Brain Advance Access originally published online on June 30, 2006
Brain 2006 129(8):2177-2188; doi:10.1093/brain/awl160
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Impact of frontal white matter lesions on performance monitoring: ERP evidence for cortical disconnection
1 Developmental Cognitive Neuroscience Unit, Institute of Child Health, University College London, Great Ormond Street Hospital for Children NHS Trust London, UK 2 Department of Radiology, Institute of Child Health, University College London, Great Ormond Street Hospital for Children NHS Trust London, UK 3 Neurosciences Unit, Institute of Child Health, University College London, Great Ormond Street Hospital for Children NHS Trust London, UK
Correspondence to: Dr Alexandra Hogan, Developmental Brain-Behaviour Unit, School of Psychology, University of Southampton, Highfield, Southampton, SO17 1BJ, UK E-mail: a.hogan{at}soton.ac.uk
We examined the impact of discrete white matter lesions in the frontal lobes on event-related potential (ERP) correlates of performance monitoring. We tested the hypothesis that abnormal performance monitoring may result from injury to white matter without evidence of injury to grey matter in the frontal lobes. It was predicted that such lesions may result in disconnection of the lateral and medial frontal cortices. The close interaction of these two areas has been implicated in performance monitoring. Two fast-choice response tasks were administered to patients with MRI-confirmed frontal white matter lesions due to sickle cell disease (SCD) vasculopathy (n = 11; age = 11–23 years; 6 unilateral left lesions and 5 bilateral lesions) and two control groups: SCD patients without brain lesions and non-sickle cell sibling controls (n = 11 each). Stimulus-locked ERP components N2 and P3 were not significantly affected by presence of lesions. The difference between response-locked components to correct trials (correct-response negativity—CRN) and erroneous trials (error-related negativity—ERN) was diminished in patients with unilateral and bilateral frontal white matter lesions. This finding was due to a significantly attenuated ERN amplitude in lesion patients compared with both sibling and non-lesion control groups. These ERP findings were not due to performance differences between groups and hence reflect a compromised neural substrate underlying performance monitoring. The latter may also contribute to the deficits in executive function tasks observed in these patients. As disruption to ERP markers of error processing was found in the absence of lesions to the lateral or medial frontal cortex, we conclude that a functional connection between these areas facilitates performance monitoring, possibly implemented via tracts traversing the deep frontal white matter.
Key Words: performance monitoring; white matter injury; sickle cell disease; event-related potentials; executive functions
Abbreviations: ACC, anterior cingulate cortex; CRN, correct-response negativity; CRT, choice-response task; DLFC, dorsolateral frontal cortex; ERN, error-related negativity; ERP, event-related potential; pMFC, posterior medial frontal cortex; SCD, sickle cell disease; SOPT, Self-Ordered Pointing Test; WCST, Wisconsin Card Sort Test
Received January 26, 2006. Revised May 4, 2006. Accepted May 5, 2006.
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