by Dr Jesse Dean.

Among stroke survivors, mobility can be limited by a high risk of falls. Such falls commonly occur during walking, and are often due to self-generated movement errors rather than external perturbations such as slips or trips. Unfortunately, rehabilitation approaches focused on strength or general balance training have failed to effectively reduce fall incidence in this population, despite the success of these approaches in older adults without neurological injuries. This discrepancy may be partially due to a lack of consideration of the gait characteristics that make stroke survivors particularly susceptible to a loss of balance. The purpose of our study was to investigate a gait characteristic that may contribute to altered balance – the adjustment of step width to stabilize fluctuations in the mechanical state of the body.

To investigate step width adjustments, 20 chronic stroke survivors walked on a treadmill at their self-selected and fastest-comfortable speeds. We quantified the link between mediolateral pelvis motion and step width on a step-by-step basis using regressions and partial correlations. Similar methods used in neurologically-intact adults have previously revealed that step width tends to increase with larger pelvis displacements and with higher velocities away from the stance leg (Fig. 1). This is thought to help stabilize the mediolateral motion of the body. Our results showed that the link between pelvis displacement and step width was weaker for steps taken with the paretic leg than for steps taken with the non-paretic leg. Moreover, this relationship was not affected by walking speed. Accompanying the weaker link between pelvis displacement and paretic step width, steps taken with the paretic leg were placed more laterally, with a larger and more variable mediolateral margin of stability – a metric often used to assess walking balance.

The altered behavior observed with paretic steps is consistent with – but does not prove – the use of a more conservative foot placement strategy to reduce the risk of loss of balance towards the paretic side, which may otherwise result from reduced paretic stepping accuracy. However, these results may provoke more questions than they answer. Most notably, can the altered biomechanical behavior be changed through training focused on paretic steps? Would doing so improve post-stroke walking balance and reduce the risk of falls? Ongoing research is working toward answering these questions, with the ultimate goal of contributing to new therapeutic approaches for improving functional mobility after a stroke.

Figure 1. In neurologically-intact adults, the mediolateral displacement and velocity of the pelvis during a step (a) is predictive of the step width at the end of the step (b). The strength of this relationship can be quantified using regressions and partial correlations over a series of steps.

Publication

Stimpson KH, Heitkamp LN, Embry AE, Dean JC. Post-stroke deficits in the step-by-step control of paretic step width. Gait Posture. 70, 136-140, 2019. DOI: 10.1016/j.gaitpost.2019.03.003

About the Author

By Dr Prakruti Patel.

Most stroke survivors regain community ambulation although, the recovery of sensorimotor impairments is often incomplete. Consequently, stroke-related impairments can increase the risk of falls from environmental perturbations like slips and trips. Effective reactive balance control is crucial to prevent a fall upon exposure to sudden external perturbations. Reactive balance control is impaired after stroke; however, whether the ability to prevent a fall is influenced by the direction of fall is not well understood. The current study identified the influence of the direction of fall on reactive balance control and fall risk in chronic stroke survivors relative to healthy adults.

Chronic ambulatory stroke survivors, age-matched adults, and young adults were exposed to single perturbations to stance via forward (SLIP) and backward (TRIP) directed surface translations at 16 m/s² for 0.20 m via a treadmill. We measured incidence of falls, postural stability which was defined as the center of mass position and velocity relative to the base of support, and compensatory step and trunk kinematics. To compare the stability between SLIPs and TRIPs, we computed the change in stability from compensatory step liftoff to touchdown (∆XCoM). Higher values for ∆XCoM indicated greater stability at touchdown. In the stroke group, incidence of falls on a SLIP (53.83%) was greater than on a TRIP (0%); however, this was not seen in the control groups (Figure A). Interestingly, all three groups showed a higher ∆XCoM on TRIPs than SLIPs, suggesting that regardless of age and unilateral brain damage, the reactive stability during a TRIP is greater than that during a SLIP (Figure B). In control groups, such differential stability between the perturbations was predominantly contributed to by the ability to control trunk position and velocity rather than compensatory step length. In contrast, in the stroke group, impaired trunk control and insufficient compensatory step length together contributed to lower stability on SLIPs compared with TRIPs.

