effector regions alternate with the somato-cognitive action network

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 the motor cortex. Image Credit: r.classen/Shutterstock.com

Background

The human motor cortex was initially described as a continuously present homunculus. In contrast, non-human primate (NHP) studies have divided M1 into anterior and posterior regions, with the body represented in the anterior and motor effector regions in the posterior.

Voluntary movement is regulated by the cinguloopercular network (CON). Animal studies have demonstrated that the anterior motor cortex projects into internal organs involved in sympathetic arousal, indicating that CON, along with M1, can not only mediate abstract actions, but also coordinate movements.

About the study

In the present study, the researchers presented a dual system that merges body action and 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 ​​from 172.0 to 1,813.0 minutes per participant (task: 353.0 minutes per individual) and used diffusion information to map the functional networks of the brain.

To verify the study results, data were obtained from three large fMRI studies, namely the Adolescent Brain Cognitive Development (ABCD) study, the United Kingdom Biobank (UKB) study and the Human Connectome Project (HCP), and the present study the results were compared.

In total, the datasets included data from almost 50,000 people. In addition, findings were placed in cross-species (macaques versus humans), clinical (postpartum stroke), and developmental (neonatal, infant, childhood, and adulthood periods) contexts, using precision functional mapping (PFM) information.

The team used a battery of motor and action functional MRI tasks to record concentrically shaped effector somatotopies, delineated by inter-effector regions (IERs) associated with CONs. The relative timings of resting-state function MRI signals for M1 regions were compared.

Functional MRI data were obtained from two heavily sampled participants (64.0 runs, 244.0 minutes per individual) during gated execution of 25 movements and a novel event-associated task with phases. separate for planning and executing hand-foot movements (12.0 strokes, 132.0 minutes per person).

For formal tests of the concentric arrangement, single and double peak Gaussian curves were fitted to task activation profiles along the dorsomedial to ventrolateral M1 axis.

Task-related functional MRI data was also obtained while individuals repeatedly uttered “ee” sounds to isolate laryngeal movement while minimizing tongue and jaw movement and breathing. Motor stimuli were reanalyzed using data from a previous large-scale study by mapping them to the cortex.

Results

Regions with distinct connectivity, structure, and function interrupt the classic homunculus, alternating with effector-specific areas (hand, mouth, and foot). The expected neuroimaging pattern included three RSFC-defined areas in each cerebral hemisphere, with connectivity limited to the contralateral homotopic motor cortex and 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 effector-specific areas. This generated an interdigital chain extending from the primary motor cortex (precentral gyrus) that had not previously been identified.

The pattern was detected in all heavily sampled adults and was reproducible at the intra-individual level. All three datasets in the study verified the interdigitation of action control-related and motor effector regions.

Moreover, functionally connected IERs exhibited lower cortical thickness but higher fractional anisotropy and intracortical myelin content than foot regions.

IERs showed robust functional connectivity to the CON, which is essential for physiological action and control, sympathetic arousal, pain, and achieving goal-directed cognitive control. Macaque and pediatric precision fMRI indicated cross-species homologs and precursors of the developmental IER system.

IERs were detected in an 11.0-month-old infant and were comparable to those seen in nine-year-old children. The pattern could be identified even in people with severe bilateral postpartum stroke.

Moreover, the motor and action fMRI task battery showed concentrically arranged effector somatotopias separated by CON-related IERs. IERs were strongly linked to the supplementary motor area (SMA) and the caudal cingulate area of ​​the dorsal anterior cingulate cortex (dACC) and were linked to the insula and the anterior surface of the prefrontal cortex.

In the striatum, IERs showed robust binding to the dorsolateral putamen. The connectivity of the thalamic IER was particularly observed with the centromedial nucleus and the posteromedial, intermediate and posteroinferior nuclei on the ventral side.

The IERs were also tightly bound to surrounding cerebellar areas and to the fundus of the central sulcus, Brodmann’s area (BA) 3a, involved in proprioception.

Additionally, IERs were linked to the middle insula, which is involved in the processing of interoceptive signals and pain; the Crus II lateral vermis; cerebellar lobules V, VIIb and VIIIa; and the dorsolateral putamen, which is essential for motor functions.

The results indicated that high-frequency delta activity might occur earlier in CON than in M1 and that M1 IERs might partially enable the execution of action plans. Preferred movement topography, double-peaked fit curves, and double laryngeal representation supported the distal-proximal concentric organization (except for hand movements in the second participant), confirmed by reanalysis of the previously published electrophysiological results.

Finally, IERs were not movement-specific and were co-activated during action planning (coordination of hands and feet) and axial body movements (including those of the eyebrows).

Conclusion

The study suggests that a whole-body action planning system breaks through M1, the samato-cognitive action network.

In M1, two parallel systems intertwine, forming an integrated-isolated pattern of effector-specific regions critical for fine motor control, linked to SCAN, critical for the integration of goals, body movements and physiology.

The SCAN also makes it possible to anticipate respiratory, cardiovascular and postural changes. The dual network integrates mind and body, aligned with the sensory systems.