Objective: To examine how a cued change in motor plan influences Parkinson’s disease (PD) patients with freezing of gait (FOG) (PD FOG; n=10), compared with those without FOG (PD non-FOG; n=10) and healthy controls (n=10).
Methods: Participants walked through a doorway in three experimental conditions: no cue; cue before gait initiation; and cue after gait initiation. The light cue was presented at the end of the pathway and signified that individuals must walk to the cue, turn around and return to starting position.
Results: Step-to-step variability (a known precursor to FOG) revealed a significant main effect of group (F2,27=32.83, p\u3c0.001), where PD FOG walked with greater step length variability than PD non-FOG and the control group. A significant interaction (F4,54=3.035, p=0.025) demonstrated that only the PD FOG group was most variable when the cue was present before gait initiation.
Conclusion: This study concludes that motor planning deficits affect gait, specifically in individuals who experience FOG. This may have important implications for the design of therapeutic interventions in PD FOG

Almeida, Quincy J.

Kielstra, Lauren

Knobl, Patricia

English

Wilfrid Laurier University

Wilfrid Laurier University Scholars Commons @ Laurier Kinesiology and Physical Education Faculty Publications Kinesiology and Physical Education 2012 The Relationship Between Motor Planning and Freezing of Gait in Parkinson’s Disease Patricia Knobl Wilfrid Laurier University Lauren Kielstra Wilfrid Laurier University Quincy J. Almeida Wilfrid Laurier University, qalmeida@wlu.ca Follow this and additional works at: https://scholars.wlu.ca/kppe_faculty Recommended Citation Knobl, Patricia; Kielstra, Lauren; and Almeida, Quincy J., "The Relationship Between Motor Planning and Freezing of Gait in Parkinson’s Disease" (2012). Kinesiology and Physical Education Faculty Publications. 11. https://scholars.wlu.ca/kppe_faculty/11 This Article is brought to you for free and open access by the Kinesiology and Physical Education at Scholars Commons @ Laurier. It has been accepted for inclusion in Kinesiology and Physical Education Faculty Publications by an authorized administrator of Scholars Commons @ Laurier. For more information, please contact scholarscommons@wlu.ca. RESEARCH PAPERThe relationship between motor planning and freezingof gait in Parkinson’s diseasePatricia Knobl, Lauren Kielstra, Quincy AlmeidaABSTRACTObjective To examine how a cued change in motor planinfluences Parkinson’s disease (PD) patients with freezingof gait (FOG) (PD FOG; n¼10), compared with thosewithout FOG (PD non-FOG; n¼10) and healthy controls(n¼10).Methods Participants walked through a doorway inthree experimental conditions: no cue; cue before gaitinitiation; and cue after gait initiation. The light cue waspresented at the end of the pathway and signified thatindividuals must walk to the cue, turn around and returnto starting position.Results Step-to-step variability (a known precursor toFOG) revealed a significant main effect of group(F2,27¼32.83, p<0.001), where PD FOG walked withgreater step length variability than PD non-FOG and thecontrol group. A significant interaction (F4,54¼3.035,p¼0.025) demonstrated that only the PD FOG group wasmost variable when the cue was present before gaitinitiation.Conclusion This study concludes that motorplanning deficits affect gait, specifically in individualswho experience FOG. This may have importantimplications for the design of therapeutic interventions inPD FOG.INTRODUCTIONParkinson’s disease (PD) is a neurodegenerativedisorder that is characterised by a lack of dopamineproducing cells in the substantia nigra compacta ofthe basal ganglia. The cardinal symptoms of PDinclude but are not limited to: bradykinesia (slowness of movement), akinesia (absence of movement), postural instability, tremor and rigidity.Freezing of gait (FOG) is argued by some to bea ﬁfth cardinal symptom distinguished by thesudden inability to initiate or continue walking.1FOG is identiﬁed as one of the major contributorsto a decreased quality of life in PD and has beenincreasing over the years appearing in about 53% ofpatients with