These results highlight that reactive balance control to large perturbations varies with regards to perturbation direction such that the stability is lower in SLIPs than TRIPs. Although aging and presence of neurological impairments increase the risk of falling, the likelihood of backward falls is higher than forward falls, particularly in chronic stroke survivors. Our results suggest that reactive balance assessment and training is crucial for fall prevention in chronic phases of recovery when a large proportion of stroke survivors achieve community ambulation, predisposing them to falls from environmental perturbations.

 Figure

A. Incidence of falls in young adults, age-matched adults (AM), and stroke survivors during a SLIP and a TRIP. B) The change in stability (DXCoM) from compensatory step liftoff (LO) to touchdown (TD). A higher value for DXCoM indicates greater change in stability from LO to TD, suggesting a more stable position. The DXCoM was greater during a TRIP than a SLIP in all the groups.

Publication

Patel, P. J., & Bhatt, T. (2018). Fall risk during opposing stance perturbations among healthy adults and chronic stroke survivors. Experimental brain research, 236(2), 619-628.

About the Author

Freezing of gait (FOG) is a very disabling symptom of Parkinson’s disease (PD). Therefore, several maneuvers to preserve gait or to support taking steps after FOG onset are of great interest to clinicians and patients. Since impaired proprioceptive processing is considered a contributing factor to FOG, we asked: would enhanced proprioceptive stimuli reduce FOG severity? We used tendon vibration to stimulate the proprioceptive system via activation of muscle spindles. The aim of this study was to verify the effects of tendon vibration on FOG severity, when used as a preventive and rescue strategy.

To induce FOG episodes, sixteen individuals known to experience FOG (so-called freezers) walked with small steps on a pressure-sensing mat. Custom-made devices were used to provide Achilles tendon vibration (100 Hz, amplitude of 1.0 mm) whenever a FOG episode was detected (1^stepisode) to test its utility as rescue strategy. Since we did not turn-off vibration until the end of the trial, we could evaluate its effects as a preventive strategy on subsequent FOG episodes. We compared the effect of tendon vibration between stimulation of the leg that was least (LA) or most affected (MA) by PD symptoms. A condition without tendon vibration (OFF) was also collected as baseline. Our results show that tendon vibration successfully alleviated FOG severity when used as a rescue strategy during the 1^st episode. However, this was only true when the LA limb was stimulated (Figure 1A). Vibration influenced the limb used to reinitiate gait after freezing, increasing the number of initiations with the contralateral leg (Figure 1E).Tendon vibration did not reduce FOG severity when used as a preventive strategy, since we observed no differences in the durations of subsequent freezing episodes (Figure 1A, in orange). This was also highlighted by a lack of difference in time between FOG episodes among conditions (Figure 1D).

Our results strengthened the notion that FOG is related to proprioceptive processing deficits. These findings ruled out attentional mechanisms, given that vibration effects were only observed unilaterally and most steps to reinitiate gait were taken with the contralateral leg. Most importantly, this study demonstrated that tendon vibration is a promising technique to alleviate FOG severity in individuals with PD, especially in those with mild symptoms. Future research should focus on transferring tendon vibration to clinic practice and test its effects on other modalities of freezing.

Figure. A: Mean (SE) tendon vibration effects on first (blue) and subsequent (orange) freezing episodes per condition. OFF: no vibration; MA: most-affected limb; LA: least-affected limb. Vertical black line refers to significant differences between conditions; B and C:  Description of walking sections analysed in the study; D: Mean (SE) time between freezing episodes per condition; E: percentage of steps used to re-initiate gait per limb.

Publication

Pereira MP, Gobbi LT, Almeida,QJ. Freezing of Gait in Parkinson’s disease: Evidence of sensory rather than attentional mechanisms through muscle vibration. Parkinsonism Relat Disord, v. 29, p. 78-82, Aug 2016. ISSN 1873-5126. doi: 10.1016/j.parkreldis.2016.05.021.

About the Author

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) can improve gait in Parkinson’s disease. It does so mainly by improving the step length and step velocity, leaving the step time unchanged. However, this temporal aspect of gait is critical in Parkinson’s disease and a pathophysiological hallmark of freezing of gait. In this study, we studied if stimulating the substantia nigra pars reticulata (SNr) would improve step time and thereby be a target to remediate freezing of gait. The SNr can be stimulated with current DBS electrodes by stimulating the most caudal contact, instead of one of the upper contacts for STN. We were interested in the effect of SNr stimulation because the SNr has inhibitory GABA-ergic projections to the mesencephalic locomotor region. This region can induce rhythmic stepping behavior and is integrated in the temporal modulation of gait. Second, combined STN+SNr stimulation have shown beneficial effects for the treatment of freezing of gait. Here, we studied different spatial and temporal gait parameters to learn more about the role of STN or SNr in locomotor integration.

