Impaired Retention of Motor Learning of Writing Skills in Patients with Parkinson's Disease with Freezing of Gait

Elke Heremans, Evelien Nackaerts, Griet Vervoort, Sanne Broeder, Stephan P Swinnen, Alice Nieuwboer, Elke Heremans, Evelien Nackaerts, Griet Vervoort, Sanne Broeder, Stephan P Swinnen, Alice Nieuwboer

Abstract

Background: Patients with Parkinson's disease (PD) and freezing of gait (FOG) suffer from more impaired motor and cognitive functioning than their non-freezing counterparts. This underlies an even higher need for targeted rehabilitation programs in this group. However, so far it is unclear whether FOG affects the ability for consolidation and generalization of motor learning and thus the efficacy of rehabilitation.

Objective: To investigate the hallmarks of motor learning in people with FOG compared to those without by comparing the effects of an intensive motor learning program to improve handwriting.

Methods: Thirty five patients with PD, including 19 without and 16 with FOG received six weeks of handwriting training consisting of exercises provided on paper and on a touch-sensitive writing tablet. Writing training was based on single- and dual-task writing and was supported by means of visual target zones. To investigate automatization, generalization and retention of learning, writing performance was assessed before and after training in the presence and absence of cues and dual tasking and after a six-week retention period. Writing amplitude was measured as primary outcome measure and variability of writing and dual-task accuracy as secondary outcomes.

Results: Significant learning effects were present on all outcome measures in both groups, both for writing under single- and dual-task conditions. However, the gains in writing amplitude were not retained after a retention period of six weeks without training in the patient group without FOG. Furthermore, patients with FOG were highly dependent on the visual target zones, reflecting reduced generalization of learning in this group.

Conclusions: Although short-term learning effects were present in both groups, generalization and retention of motor learning were specifically impaired in patients with PD and FOG. The results of this study underscore the importance of individualized rehabilitation protocols.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Writing tasks that were assessed…
Fig 1. Writing tasks that were assessed by means of the touch-sensitive writing tablet.
(A) Single-task writing with visual target zones, (B) Single-task writing without visual target zones, (C) Dual-task writing, (D) Single-task tone counting. The small circle indicates the starting point of the writing sequence and the colored target zones indicate the requested writing amplitude in the conditions with cues.
Fig 2. Writing amplitude on the transfer…
Fig 2. Writing amplitude on the transfer task during the pre, post and retention test for both groups.
Mean and standard errors are presented. For writing amplitude (% of target size) a significant Time x Group interaction was found (F = 4.74, p = 0.01), showing improvements in amplitude from pre to post test in both groups, and from pre to retention test in the PD-FOG only. In the PD+FOG a significant decrease in amplitude was shown from post to retention test. * indicates significant increase with p

Fig 3. Writing amplitude on the transfer…

Fig 3. Writing amplitude on the transfer task in the presence and absence of cues…

Fig 3. Writing amplitude on the transfer task in the presence and absence of cues for both groups.
Mean and standard errors are presented. For writing amplitude (% of target size) a significant Group x Cue interaction was found (F = 4.42, p = 0.04), showing improved performance in the presence of cues in the PD+FOG only. * indicates significant increase with p

Fig 4. Coefficient of variation of the…

Fig 4. Coefficient of variation of the writing amplitude on the transfer task during the…

Fig 4. Coefficient of variation of the writing amplitude on the transfer task during the pre, post and retention tests for both groups.
Mean and standard errors are presented. For COVampl a significant main effect of time was found (F = 5.54, p = 0.03), showing improvements in variability of amplitude from pre to retention test in both groups. * indicates significant decrease with p<0.05.

Fig 5. Accuracy of the tone-counting task…

Fig 5. Accuracy of the tone-counting task during the automatization task during single- and dual-task…

