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

Abstract

Previous studies exploring the neural substrates of executive functioning used task-specific analyses, which might not be the most appropriate approach due to the difficulty of precisely isolating executive functions. Consequently, the aim of this study was to use positron emission tomography (PET) to reexamine by conjunction and interaction paradigms the cerebral areas associated with three executive processes (updating, shifting, and inhibition). Three conjunction analyses allowed us to isolate the cerebral areas common to tasks selected to tap into the same executive process. A global conjunction analysis demonstrated that foci of activation common to all tasks were observed in the right intraparietal sulcus, the left superior parietal gyrus, and at a lower statistical threshold, the left lateral prefrontal cortex. These regions thus seem to play a general role in executive functioning. The right intraparietal sulcus seems to play a role in selective attention to relevant stimuli and in suppression of irrelevant information. The left superior parietal region is involved in amodal switching/integration processes. One hypothesis regarding the functional role of the lateral prefrontal cortex is that monitoring and temporal organization of cognitive processes are necessary to carry out ongoing tasks. Finally, interaction analyses showed that specific prefrontal cerebral areas were associated with each executive process. The results of this neuroimaging study are in agreement with cognitive studies demonstrating that executive functioning is characterized by both unity and diversity of processes.

Figure 1

Brain activation observed in the conjunction analysis between the eight executive tasks (in comparison to their respective control tasks). Regions with significant rCBF increase are superimposed upon a T1‐weighted MRI slice normalized into a standard stereotactic space [Talairach and Tournoux, 1988]. Coronal sections are shown, respectively, 69 and 43 mm posterior to the anterior commissure and transverse sections are shown, respectively, 51 and 39 mm above the reference plane. Coordinates of all significant regions are given in Table I.

Figure 2

Plots of relative cerebral activity for the regions highlighted in the conjunction analysis of the three executive processes. a: Left superior parietal cortex (BA 7). b: Right intraparietal sulcus. c: Left middle frontal gyrus (BA 46). d: Left middle frontal gyrus (BA 10). e: Left inferior frontal gyrus (BA 45). The coordinates of each voxel are indicated on the y‐axis (Montreal Neurological Institute [MNI] coordinates). Cognitive tasks are represented on the x‐axis (1–3, updating control tasks; 4–6, updating experimental tasks; 7–9, shifting control tasks; 10–12, shifting experimental tasks; 13–14, inhibition control tasks; 15–16, inhibition experimental tasks).

Figure 3

Plots of relative cerebral activity in the 16 cognitive tasks. First line: cerebral areas more active in the updating process compared to that in shifting (a–c) and inhibition (d, e) processes. Second line: cerebral areas more active in the shifting process compared to that in the inhibition (f, g) process. Third line: cerebral areas more active in the inhibition process compared to that in the updating (h) and shifting (i) processes. The coordinates of each voxel are indicated on the y‐axis (MNI coordinates); cognitive tasks are represented on the x‐axis (1–3, updating control tasks; 4–6, updating experimental tasks; 7–9, shifting control tasks; 10–12, shifting experimental tasks; 13–14, inhibition control tasks; 15–16, inhibition experimental tasks).