During the experiments, Parkinson’s disease patients with a DBS implant walked overground in three conditions (without stimulation / STN stimulation / SNr stimulation). We extracted gait parameters from inertial sensors mounted on both ankles and lower back. We observed that spatial parameters of gait, such as step length, were only improved by STN stimulation. Temporal gait asymmetry, assessed as the difference in swing times of both legs, was improved by both STN and SNr stimulation. Furthermore, a more medial location of the caudal contact was associated with a greater improvement of gait regularity by SNr stimulation. This suggests that a more medial stimulation of the SNr is more effective in reducing the variability of gait.

We observed that both STN and SNr stimulation can improve temporal gait asymmetry. This means that both target areas entrain locomotor integration at the level of the mesencephalic locomotor region. In animal experiments, stimulation of the mesencephalic locomotor region can modulate cadence, but not step length, which is in line with our results. Also, it is observed that a more medial stimulation of the SNr in rats modulates temporal integration of gait, as opposed to stimulation of the lateral part of the SNr. It might be possible that by improving gait asymmetry, the occurrence of freezing of gait could be reduced. Further research, including combined STN+SNr stimulation, is needed to confirm this finding and is being conducted at the moment (ClinTrials.gov: NCT02588144). Together, these findings help to decipher the pathophysiological networks and mechanisms involved in gait problems in Parkinson’s disease patients.

Figure. Model of the basal ganglia network including output to the central pattern generators. Stimulating subthalamic nucleus (STN) or substantia nigra pars reticulata (SNr) may influence different network loops in the brain. GPe = globus pallidus, external segment; GPi = globus pallidus, interal segment; PPN = pedunculopontine nucleus; SNc = substantia nigra pars compacta

Publication

Scholten M, Klemt J, Heilbronn M, Plewnia C, Bloem BR, Bunjes F, Krüger R, Gharabaghi A, Weiss D. Effects of subthalamic and nigral stimulation on gait kinematics in Parkinson’s disease. Front. Neurol. 2017; 8: 543. (https://www.frontiersin.org/articles/10.3389/fneur.2017.00543/full)

About the Author

After stroke, asymmetrical stepping and standing balance is commonly observed when weight bearing or spatiotemporal parameters are measured. These asymmetries are thought to circumvent stroke-related impairments and enable stroke survivors to walk and maintain their balance while standing. However, at the same time, motor planning is also impaired in stroke survivors which impacts the integration of incoming sensory information during functional daily movements and standing balance performance. This process is not well understood but could explain stroke-induced asymmetries. Movement-related cortical potentials (MRCPs) – measured using electroencephalography (EEG) – can be used to estimate motor planning processes in the cortex. After a stroke, longer duration and larger amplitude MRCPs are detected for planning paretic hand movements compared with the non-paretic hand. These differences to the MRCP are thought to reflect the longer time and greater cognitive effort needed to plan a movement, respectively. The aim of this study was to examine motor planning via MRCPs to understand whether motor planning can be attributed to difficulties with stepping and balance after a stroke.

Self-initiated stepping was performed by participants with sub-acute stroke with the paretic and non-paretic legs. Both EEG and electromyography recorded brain and muscle activity, with movement onset identified by electro-goniometers affixed to the lateral knees. There were no significant differences in stepping performance between legs or in MRCP measures (p ≥ 0.069, Figure). However, when the paretic leg was stepping, the burst onset of the biceps femoris (or hamstring) muscle influenced the MRCP amplitude (p = 0.024; Figure).

This indicates that cortical planning for initiating stepping is similar between legs after a stroke. Between-leg symmetry may indicate that a portion of the motor planning is actually to prepare for the movement as a whole (e.g. walking). Comparable motor programs may be needed to plan the shifting of the centre of mass, irrespective of whether it is to plan stepping of the paretic or non-paretic legs. It is likely that the motor plan required for stepping reflects this pattern in the sub-acute phase after stroke. The earlier hamstring muscle activity in the paretic leg may then be associated with a lower cognitive effort as measured by the MRCP. The MRCP may therefore be an important process for the timing of muscle preparation for initiating stepping in stroke survivors.

