Shared neural processes support semantic control and action understanding

Abstract

Executive-semantic control and action understanding appear to recruit overlapping brain regions but existing evidence from neuroimaging meta-analyses and neuropsychology lacks spatial precision; we therefore manipulated difficulty and feature type (visual vs. action) in a single fMRI study. Harder judgements recruited an executive-semantic network encompassing medial and inferior frontal regions (including LIFG) and posterior temporal cortex (including pMTG). These regions partially overlapped with brain areas involved in action but not visual judgements. In LIFG, the peak responses to action and difficulty were spatially identical across participants, while these responses were overlapping yet spatially distinct in posterior temporal cortex. We propose that the co-activation of LIFG and pMTG allows the flexible retrieval of semantic information, appropriate to the current context; this might be necessary both for semantic control and understanding actions. Feature selection in difficult trials also recruited ventral occipital-temporal areas, not implicated in action understanding.

Keywords: Action; Control; Executive; Semantic; fMRI.

Fig. 1

An example of the trial format. Here, “axe” is the probe, and the target is “fishing rod” (both involve a chopping action). Given that axe and fishing rod are not globally related, this is a trial from the difficult, high control action feature condition.

Fig. 2

Activation maps for action > visual (yellow) and visual > action (red), presented on the MNI-152 standard brain with cluster correction applied (voxel inclusion threshold z = 2.3, cluster significance threshold p < .05). Image is presented using radiological convention (left hemisphere on the right-hand side).

Fig. 3

Activation maps for high difficulty > low difficulty (blue/light blue) and action > visual (yellow), with the overlap in green. White circles have been placed around the overlap foci; [1] LIFG, [2] pMTG and [3] anterior cingulate. Data is presented on MNI-152 standard brain with cluster correction applied (voxel inclusion threshold z = 2.3, cluster significance threshold p < .05). Image is presented using radiological convention (left hemisphere on the right-hand side).

Fig. 4

8 mm ROI spheres placed around peaks from a ALE meta-analysis examining executive–semantic demands (Noonan et al., 2013). To allow the location of the ROIs to be compared with the independent whole-brain contrast for hard > easy trials (in blue), they are displayed together on a glass brain using DV3D, with depth information characterised by transparency (Gouws, Woods, Millman, Morland, & Green, 2009). Graphs show the mean percentage signal change for each condition at each ROI; error bars represent the standard error of the mean. All significant effects are noted on each graph. The left hemisphere is shown on the left side of the image. ROI coordinates are given in MNI space.

Fig. 5

8 mm ROI spheres placed around peaks from the literature implicated in action knowledge (from Liljeström et al., 2008, Watson et al., 2013), and visual semantics from Thompson-Schill, Aguirre, D’Esposito, and Farah (1999). Activation from the whole-brain contrast for action > visual trials is projected onto a glass brain in yellow, while the visual > action response is shown in red, using DV3D, with depth information characterised by transparency (Gouws et al., 2009). Graphs display the mean percentage signal change for each condition at each ROI; error bars represent the standard error of the mean. All significant effects are noted on each graph. ROI coordinates are given in MNI space.