In a recent study published in the Nature Journal, researchers performed precision functional mapping (PFM) and functional magnetic resonance imaging (fMRI) to map the functional organization of the motor cortex (M1) of the human brain.
Study: A somato-cognitive action network alternates with effector regions in motor cortex. Image Credit: r.classen/Shutterstock.com
Background
The human motor cortex was initially described as a continually present homunculus. Contrastingly, non-human primate (NHP) studies divided M1 into anterior and posterior regions, with the body represented in the anterior and motor effector regions in the posterior.
Voluntary motion is regulated by the cingulo-opercular network (CON). Animal studies have demonstrated the anterior motor cortex projecting into internally placed organs involved in sympathetic awakening, indicating that CON, with M1, may not only mediate abstract actions but also coordinate movements.
About the study
In the present study, researchers presented a dual system that melds action and body control into a common circuit and is characterized by a somato-cognitive action network (SCAN) alternating with M1 effector regions.
The team performed high-resolution (2.40 mm) PFM with resting-state functional connectivity (RSFC) values of 172.0 to 1,813.0 minutes per participant (task: 353.0 minutes per individual) and utilized diffusion information for mapping the functional networks of the brain.
To verify the study findings, data were obtained from three large fMRI studies, i.e., the Adolescent Brain Cognitive Development (ABCD) study, the United Kingdom Biobank (UKB) study, and the Human Connectome Project (HCP) study, and the present study findings were compared.
In total, the datasets comprised data from nearly 50,000 individuals. Further, the findings were placed in inter-species (macaques vs. humans), clinical (postpartum stroke), and developmental (neonatal, infantile, childhood, and adulthood periods) contexts, utilizing precision functional mapping (PFM) information.
The team used a motor and action functional MRI task battery to record concentric-shaped effector somatotopies, which were delineated by the CON-associated inter-effector regions (IERs). The relative timings of resting-state function MRI signals for the M1 regions were compared.
Functional MRI data were obtained from two highly sampled participants (64.0 runs, 244.0 minutes per individual) during the blocked performance of 25 movements and a new event-associated task with distinct phases for planning and execution of hand-foot movements (12.0 runs, 132.0 minutes per individual).
For formal testing of the concentric arrangement, single- and double-peak Gaussian curves were fitted to task activation profiles along the M1 dorsomedial-to-ventrolateral axis.
Task-related functional MRI data were also obtained while individuals repeatedly made 'ee' sounds to isolate laryngeal motion while minimizing tongue and jaw motion and respiration. Motor stimulations were re-analyzed using data from a previous large-scale study by mapping them onto the cortex.
Results
Regions with distinct connectivity, structure, and function interrupt the classic homunculus, alternating with effector-specific (hand, mouth, and foot) areas. The expected neuroimaging pattern comprised three RSFC-defined areas in each brain hemisphere, with connectivity limited to the homotopic contralateral motor cortex and the adjacent primary somatosensory cortex.
The regions corresponded to task-evoked activities during tongue, hand, and foot movements. Three regions with strong ipsilateral and contralateral functional connections were intertwined between the effector-specific areas. This generated an interdigitated chain extending from the primary motor cortex (precentral gyrus) that had not been identified previously.
The motif was detected among all the highly sampled adults and was reproducible at an intra-individual level. The three study datasets verified the interdigitation of action control-linked and motor effector regions.
Additionally, the functionally connected IERs exhibited lower cortical thickness but greater fractional anisotropy and intracortical myelin content than the foot regions.
The IERs showed robust functional connectivity to the CON, which is essential for action and physiological control, sympathetic arousal, pain, and achieving goal-directed cognitive control. Macaque and pediatric precision fMRI indicated cross-species homologs and developmental IER system precursors.
The IERs were detected in an infant aged 11.0 months and were comparable to those observed among children aged nine years. The pattern could be identified even among individuals with severe bilateral postpartum strokes.
Furthermore, the motor and action fMRI task battery showed concentrically arranged effector somatotopies separated by the CON-linked IERs. The IERs were strongly connected with the supplementary motor area (SMA) and the caudally located cingulate zone of the dorsal anterior cingulate cortex (dACC) and were linked to the insula and the anterior aspect of the prefrontal cortex.
In the striatum, IERs showed robust linkage with the dorsolateral putamen. Thalamic IER connectivity was especially observed with the centromedian nucleus and the posteromedial, intermediate, and posteroinferior nuclei on the ventral aspect.
The IERs were also robustly linked to the surrounding cerebellar areas and the fundus of the central sulcus, Brodmann area (BA) 3a, involved in proprioception.
In addition, the IERs were linked to the middle insula, which is involved in processing interoceptive and pain signals; the lateral vermis Crus II; the cerebellar lobules V, VIIb, and VIIIa; and the dorsolateral putamen, which is critical for motor functions.
The findings indicated that high-frequency delta activity might occur earlier in CON than in M1 and that the M1 IERs may partially enable the execution of action plans. The topography of preferred movements, double-peak fitter curves, and dual laryngeal representation supported the distal-proximal concentric organization (except hand movements in the second participant), confirmed by re-analyzing previously published electrophysiological findings.
Finally, the IERs were not motion-specific and were co-activated during action planning (hand and foot coordination) and axial bodily movements (including those of the eyebrows).
Conclusion
The study suggests that a system for whole-body action planning punctures M1, the samato-cognative action network.
In M1, two parallel systems intertwine, forming an integrate-isolate pattern of effector-specific regions critical for fine motor control, linked to the SCAN, critical for integrating goals, bodily movements, and physiology.
SCAN also enables anticipatory breathing, cardiovascular, and postural changes. The dual network integrates the mind and the body, aligned with the sensory systems.
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