A meta-analysis of executive components of working memory

Abstract

Working memory (WM) enables the online maintenance and manipulation of information and is central to intelligent cognitive functioning. Much research has investigated executive processes of WM in order to understand the operations that make WM "work." However, there is yet little consensus regarding how executive processes of WM are organized. Here, we used quantitative meta-analysis to summarize data from 36 experiments that examined executive processes of WM. Experiments were categorized into 4 component functions central to WM: protecting WM from external distraction (distractor resistance), preventing irrelevant memories from intruding into WM (intrusion resistance), shifting attention within WM (shifting), and updating the contents of WM (updating). Data were also sorted by content (verbal, spatial, object). Meta-analytic results suggested that rather than dissociating into distinct functions, 2 separate frontal regions were recruited across diverse executive demands. One region was located dorsally in the caudal superior frontal sulcus and was especially sensitive to spatial content. The other was located laterally in the midlateral prefrontal cortex and showed sensitivity to nonspatial content. We propose that dorsal-"where"/ventral-"what" frameworks that have been applied to WM maintenance also apply to executive processes of WM. Hence, WM can largely be simplified to a dual selection model.

Figure 1.

Renderings of regions related to executive processes of WM. Colors denote gyral definitions derived from the AAL atlas (Tzourio-Mazoyer et al. 2002). Prominent sulcal and gyral regions are denoted with bubbles. Literature associated with each region is listed. More general anatomical labels are associated with one or more gyri: midventrolateral prefrontal cortex (VLPFC) = inferior frontal gyrus (IFG), pars triangularis and IFG, pars opercularis; dorsolateral PFC (DLPFC) = middle frontal gyrus (MFG); premotor cortex = precentral gyrus (preCG); posterior parietal cortex (PPC) = superior parietal lobule (SPL) and inferior parietal lobule (IPL); temporalparietal junction (TPJ) = supramarginal gyrus (SMG). Other abbreviations: inferior frontal sulcus (IFS); inferior frontal junction (IFJ); superior frontal sulcus (SFS); intraparietal sulcus (IPS).

Figure 2.

ALE map of all experiments combined. The sample included 36 experiments with 461 activation foci. Results are threshold at P < 0.05, corrected for multiple comparisons using false discovery rate and a 25 voxel extent criterion. Higher ALE values are depicted in yellow.

Figure 3.

ALE maps by content. Top: ALE map of all experiments using verbal content (letters, words, digits). Middle: ALE map of all experiments using spatial content (locations, movement vectors). Bottom: ALE map of all experiments using object content (faces, scenes, houses, drawings, colors, unnamable objects). Results are threshold at P < 0.05, corrected for multiple comparisons using false discovery rate and a 25 voxel extent criterion. Higher ALE values are depicted in yellow.

Figure 4.

ALE maps by function. Distractor resistance involves preventing irrelevant external content from disrupting WM. Intrusion resistance involves preventing irrelevant memories from disrupting WM. Shifting involves changing the focus of attention within WM. Updating involves changing the content of what is stored in WM. See Materials and Methods for further details. Results are threshold at P < 0.05, corrected for multiple comparisons using false discovery rate and a 25 voxel extent criterion. Higher ALE values are depicted in yellow.

Figure 5.

Content sensitivity and functional generality of the left IFG, pars triangularis, and right caudal SFS. Top: Proportion of experiments reporting significant activation in the left IFG, pars triangularis (L_IFGTria), and right caudal SFS (R_cSFS) grouped by content (left) and function (right). Significant difference by content were found in both the left IFG, pars triangularis (χ² = 6.42, P < 0.05) and right caudal SFS (χ² = 6.25, P < 0.05). Follow-up logistic regression tests revealed that verbal content predicted activation in the left IFG, pars triangularis (t₃₄ = 2.25, P < 0.05) while spatial content predicted activation in the right caudal SFS (t₃₄ = 2.10, P < 0.05). By contrast, neither region was sensitive to differences by function (both P > 0.1). Bottom: Renderings by content (left) and function (right). Results are thresholded at P < 0.01 uncorrected for depiction of overlap and subthreshold convergence. Content key: red—verbal, green—object, blue—spatial, overlap—mix. Function key: red—distractor resistance, sienna—intrusion resistance, green—shifting, blue—updating, overlap—mix.

Figure 6.

Plots of individual activation foci by selection demands. Activation foci from experiments requiring selection amidst competition (red; high selection) and selection without competition (green: low selection). Prominent clustering from experiments involving high selection can be seen in the left midlateral PFC along the IFS as well as in dorsal posterior parietal regions. Experiments involving low selection cluster prominently around inferior parietal cortex.