White matter connections within the central sulcus subserving the somato-cognitive action network

Abstract

The somato-cognitive action network (SCAN) consists of three nodes interspersed within Penfield's motor effector regions. The configuration of the somato-cognitive action network nodes resembles the one of the 'plis de passage' of the central sulcus: small gyri bridging the precentral and postcentral gyri. Thus, we hypothesize that these may provide a structural substrate of the somato-cognitive action network. Using microdissections of 16 human hemispheres, we consistently identified a chain of three distinct plis de passage with increased underlying white matter in locations analogous to the somato-cognitive action network nodes. We mapped localizations of plis de passage into standard stereotactic space to seed functional MRI connectivity across 9000 resting-state functional MRI scans, which demonstrated the connectivity of these sites with the somato-cognitive action network. Intraoperative recordings during direct electrical central sulcus stimulation further identified inter-effector regions corresponding to plis de passage locations. This work provides a critical step towards an improved understanding of the somato-cognitive action network in both structural and functional terms. Furthermore, our work has the potential to guide the development of refined motor cortex stimulation techniques for treating brain disorders and operative resective techniques for complex surgery of the motor cortex.

Keywords: SCAN; motor cortex; plis de passage; somato-cognitive action network; white matter connectivity.

Figure 1

The plis de passage of the central sulcus. (A) Top: Lateral view of the right hemisphere of Specimen 15. The plis de passage were superimposed on the cortex in red. Right: The intra-gyral white matter connections underlying the cortical tissue of the plis de passage, as revealed through the microdissection process. Inset: Enlarged view of the middle pli de passage and a satellite middle pli de passage. Bottom: Inferior view showing the subcentral gyrus within the Sylvian fissure. A satellite inferior plis de passage was superimposed on the cortex in red. (B) Lateral view of the left hemisphere of Specimen 1 showing a striking resemblance to the somato-cognitive action network (SCAN) inter-effector pattern reported by Gordon et al., in Fig. 7b of their study.

Figure 2

Mapping of plis de passage sites and functional connectivity in relation to the somato-cognitive action network. (A) The plis de passage (PDP) sites of the 16 cadaver brains were mapped and manually registered onto the brain surface template (ICBM 2009b NLin Asym), by pointing to the corresponding site on Montreal Neurological Institute surface atlas for each subject. (B) Coordinates were averaged across cadavers to calculate a single average coordinate for each of the three PDPs (top, middle, bottom), which were highly similar to the somato-cognitive action network (SCAN) inter-effector nodes reported by Gordon et al. (C) Functional connectivity (fc) of each region was computed by correlating resting-state functional MRI signals within these regions against the signals of every other brain region, and then averaging these connectivity patterns across the three regions and across all subjects within the UK Biobank (UKB), Adolescent Brain Cognitive Development (ABCD) study and Human Connectome Project (HCP) datasets. (D) Average functional connectivity map of the three PDPs across all subjects in the UKB dataset in cortex (left) and subcortex (right). The resulting map precisely matches the SCAN described by Gordon et al. See Supplementary Fig. 3 for a nearly identical network maps in the HCP and ABCD datasets. BOLD = blood oxygen level-dependent; RSFC = resting state functional connectivity.

Figure 3

Intraoperative direct electrical stimulation sites. All stimulation sites for Patients 1–6 (A–F) are visualized on a 3D reconstruction of the anterior bank of their central sulcus and combined on the International Consortium for Brain Mapping (ICBM) 152 central sulcus template (G). Effector-specific sites are displayed in blue, while inter-effector sites [somato-cognitive action network (SCAN)] are displayed in red. H displays the spatial relationship between the inter-effector sites and the plis de passage (PDP) Montreal Neurological Institute (MNI) coordinates (top) and their probability density estimation (bottom). The three coloured circles in the top image represent the same PDP sites as in Fig. 2. (I) Box plot showing the probability of overlap between stimulation sites [inter-effector (red) versus single-effector (blue)] for the two subsectors (anterior, posterior) of area 4. Mann–Whitney U-test; not significant, ns: P ≥ 0.05.