Neurosurgical Research: Anatomical and Functional Study of Connections between the Paracentral Lobule and Primary Motor Cortex

In recent years, researchers have been continuously exploring the connections between different regions of the human brain, particularly those involving motor function and its plasticity. It is known that the paracentral lobule (PCL) and the primary motor cortex (M1) play important roles in motor output and are closely related. This study aims to gain a deeper understanding of the anatomical and functional connections between the paracentral lobule and the primary motor cortex, as well as their relevance to motor function.

Research Objectives and Background

This research was conducted jointly by Yusuke Kimura, Shoto Yamada, Katsuya Komatsu, Rei Enatsu, and others at Sapporo Medical University, Kita Hiroshima Medical Center, Sunagawa City Medical Center, and Hokkaido Children’s Health and Rehabilitation Medical Center. The study was published in the Journal of Neurosurgery. The main objective of the research was to elucidate the anatomical and functional connections between the paracentral lobule (including the supplementary motor area, SMA) and the primary motor cortex (M1).

The paracentral lobule contains the supplementary motor area, which plays an important role not only in motor preparation and motor intention but also exhibits a significant role related to motor function plasticity. Early studies led by Penfield, through electrical stimulation, discovered M1 and SMA, concluding that the supplementary motor area is a motor-related region. However, recent research has shown that increased activity in the paracentral lobule is closely related to motor impairment, suggesting its potential as a target area for rehabilitation.

Research Methods

Study Design and Patient Selection

This was a non-randomized retrospective study. Patients who underwent surgery at Sapporo Medical University Hospital between April 2019 and July 2023 were screened. Ultimately, 16 patients (10 males, 6 females, age range 11-76 years) with lesions near the central sulcus and requiring a transcallosal approach were included. Informed consent was obtained from all patients and their families.

MRI and fMRI Data Acquisition and Processing

Data were acquired using a Signa HDxt 3.0-T MRI scanner. Diffusion tensor imaging (DTI) conditions included: 18 gradient directions, field of view 220 mm, matrix 128×128, slice thickness 2.4 mm, maximum b-value 1000 sec/mm2. Functional MRI (fMRI) conditions: TR 3000 msec, TE 30 msec, matrix 64×64, slice thickness 3.0 mm, voxel size 3×3×3 mm. Patients performed a finger-tapping task during imaging.

DTI images and fMRI activation maps were overlaid onto structural MR images, and further processing was performed using the iPlan Cranial software from Brainlab, defining regions of interest (ROIs).

Electrode Placement and CCEP Measurement

During surgery, platinum grid electrodes were placed on the precentral gyrus (PCG) and paracentral lobule (PCL), with the aid of a neuronavigation system to accurately position the electrodes within the predefined ROIs. Cortico-cortical evoked potentials (CCEPs) were measured using a 32-channel MeE 1232 neuromaster system. During the measurement, CCEPs were recorded upon bipolar electrical stimulation.

Electrophysiological Measurement and Data Analysis

Patients’ pre- and post-operative motor functions of the upper limbs and hands were evaluated using the Manual Muscle Test (MMT). CCEP amplitudes and latencies were compared among different patient groups (dominant/non-dominant hemisphere, male/female, paralyzed/non-paralyzed). Additionally, the correlation between CCEP amplitudes, latencies, and DTI-derived fiber counts, average lengths, and fractional anisotropy (FA) values were measured.

Research Results

Imaging Results

DTI visualized the fiber connections between the paracentral lobule and the primary motor cortex in 14 patients, with an average FA value of 0.335, an average fiber count of 14, and an average fiber length of 66 mm.

CCEP Measurement Results

Unidirectional CCEP responses were obtained in all 16 patients, with 14 patients exhibiting bidirectional CCEP responses. No complications related to electrode placement or electrical stimulation were reported. There was no significant difference in CCEP amplitudes between the M1-to-PCL and PCL-to-M1 directions. Post-operative motor function assessment revealed 3 patients with motor impairments, 2 of whom showed improvement during the clinical course.

Statistical Analysis

Spearman correlation tests did not reveal a significant correlation between CCEP amplitudes and average FA values. CCEP latencies in both directions (from M1 to PCL and from PCL to M1) also did not show a significant correlation with fiber length. Furthermore, CCEP parameters did not differ significantly between the dominant and non-dominant hemispheres.

Discussion

This study was the first to combine DTI and bidirectional CCEP measurements to investigate the anatomical and functional connections between the paracentral lobule/supplementary motor area and the primary motor cortex. The results indicate the existence of bidirectional electrophysiological connections between these brain regions, with individual differences observed among patients. These differences may suggest variability in motor function plasticity during the rehabilitation process across individuals.

An important finding of this study is the role of SMA in motor intention and preparation, further supported by the temporary paralysis observed in some patients post-operatively, highlighting the crucial role of SMA in motor preparation.

Although this study has certain limitations, such as a small sample size, selection bias, and constraints in electrode placement positions, it provides an important foundation for future research on motor function plasticity.

Conclusion

The research results reveal the existence of anatomical and functional bidirectional connections between the paracentral lobule, including the supplementary motor area, and the primary motor cortex (M1). These findings not only provide new insights into further exploring the complexity of the motor function network but also lay the groundwork for developing targeted rehabilitation strategies in clinical settings. Future research should expand the sample size and integrate other imaging and electrophysiological techniques to gain a deeper understanding of the brain network connections underlying motor function.

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Explanations of relevant technical terms: - CCEP (cortico-cortical evoked potential): A measure of functional connectivity between brain regions. - DTI (diffusion tensor imaging): An imaging technique that analyzes the diffusion of water molecules in brain white matter. - FA (fractional anisotropy): A measure of the directionality of water molecule diffusion.