Brain (1996), 119, 551-568

Stride length regulation in Parkinson's diseaseNormalization strategies and underlying mechanisms

Meg E. Morris,1-2 Robert Iansek,1 Thomas A. Matyas2 and Jeffery J. Summers3

1 Geriatric Research Unit, Kingston Centre, Cheltenham,the 2School of Physiotherapy and Behavioural HealthSciences, La Trobe University, Bundoora and the^Department of Psychology, University of SouthernQueensland, Toowoomba, Australia

Correspondence to: Meg Morris, Geriatric Research Unit,Kingston Centre, Warrigal Road, Cheltenham 3192,Australia

SummaryResults of our previous studies have shown that the slow,shuffling gait of Parkinson's disease patients is due to aninability to generate appropriate stride length and thatcadence control is intact and is used as a compensatorymechanism. The reason for the reduced stride length isunclear, although deficient internal cue production orinadequate contribution to cortical motor set by the basalganglia are two possible explanations. In this study we haveexamined the latter possibility by comparing the long-lastingeffects of visual cues in improving stride length with that ofattentional strategies. Computerized stride analysis was usedto measure the spatial (distance) and temporal (timing)parameters of the walking pattern in a total of 54 subjectsin three separate studies. In each study Parkinson's diseasesubjects were trained for 20 min by repeated 10 m walks setat control stride length (determined from control subjectsmatched for age, sex and height), using either visual floor

Keywords: Parkinson's disease; gait; basal ganglia; attention

markers or a mental picture of the appropriate stride size.Following training, the gait patterns were monitored (i) every15 min for 2 h; (ii) whilst interspersing secondary tasks ofincreasing levels of complexity; (Hi) covertly, when subjectswere unaware that measurement was taking place. Theresults demonstrated that training with both visual cues andattentional strategies could maintain normal gait for themaximum recording time of 2 h. Secondary tasks reducedstride length towards baseline values as did covertmonitoring. The findings confirm that the ability to generatea normal stepping pattern is not lost in Parkinson's diseaseand that gait hypokinesia reflects a difficulty in activatingthe motor control system. Normal stride length can be elicitedin Parkinson's disease using attentional strategies and visualcues. Both strategies appear to share the same mechanismof focusing attention on the stride length. The effect ofattention appears to require constant vigilance to preventreverting to more automatic control mechanisms.

Abbreviations: DS = double limb support; SMA = supplementary motor area

IntroductionDecreased stride length during walking is a hallmark ofidiopathic Parkinson's disease; however, its pathogenesis andresponse to treatment are poorly understood. The reducedstride size is a primary determinant of gait hypokinesia(reduced movement) which progressively worsens as thedisease advances. Because gait disturbance is associated withan increased risk of falls (Aita et ai, 1982) and lossof independence (Schenkman, 1992), considerable effort isdirected towards the treatment of walking in Parkinson'sdisease. Pharmacological therapy is particularly effective inthe early stages of the condition; however, with diseaseprogression, patients can experience motor fluctuations(Marsden, 1994) and the short-stepped walking pattern can

© Oxford University Press 1996

re-emerge. Physiotherapy has also been advocated for themanagement of gait disorders in Parkinson's disease (e.g.Banks and Caird, 1989; Formisano et ai, 1992; Schenkman,1992), although the development of optimal rehabilitationstrategies has been hampered by an inadequate understandingof the pathogenesis of stride length disturbance. As yet thereis no definitive treatment method for assisting patients toregulate the length of the stride throughout the course ofthe disease.

The results of our previous research on gait hypokinesia(Morris et al., 1994a) suggested that Parkinson's diseasesubjects have particular difficulty with the internal regulationof stride length, even though cadence (steps per minute)

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552 M. E. Morris et al.

control is intact and is easily modulated for a variety ofconditions (Morris et al., \994b). Parkinson's disease subjectsdo have a higher cadence rate than control subjects forany given velocity; however, the increased cadence is acompensation for reduced step size (Morris et al., ]994b).