Figure: In panel A, no differences are seen between the paretic and non-paretic legs for step duration, movement related cortical potential (MRCP) amplitude or biceps femoris (BF) onset. Bars indicate standard deviations. In panel B, higher cognitive effort (MRCP amplitude) related to later onset of BF burst in the paretic leg stepping condition. Data points above the horizontal line indicate individuals with the onset of BF burst after knee flexion, and points below the line specify individuals that show a BF burst in advance of knee flexion. Smaller MRCP amplitudes were found in those with earlier onset BF suggesting that lower cognitive effort is required with an anticipatory burst of hamstring muscle activity.

Publication

• Peters S, Ivanova TK, Lakhani B, Boyd LA, Staines WR, Handy TC, Garland SJ. Symmetry of cortical planning for initiating stepping in sub-acute stroke. Clinical Neurophysiology. 2018 Apr;129(4):787-796. doi: 10.1016/j.clinph.2018.01.018. Epub 2018 Feb 1.

About the Author

Many neurological disorders lead to gait and balance impairments. Especially in older people, these disorders are a common cause of falls, associated with significant morbidity and mortality. Despite the recognition of the socio-economic burden of falls, there are very few treatment options beyond physical therapy for neurological gait and balance impairment. From a brain perspective, human locomotion relies upon a distributed neural network including primary motor, premotor areas, basal ganglia and, importantly, white matter connections between these areas. White Matter hyperintensities and other changes in the cerebral white matter (‘leukoaraiosis’) are very common in old age and associated with gait and balance dysfunction.

This review paper explores whether beneficial effects of physical training can be enhanced by using non-invasive brain stimulation, namely transcranial direct current stimulation (tDCS), in patients with neurological gait disorders. tDCS is a non-invasive neurostimulation technique that consists of delivering a weak electrical current through the scalp. This has been shown to induce bidirectional polarity-dependent changes in excitability of the underlying cortex; anodal tDCS increases cortical excitability and cathodal tDCS decreases it. The physiological and behavioural effects of tDCS have been shown to last for up to one hour, implying that tDCS also modulates the synaptic strength of intracortical and corticospinal neurons.

Across a number of our own pilot studies, we explored whether these physiological and behavioural effects may facilitate neuroplasticity during physical therapy and thus enhance its effectiveness. We applied 15 minutes of anodal tDCS over the motor and premotor cortex of both cerebral hemispheres using a central electrode in patients with Parkinson’s disease and patients with leukoaraiosis while they were also receiving gait and balance physical therapy. We found that the combination of cortical stimulation and physical therapy improved gait velocity, stride length, time taken to complete the ‘Timed Up and Go’, and postural reactions, above and beyond the positive effects of physical therapy alone. tDCS alone (without physical therapy), however, did not improve gait in patients with Parkinson’s disease or leukoaraiosis.

Our review paper and pilot studies suggest that non-invasive brain stimulation (such as tDCS) may enhance the effects of physical therapy in patients with neurological gait disorders. Large-scale, multicenter, randomized, double-blind, Phase III studies using standardized protocols based on the more robust published pilot data are needed before these techniques can be implemented into mainstream clinical practice.

Figure 1. A tDCS stimulation protocol showing anodal tDCS stimulation over the primary motor and pre-motor cortices bilaterally, and reference (cathode) electrode (blue rectangle), over the inion. B Hypothesized effect on synaptic excitability depicting the additive effect of physical therapy and tDCS (red arrow) in lowering the threshold of a motor action potential (i.e. increased cortical excitability), leading to increased cortical plasticity over motor cortical regions, and improved clinical outcomes. C Mean averaged data across pilot studies discussed in the main text, showing the largest reduction in time taken to walk 6 metres in the tDCS + physical therapy arm, compared to physical therapy with sham stimulation.

Publication

Kaski D, Bronstein AM, 2014, Treatments for Neurological Gait and Balance Disturbance: The Use of Non-invasive Electrical Brain Stimulation, Advances in Neuroscience, Vol: 2014, Pages: 1-13, ISSN: 2356-6787

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