Neural correlates of error-related learning deficits in individuals with psychopathy

Abstract

Background. Psychopathy (PP) is associated with a performance deficit in a variety of stimulus-response and stimulus-reinforcement learning paradigms. We tested the hypothesis that failures in error monitoring underlie these learning deficits.Method. We measured electrophysiological correlates of error monitoring [error-related negativity (ERN)] during a probabilistic learning task in individuals with PP (n=13) and healthy matched control subjects (n=18). The task consisted of three graded learning conditions in which the amount of learning was manipulated by varying the degree to which the response was predictive of the value of the feedback (50, 80 and 100 %).Results. Behaviourally, we found impaired learning and diminished accuracy in the group of individuals with PP. Amplitudes of the response ERN (rERN) were reduced. No differences in the feedback ERN (fERN) were found. Conclusions.The results are interpreted in terms of a deficit in initial rule learning and subsequent generalization of these rules to new stimuli. Negative feedback is adequately processed at a neural level but this information is not used to improve behaviour on subsequent trials. As learning is degraded, the process of error detection at the moment of the actual response is diminished. Therefore, the current study demonstrates that disturbed error-monitoring processes play a central role in the often reported learning deficits in individuals with PP.

Reversal deficits in individuals with psychopathy in explicit but not implicit learning conditions

“…Combined, the previous findings from our laboratory 14,18 suggest that in individuals with psychopathy, automatic adaptation of behaviour is unaffected, but impairments are present when adaptation relies on intentional use of available information. From this perspective, it can be hypothesized that response reversal is compromised in individuals with psychopathy specifically when instructions provide a context promoting controlled behavioural adaptation.…”

“…They knew in advance that each of the 2 cues was more often followed by either the go or the no-go stimulus, but that these predictive relationships were probabilistic. These instructions increased awareness of the cue-stimulus contingencies and also resemble those used in the studies conducted by von Borries and colleagues 18 and Budhani and colleagues. 7 However, in our study, participants were not explicitly informed that the predictive relationships could change during the task to prevent the task from becoming too easy, thereby reducing the risk of floor effects.…”

“…8 There is growing evidence that cognitive deficiencies observed in psychopathy include abnormalities in emotional processing, 9,10 modulation of attention, 11,12 aspects of action monitoring [13][14][15] and, importantly, associative learning. 6,7,[16][17][18] Behavioural results on associative learning in individuals with psychopathy show deficiencies in tracking stimulus-outcome contingencies and in subsequently altering behaviour in the face of changes in these contingencies. 6,7 In the study by Budhani and colleagues, 7 individuals with psychopathy showed normal acquisition but impaired response reversal in a task in which stimulusoutcome contingencies varied according to predetermined probabilities of gaining reward/ punishment (i.e., probabilistic reinforcement learning).…”

“…This prediction is also supported by the observation that the participants with OFC lesions in the study by Rolls and colleagues 20 were aware of (and could verbalize) the fact that the contingencies had changed, but were still unable to execute response reversal. Also, in the studies by von Borries and colleagues 18 and Budhani and colleagues, 7 participants were aware that the goal of the task was to learn based on reinforcement. A second prediction offered by the distinction between automatic and controlled behavioural adaptation in individuals with psychopathy is that response reversal should be intact when automatic learning is predominant.…”

Punishment and psychopathy: a case-control functional MRI investigation of reinforcement learning in violent antisocial personality disordered men

“…13 In behavioural studies off enders with antisocial personality disorder and psychopathy have shown notable impairment in using reinforcement information when choosing between punished and rewarded objects in passive avoidance, 14 extinction, 15 and reversal learning tasks. 11,16,17 The failure to use punishment information to signal inappropriate behaviour is thought to be the primary defi cit in psychopathy, and emerges early in childhood. 18 Reversal learning tasks examine the ability to adjust behaviour to changes in reinforcement contingency.…”