Elsevier

Neuropsychologia

Volume 49, Issue 14, December 2011, Pages 3981-3988
Neuropsychologia

Freezing of gait is associated with a mismatch between motor imagery and motor execution in narrow doorways, not with failure to judge doorway passability

https://doi.org/10.1016/j.neuropsychologia.2011.10.014Get rights and content

Abstract

Background

Many patients with Parkinson's disease (PD) develop freezing of gait (FoG), which may manifest as a hesitation or “getting stuck” when they attempt to pass through a doorway. In two experiments, we asked whether FoG is associated with (1) a deficit in internal representation of one's body size with respect to a doorway and (2) a mismatch between imagined and actual walking times when passing through a doorway.

Methods

23 subjects with PD (11 with and 13 without FoG) and 10 control subjects of similar age completed two experiments. In the Passability experiment, subjects judged the passability of doorways with different apertures scaled to their body widths. We compared passability estimates across groups. In the Imagery experiment, subjects timed themselves while: (1) imagining walking through doorways of different apertures and from different distances and (2) actually walking in the same conditions they had just imagined. We compared imagined and actual walking durations across groups and conditions.

Results

In the Passability experiment, the estimated just-passable doorway was wider, relative to body width, in PD subjects than in control subjects, but there was no difference between PD subjects with and without FoG. In the Imagery experiment, subjects in all groups walked more slowly through narrow doorways than though wide doorways, and subjects with FoG walked much more slowly through the narrowest doorways. PD subjects with FoG showed a large discrepancy between actual and imagined time to pass through narrow doorways, unlike PD subjects without FoG and control subjects.

Conclusions

The equivalent passability judgments in PD subjects with and without FoG indicate that FoG is not specifically associated with a deficit in ability to internally represent space with reference to body size. However, the large difference in duration between actual and imagined walking through narrow doorways in subjects with FoG suggests that PD subjects with FoG did not know how much they would slow down to pass through narrow doorways. The observed discrepancy between imagined and actual walking times may point to a specific problem that contributes to the occurrence of FoG. These results also suggest that caution should be used when interpreting brain imaging results from locomotor imagery studies with PD subjects who have FoG.

Highlights

PD subjects estimate more space needed to pass through a doorway than control subjects estimate. ► Subjects with FoG imagine walking more quickly through narrow spaces than they actually walk. ► The execution-imagery discrepancy may point to a specific problem that contributes to FoG.

Introduction

Freezing of gait (FoG) is one of the most pernicious problems that people with Parkinson's disease (PD) may encounter. This symptom, which patients often describe as a feeling that their feet are ‘glued to the floor’ when they want to walk forward, is an important cause of falls for patients who experience it, markedly limits mobility, and eventually affects up to 80% of people with PD (Hely, Reid, Adena, Halliday, & Morris, 2008). The etiology of freezing is poorly understood, but in those who are susceptible, it can be triggered by cognitive factors like distraction, anxiety, or being in a hurry; or by performing certain actions, such as initiating gait, turning, and passing through doorways or tight spaces (Bloem et al., 2004, Giladi et al., 1992). We examined two hypotheses regarding freezing in doorways to generate insights into central mechanisms underlying FoG.

It has been suggested that FoG in doorways is related to difficulty judging the passability of an opening relative to one's own body size (Almeida & Lebold, 2010). Passability judgments necessarily depend both on the internal representation of one's own spatial dimensions (“body schema”) and on visuospatial ability. If a deficit in either of these functions is an important contributor to freezing in doorways, one would expect subjects with PD and FoG to perform differently in judgments of doorway passability than subjects with PD without FoG. While differences in passability assessments between PD subjects with and without FoG have not been tested, two recent studies have asked PD subjects to judge the passability of different apertures. The first study found that PD subjects whose disease affected mainly the left side of their bodies (right brain) estimated that they needed a larger opening than either control subjects or subjects with primarily right-sided (left brain) disease (Lee, Harris, Atkinson, & Fowler, 2001). These authors speculated that patients with left-sided PD experience a shrinking of extrapersonal visual space. The second study found that subjects with PD and FoG made near-identical doorway passability estimates to those of control subjects (Cowie, Limousin, Peters, & Day, 2010). However, in this latter study, subjects performed the passability estimates after actually walking through doorways with different apertures; thus, they could rely on memory to complete the task. Also of note, neither study compared PD subjects with and without FoG.