The reason for the reduced movement amplitude inParkinson's disease has, however, not yet been fullyelucidated. An investigation by Berardelli et al. (1986)showed that upper limb movements in Parkinson's diseasewere hypometric and that reduced movement amplitudewas related to an abnormally low initial force of musclecontraction. However, they noted that patients couldintentionally match the required force in order to achieve thedesired movement amplitude, provided that sufficient timewas allowed. In another study on upper limb movement,Sheridan et al. (1987) found that Parkinson's disease subjectscould improve their movement amplitude and speed to normalvalues, although this occurred at the expense of movementaccuracy. Martin et al. (1994) also demonstrated thatParkinson's disease subjects could perform arm movements atcontrol amplitude if appropriately trained and could maintaincontrol values for each submovement in a sequence ofmovements, irrespective of external cues. The commonfinding in all of these investigations was that normalmovement size could be achieved in Parkinson's diseasegiven the appropriate conditions. In agreement with thissuggestion, our own experiments have shown that, althoughParkinson's disease patients typically walk with smaller steps,they can achieve the desired stride amplitude when providedwith visual cues (Morris et al., 1994a). Therefore, the normalfoot step pattern is not lost in Parkinson's disease, ratherthere is a problem in activating the correct stepping responsefor a given context.

In attempting to understand the reasons for the difficultyin generating appropriate stride length in Parkinson's disease,it is useful to consider recent investigations on thepathogenesis of hypokinesia. Studies on primates (Brotchieet al., 1991a, b) and individuals with Parkinson's disease(Georgiouefa/., 1993, 1994; Phillips et al., 1994; Cunningtonet al., 1995) suggest that in hypokinesia the interactionbetween the basal ganglia and supplementary motor area(SMA) is disrupted during movement performance. The SMAnormally prepares for a forthcoming predictable movementwith a steady increase in neuronal activity during thepremovement period. Once the external signal to moveoccurs, then neuronal activity in the SMA abruptly ceases(Mushiake et al., 1990). Brotchie et al. (1991a, b) foundthat, in primates, the basal ganglia discharge with brief burstsof phasic activity at the end of submovements performed ina sequence. They suggested that this activity represents aninternal cue which triggers the rapid drop in SMA neuronalactivity. The internal cue appears to be timed to ceasepremovement activity in the SMA for each submovement inwell-learned movement sequences; however, the phasic cueis not observed for novel or complex tasks (Brotchie et al.,1991a, b). Thus it appears that the basal ganglia interact with

the SMA for only learned movement sequences and it isthese sequences that require an internal cue to string thecomponents together. If the basal ganglia cue was absent ordisturbed, as in Parkinson's disease, then it is possible thatthe SMA preparatory activity would be disturbed, leading toan abnormally executed movement. In this situation theabnormal internal cue would impair preparation for eachsubmovement in the sequence and the abnormal submovementpreparation would result in an abnormally executedmovement. A normal cue or substitute cue delivered at theappropriate time could theoretically enhance preparatoryprocess and result in a more normal movement.

As well as a disorder of submovement preparation, thereduced amplitude of movement in Parkinson's diseasehypokinesia could result from a disorder of motor set for theentire movement sequence. A number of investigators havedemonstrated the presence of set related activity within thebasal ganglia nuclei (e.g. Mushiake et al, 1990; Brotchieet al, 1991a, b; Kimura et al, 1992). Neural networkmodelling also indicates that set related activity is necessaryfor running of movement sequences in addition to theprovision of internal phasic cues (Brotchie et al, 1991c). Inthe SMA, set related activity occurs in some neurons priorto predictable sequences of movement (Mushiake et al,1990). By contrast, other neurons discharge prior to eachsubmovement during the sequence. It has been proposed thatset related activity in the basal ganglia contributes to setrelated activity in the SMA occurring for whole movementsequences so as to maintain the entire sequence inpreparedness for running and execution (Iansek et al, 1995).This function could explain why individual movements inParkinson's disease are slow and underestimated in amplitude(e.g. Hallett and Khoshbin, 1980), as a deficient preparatoryprocess exists in Parkinson's disease due to the deficientcontribution from the basal ganglia.

This model of basal ganglia function suggests that gaithypokinesia in Parkinson's disease could relate to either adisturbance of motor set for whole movement sequences, orto disruption of the internal cue leading to difficulty instringing each submovement together as a result of defectivesubmovement preparation. The motor cortex plays a majorrole in execution of movements and abnormal motor set fora whole gait sequence could affect the ability to generatesufficient force to elicit a normal step for each componentof the sequence. On the other hand, absence of a phasic cueto move could result in impaired motor preparation, resultingin a shorter step, possibly because the preparation for thestep is not terminated at the appropriate locus of the gait cycle.