PD in the advanced stages of thedisease; however, the pathophysiology is stillpoorly understood.2 4Several studies have investigated the physiological mechanisms associated with FOG. FOG istypically considered a motor impairment; however,recent research suggests that declining executivefunction and deﬁcits in perception may alsocontribute to FOG.5 7 One study examined theexecutive function of PD patients and found worseperformance in patients with FOG regardless ofdisease severity.8 Spatial perceptual deﬁcits havealso been shown to interrupt the initial onlinemovement sequence in patients with FOG.9However, given that freezing occurs when turning,manoeuvring through a crowded area and evenwhen a change in gait is prompted by the closing ofan elevator door, it is important to consider howmotor planning might be associated with FOG.Somewhat related, individuals with Parkinson’sdisease who exhibit freezing also have difﬁcultyshifting attention when performing online modiﬁcation of a complex motor sequence.10 Althoughgait is typically controlled fairly automatically,when gait requires more conscious control (such aswhen planning of an upcoming event is necessary),impairments may be more readily identiﬁed.In order to evaluate how gait may be inﬂuencedby the requirement to plan an upcoming movement while walking, three groups of participantswere required to walk through a narrow doorwaywith the possibility of being cued to turn aroundand walk back. By manipulating when the cueprompted this switch, it would be possible touncover whether gait is inﬂuenced by the need toplan the switch during walking (in contrast to priorto walking). The aim was to determine if and whenthe requirement to plan an upcoming change inwalking would inﬂuence gait and trigger a freezingepisode within individuals with PD who experienced FOG (PD FOG) compared with PD non FOGand healthy control participants.METHODSParticipantsThe study involved 20 participants with PD (10 PDFOG, 10 PD non FOG) and 10 healthy, agematched control participants (table 1). All participants were recruited from the database at the SunLife Financial Movement Disorders Research andRehabilitation Centre at Wilfrid Laurier University.All participants with Parkinson’s disease weretested approximately 1 h after taking their antiParkinson’s medication. Participants in the PD FOGgroup were classiﬁed based on their self report ofFOG. The participants must have scored one orhigher on question 14 of the Uniﬁed Parkinson’sDisease Rating Scale (UPDRS II), which addresseswhether the freezing phenomenon was experiencedat the time of enrolment as a research participant.An interview was also conducted by a clinician toconﬁrm FOG in these patients at the time of thetest. All participants with PD were conﬁrmed bya movement disorder neurologist and wereexcluded if they were previously diagnosed withdementia (severe loss of cognitive ability). The nonFOG PD group had no self report of freezingSun Life Financial MovementDisorders Research andRehabilitation Centre, WilfridLaurier University, Ontario,CanadaCorrespondence toDr Quincy Almeida, WilfridLaurier University, Sun LifeFinancial Movement DisordersResearch & RehabilitationCentre, 75 University Ave W,Waterloo, ON N2L 3C5, Canada;qalmeida@wlu.caThe research presented herereflects part of the requirementsfor the Master’s degree inKinesiology, partially completedby the first author from WilfridLaurier University.Received 30 June 2011Revised 2 August 2011Accepted 4 July 2011Published Online First11 August 201198 J Neurol Neurosurg Psychiatry 2012;83:98e101. doi:10.1136/jnnp 2011 300869Movement disorders           condition. c2 tests were conducted to determine signiﬁcancebetween the conditions.RESULTSPatient demographicsNo signiﬁcant differences in age were evident between groups(see table 1), although an independent t test illustrated a significant difference in years since diagnosis between PD patientswho experienced FOG (9.8 years, SD¼5.49) and PD patientswho do not (5.3 years, SD¼3.30) (t18¼2.22, p¼0.03).Gait velocityPD FOG had signiﬁcantly slower velocity (85.09 cm/s,SD¼37.38) on average compared with the PD non FOG group(126.98 