Exploring the unity and diversity of the neural substrates of executive functioning

Collette, Fabienne; Van der Linden, Martial; Laureys, Steven; Delfiore, Guy; Degueldre, Christian; Luxen, André; Salmon, Éric · 2005 · OpenAlex-citations

DOI: 10.1002/hbm.20118

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Summary

This study investigates the neural substrates of executive functioning, specifically addressing the debate regarding whether executive processes share common neural mechanisms (unity) or rely on distinct, specialized brain regions (diversity). Previous neuroimaging research often relied on task-specific subtraction designs, which struggle to isolate specific executive components due to the multicompound nature of these tasks. To overcome this limitation, the authors employed positron emission tomography (PET) to examine three core executive processes identified by Miyake et al. (2000): updating, shifting, and inhibition. The research aimed to identify cerebral areas commonly activated across these functions as well as regions specific to each process, using conjunction and interaction analyses rather than traditional subtraction methods. Thirty-seven healthy right-handed volunteers participated in the study, divided into three groups corresponding to the executive processes under investigation. The experimental design utilized matched control tasks to isolate specific cognitive demands. Updating tasks required subjects to maintain and update information in working memory using consonants, words, or sounds, whereas control tasks involved simple storage. Shifting tasks required alternating between arithmetic operations, verbal categorizations, or visual categorizations (Navon figures), with control tasks involving single, consistent operations. Inhibition tasks included the Stroop task and an antisaccade task, requiring the suppression of prepotent responses, compared against control tasks lacking inhibitory demands. PET data were analyzed using statistical parametric mapping (SPM99) with random-effect models to account for inter-subject variability. Behavioral results confirmed that experimental tasks were more demanding than control tasks, evidenced by lower accuracy in updating tasks and slower response times in shifting and inhibition tasks. Neuroimaging results revealed a pattern of both unity and diversity. A global conjunction analysis identified shared activation across all executive tasks in the right intraparietal sulcus and the left superior parietal gyrus (BA 7). At a lower statistical threshold, the left lateral prefrontal cortex (BA 9, 10/46, and 45) was also commonly activated, suggesting these regions support general executive functions such as selective attention, amodal switching, and monitoring. Interaction analyses demonstrated diversity by identifying specific prefrontal areas associated with each process: updating was linked to the left inferior frontal gyrus, shifting to the right inferior frontal gyrus, and inhibition to the right middle frontal gyrus. The findings support the hypothesis that executive functioning is characterized by both unity and diversity. The study provides empirical evidence that while specific prefrontal regions are dedicated to distinct executive processes, posterior parietal and lateral prefrontal regions play a general, integrative role across various executive demands. This challenges earlier views that localized frontal activity alone defines executive function, highlighting instead a distributed network where posterior regions contribute to general control mechanisms. The use of conjunction and interaction analyses proved effective in disentangling common and specific neural substrates, offering a more nuanced understanding of the cognitive architecture underlying executive control.

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• executive function