Effects of remote movement and strength training on motor output: basic studies and application after stroke

Date

2013-01-02

Authors

Dragert, Katherine L.

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Abstract

Similar to quadrupedal animals, there is evidence in humans of interlimb signalling during upper and lower limb muscular activation. A product of these interconnections is modulation of motor output via remote neural input. Such remote communication can take several forms; for example, movement modifies activity between upper and lower limbs (e.g. arms to legs) and between a limb pair (e.g. one leg to the other). A specific form of modulation between homologous muscles bilaterally (i.e. the corresponding motor unit pool across the spinal cord) is also seen with strength training. However, details of these motor connections are not well known. Improved understanding of remote influences on motor output and coordination patterns may be valuable in an applied motor re-training setting. Abnormal excitability within reflex pathways of lower limb musculature is common among various neurological disorders. Thus, it is of interest whether remote inputs could be exploited to help normalize dysfunctional motor output. The primary goal of this thesis was to better our understanding of neural interlimb connections; specifically, to examine modulatory responses within the ankle flexor and extensor muscles induced by remote muscular activation associated with both rhythmic arm movement and contralateral resistance training. Further, the final objective of this work was to apply these earlier observations in the context of a post-stroke rehabilitation paradigm, aimed at normalizing muscle activation patterns within the more-affected limb. Initially, this thesis examined spinal reflex excitability within functional antagonists of the lower leg, the ankle flexors and extensor muscles, and the impact of transient, rhythmic movement on these neural networks. Hoffmann (H-) reflexes were first used as a measurement probe. Rhythmic arm cycling significantly suppressed reflex amplitude in extensors, but revealed a bidirectional (i.e. either suppression or facilitation) reflex modulation in flexor muscles. Thus, differential regulation of ankle flexor and extensor H-reflex amplitudes was evidenced during rhythmic arm movement. This may stem from differences in locomotor pattern generator output to these groups as well as increased involvement of cortical drive to the flexors relative to the extensors during rhythmic movement. These results support the presence of interlimb neural coupling, such that remote motor action (arm movement) influences lumbar spinal cord excitability. Additionally, these descending signals impact ankle flexors and extensors differentially, which illustrates a method of producing facilitative modulation of ankle flexor motor responses. Second, reciprocal inhibition (RI) was used to examine regulation of excitability between these same lower limb functional antagonists during rhythmic arm movement. Arm cycling significantly increased RI in ankle extensors, but had no effect in the flexors. This extends observation of remote motor activity-induced modulation on spinal excitability to the core circuitry that comprises the interaction between functional agonist/antagonist pairs. Moreover, the asymmetry of this effect highlights differences in descending supraspinal inputs to ankle flexors vs. extensors, and may be related to functional dorsiflexion requirements during locomotion. Subsequently, this thesis explored long term plasticity of interlimb neural modulation resulting from remote motor activation in the form of resistance training. Specifically, the within limb pair ‘cross-education’ phenomenon was investigated via unilateral isometric strength training of the ankle flexors. The first of these training interventions was implemented in a cohort of neurologically intact subjects who performed five weeks of one-sided maximal isometric dorsiflexion training. H-reflex recruitment curves were used to probe for training-induced spinal plasticity within the agonist (flexor) and antagonist (extensor) muscles bilaterally. Post-intervention, dorsiflexor torque significantly increased in the trained and untrained limbs. Further, significant changes in H-reflex excitability were detected in the trained flexor (agonist) muscle and in both extensor (antagonist) muscles. These findings reveal that muscular crossed effects can be obtained in the ankle dorsiflexor muscles, and provide novel information on agonist and antagonist spinal adaptations that accompany unilateral training. They also suggest potential for application of remote motor activation (resistance training) to induce interlimb neural plasticity within a clinical context, such as improving one-sided weakness and/or motor dysfunction following neurotrauma. The final training intervention was implemented in a chronic (>6mo post-infarct) stroke clinical group who completed six weeks of maximal isometric dorsiflexion training in the less-affected leg. Voluntary isometric strength (dorsiflexion torque, muscle activation), reciprocal inhibition (RI), walking ability and clinical function were used to quantify training effects. Post-intervention, dorsiflexion torque and maximal flexor muscle activation significantly increased in both the more-affected (untrained) and less-affected (trained) legs. Further, the relation between size of RI and level of muscle activation in the more-affected flexor muscle was significantly altered by training, and the Timed Up and Go clinical test was significantly improved. Thus, significant gains in voluntary strength, muscle activation and spinal excitability on the untrained, more-affected side after stroke can be invoked through training the opposite limb. This translates into small but observable functional improvements. Taken together, the data in this thesis provide a basis for novel motor re-training approaches. Improved understanding has been gained of the similarities and differences between remote motor influences received by ankle flexor and extensor muscles in the lower leg. These observations culminate in the implementation of a novel post-stroke training paradigm, which shows that remote muscle activation, i.e. the cross-education effect, can induce strength and functional gains in the more-affected limb.

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Keywords

Motor control, Stroke, Reflex, Interlimb, Cross education, Rehabilitation

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