Spinal automaticity of movement control and its role in recovering function after spinal injury

Figures & data

Figure 1. (a) A conceptual illustration of the primary anatomical, metabolic, and physiological properties of different types of motor units. The neural component of the motor unit consists of dendrites that make up as much as 90% of its surface area. All muscle fibers innervated by a single motor neuron are referred to as a ‘muscle unit.’ The different colors among the muscle fibers of a unit represent the unique biochemical profiles of the muscle fibers within a muscle unit. However, all of the fibers within a unit are generally homogeneous, having similar metabolic and physiological properties that will vary from fiber-to-fiber within a muscle unit, only about 5%. Motor unit phenotypes are typically designated as Fast Fatigue (FF), Fast Fatigue Resistant (FR), and Slow (S) units, reflecting properties of the motor neuron and its specific muscle unit. Muscle units are commonly designated as Fast Glycolytic (FG), Fast Oxidative Glycolytic (FOG), and Slow Oxidative (SO) [6 from modifications figure 8A,p 53]. The two fibers stained brown (ATPase activated) and tan (ATPase activity after being inhibited with a specific acid pH) signifies the fast myosin phenotype of which signifies the speed of contraction. (b) The relationship between the total cross-sectional area of all muscle fibers within a single unit relative to the total tetanic tension that can be generated by that motor unit. Note that the slow units (crosses) generate a smaller tetanic tension per total cross-sectional area of all fibers within each unit [7]; (c) The relationship between the tetanic force generated by single motor units and the cumulative force that would be generated from motor units assuming recruitment of the units with a nonlinear increase in tetanic forces among the population of motor units within the cat medial gastrocnemius [8]. When a motor pool is engaged in any movement, the rank order of recruitment for each motor pool will proceed from the smallest (fewest number of muscle fibers) to the largest motor unit i.e.highest number of muscle fibers within that motor pool.

Figure 2. (a) Drawing of the cervical spinal cord of a cat by Santiago Ramon y Cajal [10]. This classic anatomical sketch of the input projecting from the dorsal segment of the gray matter, passing through a cluster of interneurons, demonstrates a challenging perspective as to how these interneurons within this cluster defines which excitatory and inhibitory signals functionally project to either, generally the more medial flexor or, laterally located extensor motor pools in the most ventral part of the gray matter. (b) Cartoon sketch to illustrate the hypothesis that different combinations of interneurons are activated by a specific combination of proprioceptors (green curve). Such sensory ensembles involving unique combinations of interneurons mediate a unique pattern of activation of motor pools. The pattern of motor pool activation controls the next phase of the motor output, ultimately defining the next specific phase of a planned movement. The translation of sensory signals occurs in real-time. However, the motor outcome is ‘planned’ in a feedforward manner by interneurons that contribute to central pattern generation for repetitive tasks such as locomotion.

Figure 3. Feedforward regulation of maintaining balance during stepping in decerebrated cats facilitated by epidural spinal cord stimulation. (a) The cat is secured in a stereotaxic frame. An accelerometer is placed on the pelvis to record displacements, and force sensors are placed beneath each belt to record ground reaction forces (GRF) from the right and left hind limbs. (b) Right and left GRF. (c) Correlation between left and right total GRF during stepping for 10 experiments in 7 decerebrated cats (overall r = 0.98). (d) There is no correlation when the order of the left-right lateral displacements was randomized. (e) Cumulative right and left limb displacements are plotted in order of occurrence (gray line) or randomized (red line) [18]. Note that the red line (accumulation of rendomized GRFs’) diverts from the level necessary to maintain the equilibrium of the hindquarters after about 5 steps. (Modified from [18]).

Figure 4. (a) Stick diagram decomposition of a step cycle, joint angular displacement, and EMG activity of selected hindlimb muscles during testing in a representative, Uninjured, Spinally injured nontrained and step Trained spinal rat with epidural spinal cord stimulation (40 Hz at L2) and Quipazine (0.3 mg/kg). Modified from [35]. (b) The spatial distribution of the relative density of activated neurons in a cross-section of the lumbosacral spinal cord. Note the markedly greater density of active cells in the most dorsal lamina compared with the medial or ventral lamina, demonstrating the continuous input of sensory information from a TRAP mouse while resting. (c) Targeted recombination in active populations (TRAP) of mice allowed the capture of two different c-fos activation patterns in the same animal. The percentage of activated neurons that were co-labeled (c-fos+ and Td Tomato+) after performing two 30-minute bouts of stepping were quantified. About 7000 steps were taken in each bout. These data are consistent with a probabilistic-like phenomenon that can recruit many combinations of neural populations (synapses) when repetitively generating many step cycles. Only about 20% of the neurons activated from the first bout of stepping were also activated by the second bout (adapted from [37].

Figure 5. (a) Ankle trajectory of a rat robotic arm during stepping in the assist as needed (AAN) paradigm. The designed trajectory is indicated in blue and the window within which stepping occurs is in red. The black trace represents an example of the pattern of the trajectory and the corrective forces applied by the robotic arm to maintain the ankle within a trajectory of a selected width, (b) Representative EMG from the ankle flexor (green) and extensor (red) during stepping under the influence of a fixed trajectory versus an AAN trajectory. (c) Average EMG of a normalized step cycle shows higher levels of co-contraction during stepping between antagonistic muscles in the fixed versus AAN mode. Modified from [43].

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