cm/s, SD¼14.02) and the control group (148.79 cm/s,SD¼17.16) (F2,27¼18.419, p<0.05). Post hoc analysis revealedthat the PD FOG group walked signiﬁcantly slower than boththe PD non FOG (32% decrease, p¼0.0016) and control group(42.8% decrease, p<0.01). In contrast, no signiﬁcant differenceswere identiﬁed between the control and PD group. There was nosigniﬁcant difference between conditions for gait velocity.Step lengthA signiﬁcant main effect of group was found between the PDFOG (44.78 cm, SD¼17.64), PD non FOG (68.03 cm, SD¼8.77)and control group (74.83 cm, SD¼9.42) (F2,27¼16.32, p<0.01).Post hoc analysis conﬁrmed that participants who experienceFOG have signiﬁcantly smaller step lengths than both the PDand control group. The PD non FOG group did not signiﬁcantlydiffer from the control group with respect to step length. Asigniﬁcant interaction between group and condition illustratesthat PD FOG had signiﬁcantly smaller step lengths comparedwith the control and PD non FOG group when the light cue waspresent before gait initiation (F4,54¼2.56, p<0.05).Double support phaseIt was observed that the PD FOG group (0.498% GC, SD¼0.517)spends signiﬁcantly more time in double support phasecompared with PD non FOG (0.248% GC, SD¼0.066, p¼0.0017)and healthy controls (0.243% GC, SD¼0.163, p<0.0014)(F2, 27¼10.318, p<0.05). The PD non FOG group and the healthycontrol group did not differ signiﬁcantly from one another.Step-to-step variabilityWhen comparing groups, a main effect was identiﬁed(F2,27¼32.83, p<0.001). Post hoc analysis revealed that PD FOGhad signiﬁcantly more variability in their step length (5.54 cm,SD¼4.536) when compared with PD non FOG (3.05 cm,SD¼1.877, p<0.001) and healthy controls (2.90 cm, SD¼1.782,p<0.001). No signiﬁcant differences were found between the PDand the healthy control group.Interesting to note is the main effect of condition (ﬁgure 2). Inthe light cue before gait initiation condition (4.58 cm), participants had signiﬁcantly more variability in their step lengthwhen compared with the no light cue condition (3.52 cm) andthe light cue after initiation condition (3.38 cm) (F2,54¼11.267,p<0.001). Post hoc analysis conﬁrmed that when the light cuewas present before gait initiation, participants had more variability than both the no light condition (p¼0.001) and when thelight cue was present after gait initiation (p<0.001).A signiﬁcant interaction of step length variability was alsofound when comparing group and condition (F4,54¼3.035,p¼0.025) (ﬁgure 3). This interaction is driven by the PD FOGgroup, in which the group had signiﬁcantly higher variabilitywhen the light cue was present before initiation of gait condition (7.03 cm) than both no light cue (4.83 cm) and light cueafter initiation condition (4.77 cm). Post hoc analysis conﬁrmedthat the PD FOG group differed signiﬁcantly from both the PDnon FOG and control group when comparing between no lightcue and light cue after initiation conditions. The results indicatethat the PD FOG group was signiﬁcantly more variable whenthe light cue was present after gait initiation than the othergroups, and neither the PD non FOG group nor the healthycontrol group differed signiﬁcantly in variability as a result ofa light cue condition.Frequency of freezing episodesThe frequency of freezing episodes within the PD FOG groupwas obtained by observing each trial through video recordings. Ac2 analysis demonstrated a signiﬁcant group effect betweenconditions (c2¼10.059, DF¼2, p<0.01). Upon further examination, a c2 analysis conﬁrmed that the condition in which thelight cue was present after gait initiation (47.5%) had signiﬁcantly higher number of freezing episodes than no light cueFigure 2 Within trial step-to-step variability across conditions in PDFOG, PD non-FOG and healthy controls.Figure 3 Within trial step-to-step variability interaction betweengroups and conditions.100 J Neurol Neurosurg Psychiatry 2012;83:98e101. doi:10.1136/jnnp 2011 300869Movement disorders           (16.4%, c2¼9.935, p<0.002) and light cue before initiation(35.8%, c2¼4.308, p<0.05). In addition, having no light cueelicited signiﬁcantly less freezes than when the light cuewas present before