Neuromechanical interactions between the limbs during human locomotion: an evolutionary perspective with translation to rehabilitation.

During bipedal locomotor activities, humans use elements of quadrupedal neuronal limb control. Evolutionary constraints can help inform the historical ancestry for preservation of these core control elements support transfer of the huge body of quadrupedal non-human animal literature to human rehabilitation. In particular, this has translational applications for neurological rehabilitation after neurotrauma where interlimb coordination is lost or compromised. The present state of the field supports including arm activity in addition to leg activity as a component of gait retraining after neurotrauma.

High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke.

Hemiparesis after stroke decreases ability to dorsiflex the more-affected ankle during walking. Increased strength would be beneficial, but the more-affected limb is often too weak to be trained. In neurologically intact participants, training one limb induces strength gains in the contralateral, untrained limb. This approach remains unexplored post-stroke. The aim of this study was to test the hypothesis that unilateral dorsiflexor high-intensity resistance training on the less-affected side increases strength and motor output bilaterally following stroke. 19 participants (84.1 ± 77.6 months post-infarct) performed 6 weeks of maximal isometric dorsiflexion training using the less-affected leg. Voluntary isometric strength (dorsiflexion torque, muscle activation), reciprocal inhibition (RI), walking ability (gait speed, kinematics, EMG patterns), and clinical function were measured within 1 week before and 4 days following training. Post-intervention, dorsiflexion torque increased by ~31 % (p < 0.05) in the more-affected (untrained) and by ~34 % (p < 0.05) in the less-affected (trained) legs. Muscle activation significantly increased bilaterally, by ~59 and ~20 % in the trained and untrained legs, respectively. Notably, 4 participants who were unable to generate functional dorsiflexion on the more-affected side before training could do so post-intervention. Significant correlations between muscle activation and size of RI were noted across muscle groups before and after training, and the relation between size of RI and level of muscle activation in the more-affected tibialis anterior muscle was significantly altered by training. Thus, significant gains in voluntary strength and muscle activation on the untrained, more-affected side after stroke can be invoked through training the opposite limb. We demonstrate residual plasticity existing many years post-stroke and suggest clinical application of the cross-education effect where training the more-affected limb is not initially possible.

Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors.

Training a muscle group in one limb yields strength gains bilaterally-the so-called cross-education effect. However, to date there has been little study of the targeted application of this phenomenon in a manner relevant to clinical rehabilitation. For example, it may be applicable post-stroke, where hemiparesis leads to ankle flexor weakness. The purpose of this study was to examine the effects of high-intensity unilateral dorsiflexion resistance training on agonist (tibialis anterior, TA) and antagonist (plantarflexor soleus, SOL) muscular strength and H-reflex excitability in the trained and untrained limbs. Ankle flexor and extensor torque, as well as SOL and TA H-reflexes evoked during low-level contraction, were measured before and after 5 weeks of dorsiflexion training (n = 19). As a result of the intervention, dorsiflexor maximal voluntary isometric contraction force (MVIC) significantly increased (P < 0.05) in both the trained and untrained limbs by 14.7 and 8.4%, respectively. No changes in plantarflexor MVIC force were observed in either limb. Significant changes in H-reflex excitability threshold were also detected: H(@thresh) significantly increased in the trained TA and SOL; and H(@max) decreased in both SOL 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. It is possible that the ability to strengthen the ankle dorsiflexors bilaterally could be applied in post-stroke rehabilitation, where ankle flexor weakness could be counteracted via dorsiflexor training in the less-affected limb.

Rhythmic arm cycling modulates Hoffmann reflex excitability differentially in the ankle flexor and extensor muscles.

