Brain Advance Access originally published online on February 25, 2004
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Brain, Vol. 127, No. 5, 1108-1126, 2004
© 2004 Guarantors of Brain
doi: 10.1093/brain/awh135
Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions
1 University of Oxford, Department of Experimental Psychology and 2 Oxford Centre for Enablement, Department of Clinical Neurology, Radcliffe Infirmary, UK
Correspondence to: Professor E. T. Rolls, University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK E-mail: edmund.rolls{at}psy.ox.ac.uk
Damage to the orbitofrontal cortex (OFC) in humans has been associated with disinhibited or socially inappropriate behaviour and emotional changes. Some of the changes may be related to difficulty in responding correctly to rewards and punishers, in that these patients have difficulty in learning to correct their choice of a visual stimulus when it is no longer associated with reward. We extend this fundamental approach by investigating the relationship between frontal dysfunction and impulsive behaviour, the behavioural, emotional and personality changes seen in patients with prefrontal cortex damage, and thus in addition illuminate the cognitive and biological processes that are impaired in impulsive people. OFC patients (n = 23) performed more impulsively on both self-report and cognitive/behavioural tests of impulsivity, reported more inappropriate ‘frontal’ behaviours, and performed worse on a stimulus–reinforcement association reversal task, than non-OFC prefrontal cortex lesion control (n = 20) and normal control (n = 39) participants. Further, OFC patients experienced more subjective anger than non-OFC and normal participants, and less subjective happiness than normals; and had a faster subjective sense of time (overestimated and underproduced time intervals) than normal controls, while non-OFC patients did not differ from normals. Finally, both OFC and non-OFC patients were less open to experience than normal participants. There were no differences between OFC patients, non-OFC lesion patients and normal controls on all other personality traits, most notably extraversion. In a spatial working memory task, the non-OFC group, most of whom had dorsolateral prefrontal cortex lesions, were impaired in that they repeatedly returned to previously chosen empty locations (‘within errors’), whereas OFC patients were not impaired on this measure. Thus there is a dissociation between the effects of OFC damage which does not affect this measure of spatial working memory but does affect impulsive and inappropriate behaviour, reversal, personality, time perception and emotion; and dorsolateral prefrontal cortex damage which does affect this measure of spatial working memory, but not impulsive and inappropriate behaviour, reversal, personality, time perception and emotion. The effects of OFC damage on impulsive and related behaviours described here have implications for understanding impulsive behaviour.
Key Words: impulsivity; time perception; emotion; personality; orbitofrontal cortex
Abbreviations: ACA= anterior communicaing artery; BIS = Barrat Impulsiveness Scale; DLFC = dorsolateral prefrontal cortex; MCA = middle cerebral artery; MFFT = Matching Familiar Figures Test; OFC = orbitofrontal cortex; PFC = prefrontal cortex; SWM = spatial working memory
Received July 10, 2003. Accepted December 27, 2003.
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