initiation (c2¼5.876, p<0.02).DISCUSSIONThe primary objective of the study was to evaluate how gaitmight be inﬂuenced by a cued change in motor planning in PDFOG (compared with PD non FOG and healthy controls).Outcome measures included: step to step variability, steplength, velocity and double support time. The observable freezefrequency in conjunction with the previously mentioned gaitparameters demonstrated that cognitively altering a gait patternwith an additional attentional focus may have detrimentaleffects on gait in PD FOG.This is the ﬁrst study to show that freezers exhibit changes ingait parameters with an alteration of a movement plan. Thecurrent study found increased step to step length variabilitywithin the PD FOG group, and was more profound when thelight cue was present before gait initiation, suggesting that gaitadjustments were made in order to pass through the doorwaysafely. It is important to note that freezers were the only groupto illustrate this effect, demonstrating that increasing cognitivedemands may have a negative effect on gait in PD FOG patients.The results support the notion that when gait becomesabnormal and less automatic, gait asymmetry may rely oncognitive input and attention.11 The use of an intentional switchcue allowed for further testing of the hypothesis sinceresponding to a switch cue requires intentional control (requiringprefrontal activation) to initiate new motor set.12 14 If this werethe case, then we would expect greater interruptions of movement and more freezes when the light cue is present after gaitinitiation. Interestingly, increased step length variability and anincreased number of freezes were evident when the light cue waspresent before and after gait initiation conditions compared withno light cue condition. Most observable freezes when the lightcue was present after gait initiation condition occurred after thelight cue was presented, suggesting that an unexpected change inthe outcome or goal of a movement plan in PD FOG may alsoelicit freezing. These ﬁndings support Almeida et al in 2003, inwhich individuals with PD were unable to separate plans ofaction, which may be related to attention shifting deﬁcits whentransferring between different motor sets.10 14 17The results provide evidence that FOG may be inﬂuenced bydifﬁculty in processing a voluntary switch within a movementtask through executive function decline. Increased time indouble support phase, step to step variability, decreased velocity,step length and observed freezing episodes during the light cueconditions all support the implication that individuals withFOG alter their gait in response to a shift in attention whileswitching movement tasks and may trigger FOG episodes.PD patients were tested in their ‘ON’ state of medication asmentioned earlier to get an accurate understanding of thepotential effects during their everyday activities. Although thismay be a potential limitation to the study, previous researchindicates that FOG may be typically unresponsive to medication.18 Future studies may include patients in their ‘OFF’ stateto get an understanding of basal ganglia contributions to FOG inattentionally demanding situations. It is also important toconsider that our PD FOG group was slightly older (althoughnot signiﬁcantly), with longer disease duration and higher motorseverity as determined by the UPDRS. Thus, it is possible thatadvanced disease, or other differences between groups such ascognitive decline, depression and anxiety, might account for theperformance differences between groups. While it was not thefocus of this study to address these issues, future research shouldbe directed at examining these potential inﬂuences more thoroughly. The fact remains that the number of freezes, decrease instep length and an increased variability of step length wereall speciﬁcally inﬂuenced by condition in only the PD FOGgroup. Overall, the motor planning required to switch betweenmotor sets is an important factor that needs to be considered,since there is potential to develop new treatment strategies forindividuals with PD FOG.Acknowledgements We gratefully acknowledge the assistance of the lab