Neuromechanical principles underlying movement modularity and their implications for rehabilitation

Abstract

Neuromechanical principles define the properties and problems that shape neural solutions for movement. Although the theoretical and experimental evidence is debated, we present arguments for consistent structures in motor patterns, i.e., motor modules, that are neuromechanical solutions for movement particular to an individual and shaped by evolutionary, developmental, and learning processes. As a consequence, motor modules may be useful in assessing sensorimotor deficits specific to an individual and define targets for the rational development of novel rehabilitation therapies that enhance neural plasticity and sculpt motor recovery. We propose that motor module organization is disrupted and may be improved by therapy in spinal cord injury, stroke, and Parkinson's disease. Recent studies provide insights into the yet-unknown underlying neural mechanisms of motor modules, motor impairment, and motor learning and may lead to better understanding of the causal nature of modularity and its underlying neural substrates.

Copyright © 2015 Elsevier Inc. All rights reserved.

Figures

Figure 1. Neuromechanics and rehabilitation

Movement is influenced by both the neural and biomechanical systems of the body and their interaction with the environment. Experience-dependent plasticity shapes the individual-specific patterns that determine how we move. Novel rehabilitation paradigms seek to restore motor function by enhancing endogenous neural plasticity through a number of mechanisms and to sculpt the plasticity via task-specific training.

Figure 2. Motor modules define functional co-activation of muscles

For walking, descending commands from the spinal cord, brainstem, and cortex can modulate spinal motor modules. Each motor module selectively co-activated multiple muscles with a characteristic level of activation (colored bars) to produce the mechanical output needed to achieve a given locomotor subtask (Clark et al., 2010; Neptune et al., 2009). The particular timing of recruitment (colored lines, top right) can vary across steps, across gait speeds, and environmental demands. The activity of individual muscles express unique temporal patterns of activity (black lines, bottom right) due to their different contributions to different motor modules (colored lines, bottom right).

Figure 3. Different motor modules deficits and improvements in spinal cord injury, stroke, and Parkinson’s disease

Colored bars represent motor modules, with the height of each bar representing the extent to which an individual muscle is part of that motor module. Color of motor modules across conditions and/or population (e.g., able-bodied to pre-SCI) represents similarity between motor modules. A) Spinal cord injury disrupts both descending connectivity and spinal organization. Accordingly, motor modules resembling those found in able-bodied individuals are reduced after incomplete spinal cord injury, and additional motor modules characterized by co-contraction can emerge (not shown) (Hayes et al., 2014a). After rehabilitation, motor modules may be reshaped and better resemble those in able-bodied individuals (Hayes et al., 2012). In animals with complete spinal cord transection, a few motor modules can account for a large degree of variance in muscle activity for reactive balance in response to support surface translations (Chvatal et al., 2013). In the intact condition, the total variance explained by an increasing number of motor modules is significantly different from the variance explained in randomly shuffled data, indicative of consistent structure in muscle activity (red vs. blue lines). However, after complete spinal transection, the variance explained by motor modules does not differ in from that obtained by randomly shuffling data, suggesting that no consistent structure exists (red vs. black lines). B) Stroke disrupts corticospinal drive, and impairs independent recruitment of joint actions. Motor modules for walking in the paretic leg are merged versions of those found in able-bodied individuals. Merging can occur between different modules that are associated with different motor deficits (Clark et al., 2010). After rehabilitation, splitting of motor modules is hypothesized to occur that would be associated with improved performance. C) Parkinson’s disease impairs basal ganglia function and is associated with inappropriate selection of motor patterns as well as cortical hyperexcitability. Accordingly, in individuals with PD, the number of motor modules in walking and reactive balance are similar to those found in healthy individuals (Rodriguez et al., 2013; Roemmich et al., 2014). However, in young, healthy adults, motor modules for reactive balance to support surface translation and overground walking are similar, suggesting a common subcortical origin for the recruited motor modules. In contrast, in individuals with PD that have balance impairments, motor modules from reactive balance and walking can appear to be completely distinct, consistent with increased attention and cortical control of gait. After rehabilitation, motor modules may become more similar across tasks, suggesting improved automatic, subcortical control of gait (Allen et al., 2014).