External exercise cues and dual task ability during gait in people with PD

Beck, Intzandt & Almeida (2018)

Gait, or walking, is a well-learned series of movements, achieved with little attention (so mostly subconscious), and facilitated by the basal ganglia. In particular, the dorsal striatum is implicated in the process, with loops to and from the sensorimotor cortex. The dorsal striatum is also the initial area of degeneration in Parkinson’s Disease, and so it makes sense that people with PD shift to a more conscious control of walking.

However, controlling gait more consciously increases the demand on attentional resources. As a result, when walking while completing a secondary task, people with PD display worsened gait – increased step time, percentage of time spent in double support, step-to-step variability, and decreased step length.

Cues can influence how movements are controlled. External cues, those that direct attention externally to the effect of an action on the environment, utilise automatic process, and sensorimotor cortical areas. Conversely, internal cues direct attention to one’s own limb movement, relying on conscious processes that linked to the frontal cortex.

It could be argued that if individuals with PD have disrupted automatic movement processing, that providing an internal focus of attention could help improve a movement. However, in a study that measured postural sway on a force platform with PD patients ON dopaminergic medication, an external cue to focus on the movement of the platform led to better performance than the internal cue to focus on the movement of the feet. External cues were detrimental in the OFF state, though.

The authors thus propose that years of basal ganglia degeneration and compensation via conscious control leads to people with PD unable to utilise automatic processes. A solution, therefore, would be to improve the ability to process automatically, facilitating an enhancement of dual task ability.

Aims

The study used a form of goal-based exercised previously used by the research group with success – PD-SAFEx. There were three key aims of the study:

  1. Would the goal-based exercise programme, in conjunction with an external focus of attention, improve dual talk walking ability?
  2. Would external and internal focuses of attention have an effect on motor symptom severity, as measured by the UPDRS-III? It was expected that the external group would see improvements.
  3. Finally, would external or internal focuses of attention with the exercise programme lead to long term neuronal changes? This would be measured by using a washout period, to see if walking behaviour persisted 8 weeks following programme cessation.

Design

Three parallel groups were assessed with instrumental measures – gait, and performance of secondary task (digit-monitoring) while walking – and clinical measures – the UPDRS.  Other secondary measures were collected for the sake of control, and can be found on page 5 of my hand-written notes.

The three groups – (1) external, (2) internal and (3) control –  were all assessed before the 11-week programme, and after the programme. The control group was not included in the washout assessment, so statistical analysis was broke into part A and part B. Part A included comparisons of the three groups pre- and post-assessment, and part B compared external and internal at all three evaluation times.

Results and Discussion

Due to the many results the design generated, I will begin this section with the conclusions and list some of the results that support each conclusion. As linked to earlier, my (messily) handwritten notes can be found here.

Conclusion 1: External focus of attention with goal-based exercises did not improve motor symptom severity (UPDRS) and dual-task walking ability more than an internal focus of attention. 

Support:

  • UPDRS scores decreased (improved) from pre to post to washout tests ON and OFF dopaminergic medication, in BOTH external and internal groups.
  • Gait did not improve in external from pre to post assessment.
    • This might be because an external focus of attention didn’t improve automatic control functioning, or maybe that the length of the programme was not enough for neuronal changes to occur. Step time did improve from pre to post in external, in part A analysis, which might indicate a trend could develop with a longer programme, influencing the other gait measures.

Conclusion 2: External focus of attention did improve gait without hindering performance in the secondary task. 

Support:

  • While some gait measures improved from pre to washout assessment, such as step time and % time spent in double support, the internal group also displayed much poorer performance in the secondary task. Both groups saw minor changes in secondary task error at post-assessment, but while external remained unchanged at washout, internal saw 42% more error compared to the pre test.
    • It should also be noted that error in the digit-monitoring task was also high for the internal group even performed by itself. The authors did not offer an explanation as to why single task performance might be harmed for the internal group.

Conclusion 3: Improvements for internal in step time and % of time spent in double support are likely due to consciously controlling gait and not an improvement in dual task ability. 

Support:

  • Same as the evidence for the second conclusion.

Conclusion 4: External focus of attention with exercise may have improved basal ganglia function. 

Support:

  • Lack of drop off in secondary task performance for the external group. The number of errors made in the external group in the digit-monitoring task increased from pre to post, although only by 6%, and then decreased slightly from post to washout (-1%).
  • UPDRS-III scores improved in external, mostly so in the OFF state, from pre to post, by 5.4 points which is greater than the minimal clinical important 5-point change (Schrag et al., 2006). Improvements for external in both ON and OFF qualified for Shulman’s lower 4.5-point standard.
  • As the authors cite in the paper, UPDRS scores reflects dopamine levels in the basal ganglia.

Further thoughts

One critique of the study the authors make, is that the method to induce an external focus of attention is not effective enough. As Gabriele Wulf has found in some of her research, the distance of the external focus of attention from the body affects motor learning and performance. Thus, the study in focus, which placed coloured labels in four different locations directly on the body, might not have utilised optimal external cues.

The authors argued that the label method was still a valid method due to a previous study that used labels on gymnasts to induce an external focus of attention. However, the use of labels in the study in focus may still not be optimal. In the gymnast study, participants were instructed to focus on the direction tape on their chest was facing (external) when landing a 180º airborne turn. The internal group were told to focus on the direction their hands were facing on landing. There are two problems with this. Firstly, the gymnast study did not compare the external cue with an internal cue that involved the same body part (the chest) so the results aren’t as sound as they could be. Secondly, the chest might be a unique part of the body in this context anyway, because to face the chest in a certain direction would require the gymnasts to move the whole body and not focus on individual limb movements. Hence, this resembles more an external or metaphorical cue, and maybe saying “face the chest in this direction” would act more as an external cue and induce automatic processing and better motor performance, even without the tape marker.

Therefore, while I do believe coloured labels on limbs are likely effective when used in external cues, it is also worthwhile considering that there is still some focus on limb movement as in an internal cue.

From my experience as a strength coach, I use external cues as much as possible when teaching athletes skills. For example, an acceleration wall drill I have used when training footballers recently, I have used the cue “smash through the wooden plank with the knee” (which obviously gets shortened when repeated) to encourage a powerful knee drive. This metaphorical cue acts as an external cue (focusing on the effect of the body on its environment), to hopefully achieve better motor performance and learning. This directs the attention away from thinking about flexing the hip, flexing the knee, dorsiflexing the ankle whilst extending the leg in contact with the ground and staying tall throughout, all of which would require slower and more conscious processing, and all of which can be processed automatically with the cue “smash the wood”.

Similarly, a cue to direct the chest in a certain direction on landing possibly directs attention away from the leg and arm movements, and core bracing that I guess would be required to successfully perform the gymnastic manoeuvre. The leg and arm movements can then be processed automatically. Not only does this mean the taped chest marker in the gymnast study could have been redundant, but it means the coloured labels in Beck et al. (2018) might not be optimal as the attention isn’t taken far enough away from the limb movements. And I mean hierarchically distant, as opposed to physically distant in terms of marker placement.

Whilst I don’t currently have access to all the exercises in the PD SAFEx programme, the examples I have seen – e.g. lifting the knee with the contralateral arm touching the ear, also cued as “push the green label up” for the knee movement – may be difficult to externally cue due to the lack of complexity and use of the body as a whole. A knee raise is hard to separate from the movements of the limbs as it is defined by the movements of the limbs.

This is something I will certainly be looking into as I currently read into the literature for a project proposal to achieve my PhD.

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