & Price, 1995). Areduction in afferent input from the amygdala could disrupt thedevelopment of orbital frontal cortex to an increasingly greater

degree as development progresses. Third, studies suggest thatpsychopathy is associated with higher rates of drug abuse and polydrug use (Hemphill, Hart, & Hare, 1994; Smith & Newman, 1990).Alcohol- and drug-dependent individuals present with impairedperformance on measures assessing the functioning of orbitalfrontal cortex (Bechara et al., 2001; Grant, Contoreggi, & London,2000; Rogers & Robbins, 2001). It is thus also possible that theapparent developmental effect seen here is simply a consequenceof the lifestyle chosen by psychopathic individuals. Fourth, it ispossible that the PCL–R used to assess psychopathic tendencies inadults and the antisocial process screening device (ASPD) used toidentify psychopathic tendencies in children, lead to the selectionof participants with different pathologies. However, it should benoted in this context that the functional impairments seen inchildren and adults with psychopathic tendencies are very similarin form and magnitude with respect to amygdala functioning andin form but not magnitude with respect to orbital/ventrolateralprefrontal cortex functioning. In addition, the behavioral depic-tions described by the PCL–R and APSD are similar.

There are two potential caveats to consider with respect to thecurrent study. First, we did not include a measure of anxiety. It hasbeen suggested, on the basis of self-report measures of anxiety,that both comparison and psychopathic individuals can vary on thedimension of negative affectivity (Schmitt & Newman, 1999).However, in our own ongoing work and in the literature moregenerally, there are no indications that patients with anxiety dis-orders show any superiority for response reversal learning. Sec-ond, the possibility that differences in the level of motivationmight have influenced the results. However, it should be noted thatthe individuals with psychopathy were performing similarly to thecomparison individuals during the acquisition of the 80–20 con-tingency but showing impairment for the reversal of the 100–0and the 80–20 contingencies. This is despite the fact that thecomparison individuals found the acquisition of the 80–20 con-tingency more difficult and the reversal of the 80–20 contingencyeasier than the reversal of the 100–0 contingency. In other words,a motivation-based account would need to explain how reducedmotivation would give rise to difficulty with the “easy” 100–0reversal and the “difficult” 80–20 reversal but not the “mediumdifficulty” 80–20 acquisition.

In summary, in this study, we investigated the performance of adultindividuals with psychopathy on a probabilistic response reversaltask. In line with predictions, adults with psychopathy performed theacquisition phases successfully. Also as predicted they showed aperformance deficit in both simple and probabilistic conditions rela-tive to comparison individuals. We suggest that this data is problem-atic for accounts suggesting either generalized difficulties processingpunishment information or response modulation (i.e., shifting atten-tion away from the goal of responding to gain reward to the peripheralpunishment information). We do however suggest that they are in linewith cognitive accounts such as the IES model.

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Received March 1, 2004Revision received January 21, 2005

Accepted January 10, 2006 �

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