Executive semantic processing is underpinned by a large-scale neural network: revealing the contribution of left prefrontal, posterior temporal, and parietal cortex to controlled retrieval and selection using TMS

Abstract

To understand the meanings of words and objects, we need to have knowledge about these items themselves plus executive mechanisms that compute and manipulate semantic information in a task-appropriate way. The neural basis for semantic control remains controversial. Neuroimaging studies have focused on the role of the left inferior frontal gyrus (LIFG), whereas neuropsychological research suggests that damage to a widely distributed network elicits impairments of semantic control. There is also debate about the relationship between semantic and executive control more widely. We used TMS in healthy human volunteers to create "virtual lesions" in structures typically damaged in patients with semantic control deficits: LIFG, left posterior middle temporal gyrus (pMTG), and intraparietal sulcus (IPS). The influence of TMS on tasks varying in semantic and nonsemantic control demands was examined for each region within this hypothesized network to gain insights into (i) their functional specialization (i.e., involvement in semantic representation, controlled retrieval, or selection) and (ii) their domain dependence (i.e., semantic or cognitive control). The results revealed that LIFG and pMTG jointly support both the controlled retrieval and selection of semantic knowledge. IPS specifically participates in semantic selection and responds to manipulations of nonsemantic control demands. These observations are consistent with a large-scale semantic control network, as predicted by lesion data, that draws on semantic-specific (LIFG and pMTG) and domain-independent executive components (IPS).

Figure 1

Example trials for the semantic tasks and the Navon tasks. Participants had to select the target word that was either strongly related to the cue shown above (high relatedness), weakly related (low relatedness), or unrelated but similar to the cue in one of the following semantic dimensions: color, shape, size, or texture (feature selection). In the Navon tasks, participants had to choose the target compound letter that resembled the cue letter either in its global shape (global Navon) or in its local, smaller elements (local Navon). Target items are underlined, and compound letters are enlarged for illustration purposes.

Figure 2

Stimulation sites. rTMS was delivered to the pars triangularis of LIFG, pMTG, and IPS. Images on the right include probability maps, which were available for target regions in BA 44 and BA 45 and the superior (SPL) and inferior parietal lobe (IPL). Stimulation sites are displayed on axial and saggital slices in MNI space, with reference to y and x coordinates, respectively. orange = pars triangularis, yellow = inferior and superior temporal sulcus, purple = Sylvian fissure, blue = IPS.

Figure 3

Reaction times. Performance at baseline (no TMS) and post-TMS following stimulation of LIFG, pMTG, and IPS. High = high relatedness; Low = low relatedness; Feat = feature selection. Error bars denote SEM.

Figure 4

TMS effect. Difference scores between post-TMS and baseline performance (TMS–no TMS) for reaction time. Positive values indicate a decline in performance after brain stimulation, whereas negative values indicate improvement. High = high relatedness; Low = low relatedness; Feat = feature selection. *p < .05. Error bars denote SEM.