In addition to a possible difficultly assessing the environment with respect to their own body dimensions, it is possible that PD subjects have a deficit in intuitively understanding their own facility for action, including how much motion a particular motor command is likely to produce and how long different actions (such as locomotion) will take to perform (Ivanenko et al., 2011, Krakauer et al., 1999). In healthy subjects, the same internal representations used for motor execution are also thought to be used for motor imagery (Decety, 1996, Jeannerod, 1995). This similarity is supported by studies showing that mental rehearsal can improve performance (Kohl & Roenker, 1980), by demonstrations of a large overlap in brain areas active for imagined and actual movement (Roth et al., 1996), and by evidence that imagined and executed movements are of similar duration and scale similarly in response to distance and accuracy requirements (Decety and Jeannerod, 1995, Stevens, 2005).

Motor imagery depends on the supplementary motor area (SMA) (Roland, Larsen, Lassen, & Skinhøj, 1980), which, as a primary target of basal ganglia output, is underactive in people with Parkinson's disease (Jacobs et al., 2009, Jahanshahi et al., 1995, Roland et al., 1980). Thus, it is unsurprising that motor imagery seems to be affected in PD. For instance, slow decay of motor-related potentials during motor imagery in advanced PD has been reported (Cunnington, Iansek, Johnson, & Bradshaw, 1997), and a study demonstrated that for PD patients with symptoms mainly on the right side, motor imagery of the right hand was slowed relative to motor imagery of the left hand (Helmich, de Lange, Bloem, & Toni, 2007). These results are consistent with the assumption that the internal representation used by motor imagery is the same representation used for actual movement; one would expect slower movement of the hand on the more affected side, as well as slower motor imagery. However, the primary motor deficit included in these studies is bradykinesia, which tends to be consistent across situations and repetitions. FoG, in contrast, is intermittent. It is not known whether the gait abnormalities present with FoG (including extreme slowing, variable cadence, and occasional arrests) are reflected in a common internal representation that is used both for motor imagery and for motor execution, or whether, in subjects with FoG, there is a dissociation between motor imagery and motor execution.

By carrying out two experiments with the same group of subjects, we tested two separate hypotheses about FoG in doorways. In the Passability experiment, we asked healthy older subjects and subjects with PD (with and without FoG) to assess the passability of various door widths. If FoG is associated with difficulty in evaluating the constraints in the environment with respect to the body schema, or with perceptual crowding of extrapersonal space, subjects with FoG should estimate that they need wider doorways than subjects without FoG.

In the Imagery experiment, we asked the same subjects to time themselves while they imagined walking through doorways of different widths. As a control for ability to imagine themselves walking, we also asked subjects to time themselves while they imagined walking different distances to and through a doorway. We compared the duration of motor imagery of walking to the duration of actual walking in the same conditions. If FoG is associated with a general mismatch between motor imagery and motor execution, then PD subjects with FoG should have trouble imagining how long it would take them to actually walk in a variety of situations. If FoG is associated with a specific failure to accurately represent one's own motor facility in situations provoking freezing of gait, then PD subjects with FoG should have particular trouble imagining how long it would take them to walk through narrow doorways.

Section snippets

Subjects

Thirty-four subjects (11 diagnosed with idiopathic PD who reported freezing of gait, 13 diagnosed with idiopathic PD who did not report freezing of gait, and 10 healthy older controls), participated in the study after signing an informed consent form approved by the Institutional Review Board of Oregon Health & Science University (OHSU). See Table 1 for demographic and clinical details. Exclusion criteria were: dementia or other neurological diseases, vestibular disorders, musculoskeletal gait

Subject demographics

Subject demographics are presented in Table 1, Table 2. Subjects in all groups were well matched in age and body width. Among the subjects with PD, those with and without FoG had similar disease durations, and sides of disease onset were equally balanced, but the subjects with FoG had more severe Hoehn and Yahr stages and UPDRS scores than the subjects without FoG.

Passability experiment

Fig. 2 shows passability estimates. Healthy subjects judged that they could easily pass through a doorway that was 97% of their body

Main findings

In two experiments with the same subjects, we tested two hypotheses about the FoG that many subjects with PD experience when passing through doorways. Results suggest that FoG is not associated with a problem judging passability, but that it is associated with a discrepancy between motor imagery and motor execution when passing through narrow doors.

Conclusion

We found that, although changes in visuospatial processing distinguished PD subjects from age-matched healthy control subjects, they did not distinguish between PD subjects with and without FoG. In addition, there was no general motor imagery deficit associated with FoG. However, FoG was specifically associated with a tendency to imagine passing through a narrow doorway more quickly than one could execute such a passage. The observed discrepancy between imagined and actual walking times may

Acknowledgements

We are grateful to the subjects who participated in this study, to Triana Nagel for help scheduling and testing subjects, and to Charlie Russell for building the equipment. This study was funded by grants from NIH (R37AG006457, T32AT002688, and T32NS045553).

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