Muscle anatomy is reflected in the spatial organization of the spinal motoneuron pools

Abstract

Neural circuits embed limb dynamics for motor control and sensorimotor integration. The somatotopic organization of motoneuron pools in the spinal cord may support these computations. Here, we tested if the spatial organization of motoneurons is related to the musculoskeletal anatomy. We created a 3D model of motoneuron locations within macaque spinal cord and compared the spatial distribution of motoneurons to the anatomical organization of the muscles they innervate. We demonstrated that the spatial distribution of motoneuron pools innervating the upper limb and the anatomical relationships between the muscles they innervate were similar between macaque and human species. Using comparative analysis, we found that the distances between motoneuron pools innervating synergistic muscles were the shortest, followed by those innervating antagonistic muscles. Such spatial organization can support the co-activation of synergistic muscles and reciprocal inhibition of antagonistic muscles. The spatial distribution of motoneurons may play an important role in embedding musculoskeletal dynamics.

Fig. 1. Model of motoneuron pool anatomy in a macaque.

a Circles show averaged locations in the transverse plane of the MNs shown in b, the shaded areas are standard deviations along the dorsoventral and mediolateral directions in the transverse plane calculated across all motoneuron locations in four cervical and two thoracic segments. Gray matter outlines are shown for the caudal portion of the fifth cervical segment (C5C) and the caudal portion of the first thoracic segment (T1C, gray fill). The axis’s origin  is at the central canal. b 3D view of the individual motoneuron locations (colored circles, circle size is not to scale) and gray matter outlines for spinal segments C5 - T2. Central canal locations are shown as open circles. Motoneuron pool colors are the same as in a. The rostrocaudal spacing is not to scale. c The rostrocaudal distributions of the motoneuron locations shown in b. Black circles indicate averages and colored vertical lines indicate standard deviations across the rostrocaudal coordinate (Z) of MNs shown in b.

Fig. 2. Musculoskeletal models.

Screenshots of OpenSim musculoskeletal models of macaque (a) and human (b) upper limbs. Red lines illustrate the origin, insertion, and wrapping geometry of the musculotendinous actuators representing the anatomical arrangement of individual muscles or muscle compartments. For example, two heads of biceps are modeled as two actuators with origin locations on different bones and a common insertion location. All actuators are shown, but not all are labeled for clarity. The bones are shown for illustration purposes only, the inertial geometries of limb segments to which the actuators attach are not shown. The OpenSim logo is added when exporting screenshots from the graphical user interface.

Fig. 3. Comparison of MN locations between the macaque and human spinal cords.

a Gray violin plots show the distribution of MNs from Fig. 1 along the rostrocaudal direction across spinal segments. Colored bars show the rostrocaudal ranges of corresponding MN pools from a human anatomy textbook. b Circles (size no to scale) show MN locations from Fig. 1 in the transverse plane per spinal segment from the macaque model. Gray matter outlines aligned on the central canal at the origin of the axes are from the macaque model. Black open ovals show the distributions of unidentified MN pools adapted from human staining studies summarized and numbered as in ref. .

Fig. 4. Anatomical distances between MN pools and the length correlations between muscles they innervate.

Correlation matrix of the relative distances between the centers of MN pools in all dimensions (a) and only in the transverse plane with rostrocaudal distribution excluded (b) calculated using the model shown in Fig. 1. Distances were calculated between the centers of MN pools for each pair of MN pools relative to the maximum distance across all pairs. Black indicates short distance, white indicates long distance. c Matrix of Pearson correlation coefficients (R) between muscle length changes evaluated across the full range of motion of the macaque forelimb in Fig. 3a only including the muscles whose MN pools were labeled by ref. . Yellow indicates agonistic actions of muscle lengths changing together, i.e., lengthening and shortening together; blue indicates antagonistic actions of reciprocally changing muscle lengths, i.e., lengthening while the other muscle is shortening. Muscles included here are those whose motoneurons are also included in the spinal cord model.

Fig. 5. The anatomical relationships between upper limb muscles of human and macaque.

Matrices of Pearson correlation coefficients (R) between muscle length changes evaluated across the full range of motion of the OpenSim models of the human arm (a) and macaque forelimb (b) shown in Fig. 2. Yellow indicates agonistic actions; blue indicates antagonistic actions as in Fig. 4c. Muscle lengths are used here to compare the functional relationships between the upper extremity muscles of human and macaque musculoskeletal models.

Fig. 6. Comparative analysis of the spatial arrangement of MN pools and the anatomical relationships between muscles they innervate.

a Histogram of 3D distances between MN pools. Vertical solid and dashed lines show the median and interquartile ranges, respectively. b Histogram of 2D distances in the transverse plane between MN pools. Vertical solid and dashed lines show the median and interquartile ranges, respectively. c 3D distances between MN pools vs. Pearson correlation coefficients (R) between lengths of muscles they innervate. Blue and red dots show distanced between MN pools that innervate muscles with positively correlated lengths illustrating extensor and flexor synergies, respectively. Magenta dots show distances between MN pools that innervate muscles with negatively correlated lengths illustrating antagonists. d The same as in c, but for 2D distances. Outliers are shown as open circles.