Brain Advance Access originally published online on September 19, 2006
Brain 2006 129(12):3315-3328; doi:10.1093/brain/awl244
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Functions of the left superior frontal gyrus in humans: a lesion study
1 Federation de Neurologie Paris, France 2 INSERM U.610 Paris, France 3 Service de Neuroradiologie Paris, France 4 Service de Neurochirurgie Paris, France 5 Urgences cérébro-vasculaires, AP-HP, Hôpital de la Pitié-Salpêtrière Paris, France 6 Université Pierre et Marie Curie-Paris 6 Paris, France 7 Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology MA, USA
Correspondence to: Richard Levy, MD, PhD, Fédération de Neurologie, Hôpital de la Salpêtrière, 47, bd de l'hôpital, 75651 Paris cedex 13, France E-mail: richard.levy{at}psl.aphp.fr
The superior frontal gyrus (SFG) is thought to contribute to higher cognitive functions and particularly to working memory (WM), although the nature of its involvement remains a matter of debate. To resolve this issue, methodological tools such as lesion studies are needed to complement the functional imaging approach. We have conducted the first lesion study to investigate the role of the SFG in WM and address the following questions: do lesions of the SFG impair WM and, if so, what is the nature of the WM impairment? To answer these questions, we compared the performance of eight patients with a left prefrontal lesion restricted to the SFG with that of a group of 11 healthy control subjects and two groups of patients with focal brain lesions [prefrontal lesions sparing the SFG (n = 5) and right parietal lesions (n = 4)] in a series of WM tasks. The WM tasks (derived from the classical n-back paradigm) allowed us to study the impact of the SFG lesions on domain (verbal, spatial, face) and complexity (1-, 2- and 3-back) processing within WM. As expected, patients with a left SFG lesion exhibited a WM deficit when compared with all control groups, and the impairment increased with the complexity of the tasks. This complexity effect was significantly more marked for the spatial domain. Voxel-to-voxel mapping of each subject's performance showed that the lateral and posterior portion of the SFG (mostly Brodmann area 8, rostral to the frontal eye field) was the subregion that contributed the most to the WM impairment. These data led us to conclude that (i) the lateral and posterior portion of the left SFG is a key component of the neural network of WM; (ii) the participation of this region in WM is triggered by the highest level of executive processing; (iii) the left SFG is also involved in spatially oriented processing. Our findings support a hybrid model of the anatomical and functional organization of the lateral SFG for WM, according to which this region is involved in higher levels of WM processing (monitoring and manipulation) but remains oriented towards spatial cognition, although the domain specificity is not exclusive and is overridden by an increase in executive demand, regardless of the domain being processed. From a clinical perspective, this study provides new information on the impact of left SFG lesions on cognition that will be of use to neurologists and neurosurgeons.
Key Words: prefrontal cortex; working memory; cognitive functions; human; neuropsychology
Abbreviations: CI, confidence interval; FEF, frontal eye field; MMSE, Mini-Mental State Examination; PFC, prefrontal cortex; SEM, standard error of measurement; SFG, superior frontal gyrus; WM, working memory
Received December 16, 2005. Revised August 4, 2006. Accepted August 10, 2006.
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