Abnormal synergies and associated reactions post-hemiparetic stroke reflect muscle activation patterns of brainstem motor pathways

Abstract

Individuals with moderate-to-severe post-stroke hemiparesis cannot control proximal and distal joints of the arm independently because they are constrained to stereotypical movement patterns called flexion and extension synergies. Accumulating evidence indicates that these synergies emerge because of upregulation of diffusely projecting brainstem motor pathways following stroke-induced damage to corticofugal pathways. During our recent work on differences in synergy expression among proximal and distal joints, we serendipitously observed some notable characteristics of synergy-driven muscle activation. It seemed that: paretic wrist/finger muscles were activated maximally during contractions of muscles at a different joint; differences in the magnitude of synergy expression occurred when elicited via contraction of proximal vs. distal muscles; and associated reactions in the paretic limb occurred during maximal efforts with the non-paretic limb, the strength of which seemed to vary depending on which muscles in the non-paretic limb were contracting. Here we formally investigated these observations and interpreted them within the context of the neural mechanisms thought to underlie stereotypical movement patterns. If upregulation of brainstem motor pathways occurs following stroke-induced corticofugal tract damage, then we would expect a pattern of muscle dependency in the observed behaviors consistent with such neural reorganization. Twelve participants with moderate-to-severe hemiparetic stroke and six without stroke performed maximal isometric torque generation in eight directions: shoulder abduction/adduction and elbow, wrist, and finger flexion/extension. Isometric joint torques and surface EMG were recorded from shoulder, elbow, wrist, and finger joints and muscles. For some participants, joint torque and muscle activation generated during maximal voluntary contractions were lower than during maximal synergy-induced contractions (i.e., contractions about a different joint), particularly for wrist and fingers. Synergy-driven contractions were strongest when elicited via proximal joints and weakest when elicited via distal joints. Associated reactions in the wrist/finger flexors were stronger than those of other paretic muscles and were the only ones whose response depended on whether the non-paretic contraction was at a proximal or distal joint. Results provide indirect evidence linking the influence of brainstem motor pathways to abnormal motor behaviors post-stroke, and they demonstrate the need to examine whole-limb behavior when studying or seeking to rehabilitate the paretic upper limb.

Intrinsic properties of spinal motoneurons degrade ankle torque control in humans

“…These hyperexcitable motoneurons are much more sensitive to afferent inputs which may lead to spasticity and even hypertonicity, where individuals are unable to derecruit and cease discharge of motoneurons. Furthermore, more excitable motoneurons also amplify the commands of weak and indirect motor pathways (e.g., reticulospinal) which is theorized to generate a loss of independent joint control (Dewald et al, 1995, Ellis et al, 2016, Li et al, 2019, McPherson et al, 2018a, McPherson et al, 2018c, McPherson and Dewald, 2022).…”

“…Furthermore, more excitable motoneurons also amplify the commands of weak and indirect motor pathways (e.g., reticulospinal) which is theorized to generate a loss of independent joint control (Dewald et al, 1995, Ellis et al, 2016, Li et al, 2019, McPherson et al, 2018a, McPherson et al, 2018c, McPherson and Dewald, 2022.…”

Corticospinal and corticoreticulospinal projections benefit motor behaviors in chronic stroke

“…We also found that muscle individuation was poorer during FDI task performance than BIC performance; in other words, non-instructed muscles throughout the UE showed greater activity during controlled movement at the index finger than elbow. These results differ from other chronic stroke studies that found worse individuation with proximal movement (Zackowski et al ., 2004; McPherson & Dewald, 2022) or no segmental difference (Lang & Beebe, 2007). This disagreement may reflect differences in how non-instructed muscle activity was elicited.…”

“…Of the chronic stroke studies that compared motor behaviors between segments, most used subjective clinical scales or unmatched testing paradigms. This has led to conflicting results, with some investigators finding differences in particular segmental behaviors (Lang et al, 2006;Cho et al, 2012) (Zackowski et al, 2004;McPherson & Dewald, 2022) and others finding none (Mercier & Bourbonnais, 2004;Lang et al, 2006;Lang & Beebe, 2007). Collectively, these observations call into question whether segmental behavioral differences exist in the chronic phase or are an artifact of the testing instruments.…”

Motor unit firing rate modulation is more impaired during flexion synergy-driven contractions of the biceps brachii in chronic stroke

“…Synergy-driven elbow flexion is thought to arise from a greater reliance on the reticulospinal tracts (RST) post stroke, and their relatively diffuse projections to multiple motor pools (Dewald et al ., 1995; Owen et al ., 2017; Karbasforoushan et al ., 2019; McPherson & Dewald, 2022). In short, due to the diffuse projections of the RST, excitatory drive intended for motoneurons of the shoulder abductors produces an involuntary activation of elbow flexor motoneurons.…”