teamand patients at the Sunlife Financial Movement Disorder Research and RehabilitationCentre, ON, Canada for their contributions to this research.Funding Patricia Knobl received support from Natural Sciences and EngineeringResearch Council of Canada. Dr Almeida received support from the Parkinson’s Societyof Canada for portions of the current research project. Support was also provided fromSun Life Financial, Natural Sciences and Engineering Research Council of Canada,Canadian Foundation for Innovation, Ontario Rehabilitation Research Advisory Networkand Wilfrid Laurier University’s Science & Technology Endowment Fund. The fundingsource had no role in the study design, data collection, analysis, interpretation of theresults, in the writing of the paper or decision to submit the paper for publication.Competing interests None.Ethics approval This study was approved by the Research Ethics Board at WilfridLaurier University.Provenance and peer review Not commissioned; externally peer reviewed.REFERENCES1. Giladi N, Fahn S. Freezing phenomenon, the fifth cardinal sign of Parkinsonism.Progress in Alzheimer’s and Parkinson’s Diseases, in Parkinson’s Disease, PlenumPress Division, Plenum Publishing Corporation, New York, NY 10013 Vol. 49,1998;329 35:888.2. Moore O, Peretz C, Giladi N. Freezing of gait affects quality of life of peoples withParkinson’s disease beyond its relationships with mobility and gait. Mov Disord2007;22:2192 5.3. Fahn S. The freezing phenomenon in parkinsonism. Adv Neurol 1995;67:53 63.4. Giladi N. Gait disturbances in advanced stages of Parkinson’s disease. Adv Neurol2001;86:273 8.5. Hausdorff JM, Schaafsma JD, Balash Y, et al. Impaired regulation of stridevariability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res2003;149:187 94.6. Giladi N, Mcmahon D, Przedborski S, et al. Motor Blocks in Parkinsons disease.Neurology 1992;42:333 9.7. Nieuwboer A, Dom R, De Weerdt W, et al. Abnormalities of the spatiotemporalcharacteristics of gait at the onset of freezing in Parkinson’s disease. Mov Disord2001;16:1066 75.8. Amboni M, Cozzolino A, Longo K, et al. Freezing of gait and executive functions inpatients with Parkinson’s disease. Mov Disord 2008;23:395 400.9. Almeida QJ, Lebold CA. Freezing of gait in Parkinson’s disease: a perceptual causefor a motor impairment? J Neurol Neurosurg Psychiatry 2010;81:513 18.10. Schwab RS, Chafetz ME, Walker S. Control of 2 simultaneous voluntary motor actsin normals and in parkinsonism. AMA Arch Neurol Psychiatry 1954;72:591 8.11. Yogev G, Plotnik M, Peretz C, et al. Gait asymmetry in patients with Parkinson’sdisease and elderly fallers: when does the bilateral coordination of gait requireattention. Exp Brain Res 2007;177:336 46.12. Geuze RH. Stability of bimanual coordination in Parkinson’s disease and cognitivemodulation of intention. Motor Control 2001;5:361 84.13. Scholz JP, Kelso JA. Intentional switching between patterns of bimanualcoordination depends on the intrinsic dynamics of the patterns. J Mot Behav1990;22:98 124.14. Almeida QJ, Wishart LR, Lee TD. Disruptive influences of a cued voluntary shift oncoordinated movement in Parkinson’s disease. Neuropsychologia 2003;41:442 52.15. Horstink MW, Berger HJC, Vanspaendonck KPM, et al. Bimanual simultaneousmotor performance and impaired ability to shift attention in Parkinsons disease.J Neurol Neurosurg Psychiatry 1990;53:685 90.16. Robertson C, Flowers KA. Motor Set in Parkinsons disease. J Neurol NeurosurgPsychiatry 1990;53:583 92.17. Talland GA, Schwab RS. Performance with Multiple Sets in Parkinsons Disease.Neuropsychologia 1964;2:45 53.18. Giladi N, Huber Mahlin V, Herman T, et al. Freezing of gait in older adults with highlevel gait disorders: association with impaired executive function. J Neural Transm2007;114:1349 53.J Neurol Neurosurg Psychiatry 2012;83:98e101. doi:10.1136/jnnp 2011 300869 101Movement disorders           

The Relationship Between Motor Planning and Freezing of Gait in Parkinson’s Disease

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The Relationship Between Motor Planning and Freezing of Gait in Parkinson’s Disease

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