Exploration of the neural substrates of executive functioning by functional neuroimaging

Collette, Fabienne; Hogge, Michaël; Salmon, Éric; Van der Linden, Martial · 2005 · OpenAlex-citations

DOI: 10.1016/j.neuroscience.2005.05.035

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Summary

This review examines the neural substrates of executive functioning, addressing the debate over whether these high-level cognitive processes rely on a unitary frontal lobe system or a distributed cerebral network. Motivated by neuropsychological evidence showing that executive functions—such as updating, shifting, and inhibition—are distinct yet related processes, the authors analyze functional neuroimaging studies (PET and fMRI) to map the specific brain regions involved. The review highlights that traditional subtraction designs often yield heterogeneous results due to the complex, multi-component nature of executive tasks, prompting an evaluation of more rigorous conjunction and interaction analyses. The authors first review studies using subtraction paradigms, where executive tasks are compared to control tasks. These studies demonstrate that executive functions recruit both anterior (prefrontal) and posterior (primarily parietal) regions. For instance, updating tasks activate the dorsolateral prefrontal cortex and parietal areas, with the frontopolar cortex playing a predominant role in evaluating internally generated information. Shifting tasks engage a unitary set of mechanisms involving the superior parietal cortex and dorsolateral prefrontal cortex. Inhibition studies reveal heterogeneous activations, including the inferior frontal gyrus and anterior cingulate, depending on the specific inhibitory demand, such as resolving interference versus suppressing prepotent responses. Dual-task coordination appears to rely on increased activity or interaction within networks already activated by single tasks, specifically involving a left-sided fronto-parietal network. To address the limitations of subtraction designs, the review details recent conjunction analyses that identify common neural substrates across multiple tasks assessing the same executive process. These analyses confirm the critical role of parietal areas and demonstrate specificity in the neural substrates for updating, shifting, and inhibition. Furthermore, the authors note that fMRI studies reveal both transient and sustained activity patterns in these regions, suggesting that the temporal dynamics of activation are as important as spatial localization for characterizing functional roles. The significance of this work lies in its confirmation that executive functioning is not restricted to the frontal lobes but depends on a distributed network including posterior regions. The findings support the hypothesis that while executive functions share common neural mechanisms, they also possess distinct neural substrates. The review concludes that future research must account for both the localization and the temporal pattern of cerebral activity to better understand the functional role of areas associated with executive control, moving beyond the limitations of simple subtraction designs.

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