Fig 5. Accuracy of the tone-counting task during the automatization task during single- and dual-task writing.
Mean and standard errors are presented. For accuracy of the tone-writing task (%) a significant Time x Task interaction was found (F = 9.17, p
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References
    1. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol. 2011; 10(8):734–744. 10.1016/S1474-4422(11)70143-0 - DOI - PMC - PubMed
    1. Vercruysse S, Gilat M, Shine JM, Heremans E, Lewis S, Nieuwboer A. Freezing beyond gait in Parkinson's disease: a review of current neurobehavioral evidence. Neurosci Biobehav Rev. 2014; 43:213–227. 10.1016/j.neubiorev.2014.04.010 - DOI - PubMed
    1. Plotnik M, Giladi N, Hausdorff JM. Is freezing of gait in Parkinson's disease a result of multiple gait impairments? Implications for treatment. Parkinsons Dis. 2012; 2012:459321 10.1155/2012/459321 - DOI - PMC - PubMed
    1. Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Wenderoth N, Swinnen SP, et al. Abnormalities and cue dependence of rhythmical upper-limb movements in Parkinson patients with freezing of gait. Neurorehabil Neural Repair. 2012; 26(6):636–645. 10.1177/1545968311431964 - DOI - PubMed
    1. Heremans E, Nackaerts E, Vervoort G, Vercruysse S, Broeder S, Strouwen C, et al. Amplitude manipulation evokes upper limb freezing during handwriting in patients with Parkinson's disease with freezing of gait. PLoS One. 2015; 10(11):e0142874 10.1371/journal.pone.0142874 - DOI - PMC - PubMed
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The project was funded by the Research Foundation – Flanders (FWO) (project G.0906.11). EH is a Postdoctoral Researcher and EN a Research Assistant at the Research Foundation – Flanders (FWO). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Fig 3. Writing amplitude on the transfer…
Fig 3. Writing amplitude on the transfer task in the presence and absence of cues for both groups.
Mean and standard errors are presented. For writing amplitude (% of target size) a significant Group x Cue interaction was found (F = 4.42, p = 0.04), showing improved performance in the presence of cues in the PD+FOG only. * indicates significant increase with p

Fig 4. Coefficient of variation of the…

Fig 4. Coefficient of variation of the writing amplitude on the transfer task during the…

Fig 4. Coefficient of variation of the writing amplitude on the transfer task during the pre, post and retention tests for both groups.
Mean and standard errors are presented. For COVampl a significant main effect of time was found (F = 5.54, p = 0.03), showing improvements in variability of amplitude from pre to retention test in both groups. * indicates significant decrease with p<0.05.

Fig 5. Accuracy of the tone-counting task…

Fig 5. Accuracy of the tone-counting task during the automatization task during single- and dual-task…

Fig 5. Accuracy of the tone-counting task during the automatization task during single- and dual-task writing.
Mean and standard errors are presented. For accuracy of the tone-writing task (%) a significant Time x Task interaction was found (F = 9.17, p
Similar articles
Cited by
References
    1. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol. 2011; 10(8):734–744. 10.1016/S1474-4422(11)70143-0 - DOI - PMC - PubMed
    1. Vercruysse S, Gilat M, Shine JM, Heremans E, Lewis S, Nieuwboer A. Freezing beyond gait in Parkinson's disease: a review of current neurobehavioral evidence. Neurosci Biobehav Rev. 2014; 43:213–227. 10.1016/j.neubiorev.2014.04.010 - DOI - PubMed
    1. Plotnik M, Giladi N, Hausdorff JM. Is freezing of gait in Parkinson's disease a result of multiple gait impairments? Implications for treatment. Parkinsons Dis. 2012; 2012:459321 10.1155/2012/459321 - DOI - PMC - PubMed
    1. Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Wenderoth N, Swinnen SP, et al. Abnormalities and cue dependence of rhythmical upper-limb movements in Parkinson patients with freezing of gait. Neurorehabil Neural Repair. 2012; 26(6):636–645. 10.1177/1545968311431964 - DOI - PubMed
    1. Heremans E, Nackaerts E, Vervoort G, Vercruysse S, Broeder S, Strouwen C, et al. Amplitude manipulation evokes upper limb freezing during handwriting in patients with Parkinson's disease with freezing of gait. PLoS One. 2015; 10(11):e0142874 10.1371/journal.pone.0142874 - DOI - PMC - PubMed
Show all 49 references
Publication types
MeSH terms
Grants and funding
The project was funded by the Research Foundation – Flanders (FWO) (project G.0906.11). EH is a Postdoctoral Researcher and EN a Research Assistant at the Research Foundation – Flanders (FWO). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib .nbib
Format: AMA APA MLA NLM
Fig 4. Coefficient of variation of the…
Fig 4. Coefficient of variation of the writing amplitude on the transfer task during the pre, post and retention tests for both groups.
Mean and standard errors are presented. For COVampl a significant main effect of time was found (F = 5.54, p = 0.03), showing improvements in variability of amplitude from pre to retention test in both groups. * indicates significant decrease with p<0.05.
Fig 5. Accuracy of the tone-counting task…
Fig 5. Accuracy of the tone-counting task during the automatization task during single- and dual-task writing.
Mean and standard errors are presented. For accuracy of the tone-writing task (%) a significant Time x Task interaction was found (F = 9.17, p

References

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    1. Vercruysse S, Gilat M, Shine JM, Heremans E, Lewis S, Nieuwboer A. Freezing beyond gait in Parkinson's disease: a review of current neurobehavioral evidence. Neurosci Biobehav Rev. 2014; 43:213–227. 10.1016/j.neubiorev.2014.04.010
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