Rhythmic arm movement significantly suppresses H-reflex amplitude in the soleus (SOL) muscle. This is evidence of neural linkages between the arms and legs which can be exploited during locomotion and have been ascribed to the descending effects of CPGs for arm cycling. However, the generalizability of the effects of arm movement on reflex excitability within the lower leg musculature has not been confirmed, as findings have been limited solely to the ankle extensor group. Here we tested the hypothesis that rhythmic arm movement similarly modulates H-reflex amplitude in both the ankle flexors and extensors by observing responses in the SOL and tibialis anterior (TA) muscles. SOL and TA H-reflex recruitment curves were recorded bilaterally during control and 1Hz arm cycling conditions. Our results showed significant suppression in H-reflex amplitude (H(max)) in the SOL muscle in both the dominant and non-dominant legs during arm movement. However, results also revealed an unpredicted bidirectional (i.e. either suppression or facilitation) modulation of TA reflex amplitude that was not present in the SOL muscle. These findings suggest a differential regulation of ankle flexor and extensor H-reflex responses during rhythmic arm movement. This may be the result of differences in CPG output to the flexors and extensors during rhythmic movement, as well as increased involvement of cortical drive to the flexors relative to the extensors during rhythmic movement. These findings may be pertinent to future investigation of rehabilitative therapies that involve facilitative modulation of ankle flexor motor responses.

Differential modulation of reciprocal inhibition in ankle muscles during rhythmic arm cycling.

Interlimb neural linkages relay activity related to rhythmic arm movement to the lumbar spinal cord. This is detected by modulated reflex amplitudes in muscles remote from the rhythmic movement. Improved understanding of modulation in ankle flexor and extensor muscles due to rhythmic arm movement can be gained using modulation of spinal excitability as a probe. The modulatory effect of rhythmic arm movement on Ia reciprocal inhibition (RI) between functional antagonists at the ankle has not been studied. We investigated the influence of rhythmic arm cycling on short latency (∼55ms post-stimulus) RI between ankle flexor (tibialis anterior, TA) and extensor (soleus, SOL) muscles at varying (0.9, 1.0, 1.2, 1.5 and 2.0× motor threshold (MT)) stimulus intensities. We hypothesized that arm cycling would increase RI between antagonists, but that movement conditioning would vary depending on stimulus intensity used to evoke the RI response. Amplitude of RI deduced from suppression of ongoing EMG activity was compared in static and arm cycling conditions. Arm cycling significantly (p<0.05) increased RI in SOL at 1.0×MT, but had no effect in TA at any stimulus intensity (p>0.05). Descending signals arising from rhythmic arm movement significantly alter transmission in RI pathways between ankle flexor and extensor muscles differentially. This may be due to differences in descending supraspinal inputs to ankle flexors vs. extensors, and could be related to functional requirements during locomotion.

Enhancement of arm and leg locomotor coupling with augmented cutaneous feedback from the hand.

Cutaneous feedback from the hand could assist with coordination between the arms and legs during locomotion. Previously we used a reduced walking model of combined arm and leg (ARM&LEG) cycling to examine the separate effects of rhythmic arm (ARM) and leg (LEG) movement. Here we use this same paradigm to test the modulation H-reflexes with and without interlimb cutaneous conditioning evoked by stimulating a nerve innervating the hand (superficial radial, SR). It was hypothesized that both ARM and LEG would contribute significantly to suppression of H-reflex amplitude during ARM&LEG. We also predicted a conservation of interlimb cutaneous conditioning during movement and an interaction between arm and leg rhythmic movement control. Subjects were seated in a recumbent ARM&LEG cycle ergometer and maintained a low-level soleus contraction for all tasks. H-reflex amplitude was facilitated by cutaneous conditioning evoked by stimulation of the SR nerve. H-reflex amplitudes were taken from recruitment curves and included modulation of 50% H max and H max. The suppressive effect of arm was less than that for LEG and ARM&LEG, while suppression during LEG and ARM&LEG were generally equivalent. For H-reflexes conditioned by cutaneous input, amplitudes during ARM&LEG instead were in between those for ARM and LEG modulation. Multiple regression analysis revealed a significant contribution for arm only in trials when SR stimulation was used to condition H-reflex amplitudes. We suggest that there is a measurable interaction between neural activity regulating arm and leg movement during locomotion that is specifically enhanced when cutaneous input from the hand is present.