In considering which of these two motor control mechanismsunderpin gait hypokinesia, it is important to recount thatParkinson's disease patients have a fundamental disturbancein stride length regulation and that cadence control remainsintact (Morris et al., 1994 a, b). It becomes difficult to implicateabnormal cue production by the basal ganglia as the cause ofreduced stride length because the function of the internal cueis to string together submovements in a sequence precisely

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Stride length regulation in Parkinson's disease 553

(Iansek et al., 1995). In parkinsonian gait the submovementsappear to be strung together normally, as reflected by the findingthat patients retain the ability to modulate walking cadence(Morris et al., 1994b). We are therefore left with the hypothesisthat reduced stride length in Parkinson's disease may be dueto inadequate motor set for gait.

Clinically, a number of strategies have been used toenhance walking in Parkinson's disease. The most well-known method is the use of visual cues placed on the floorat the desired step length to assist with gait initiation andexecution (Quintyn and Cross, 1986; Bagley et al., 1991).According to Purdon Martin (1967), visual cues are necessaryto elicit the normal stepping response in Parkinson's diseaseand 'without seeing them [his] voluntary effort is of noavail'. External cues may thus have access to motor controlmechanisms which bypass the basal ganglia-SMA loop toenhance movement preparation for each step within thesequence. Alternatively, the cues might simply act to enhanceset for large strides by focusing the patients attention onwalking with criterion step length. From this viewpoint, otherclinicians have noted that visual cues are not always necessaryto facilitate movement and that attentional strategies such asmentally rehearsing the forthcoming movement sequencebefore it is performed, concentrating on the movement duringexecution, and avoiding dual task performance also improvethe gait pattern in Parkinson's disease (Quintyn and Cross,1986; Yekutiel et al., 1991; Morris et al., 1995; Morris andIansek, 1996). It is possible that attentional strategies facilitatea more normal locomotor pattern by enhancing motor set forthe entire gait sequence.

Because it is not yet clear whether stride length decrementsin Parkinson's disease are due to a disorder of motor set ordefective internal cueing, it has been difficult to structurerehabilitation strategies for gait hypokinesia on a rationalbasis. This problem is compounded by the paucity ofcontrolled clinical trials to evaluate the immediate andlonger-term effects of gait training in Parkinson's disease.Evaluations of attentional strategies (e.g. Quintyn and Cross,1986; Yekutiel et al., 1991; Morris et al, 1995) and cueingtechniques (Martin, 1967; Forssberg et al., 1984; Bagleyet al, 1991; Weissenborn, 1993) amount to only a handfulof anecdotal reports and single session studies.

The purpose of this series of experiments was to examinethe influence of motor set for the entire gait sequence on theregulation of stride length in Parkinson's disease bycomparing the effects of two training strategies on the spatialand temporal parameters of gait. In the first study, wecompared the effects of external cues with a specificattentional strategy to ascertain whether these two methodsused similar or different motor control mechanisms tonormalize stride length. The degree to which Parkinson'sdisease subjects could be trained to walk to control parametersusing each of the strategies was determined, and then weexamined the duration of normal gait once the strategieswere removed. In the second study we examined the effectsof a secondary task performance on the gait pattern following

training with either visual cues or the attentional strategy. Aseries of secondary verbal-cognitive tasks of increasing levelsof complexity were used to clarify whether the strategiesused attentional or non-attentional mechanisms in themaintenance of normal gait. In the final study, covertmonitoring of the gait pattern enabled further examinationof the extent to which attentional resources and socialmotivation provided by supervision enabled the gains fromvisual cue training to be retained. Collectively, the resultssuggested that maintenance of normal gait is possible inParkinson's disease for short time periods and the underlyingbasis for the sustained improvement is by the use of motorcontrol mechanisms which utilize attentional resources. Thesecontrol mechanisms appear to bypass the basal ganglia-SMAinteraction in order to enhance motor set for large strides forthe entire gait sequence.

MethodSubjectsA total of 54 subjects was recruited for the three studies.Twenty-seven subjects with idiopathic Parkinson's diseasewere recruited from the Kingston Centre, Australia and thesame number of age-, sex- and height-matched controls wererecruited from senior citizens groups in the Melbournemetropolitan region. In the first and second studies therewere 16 Parkinson's disease subjects and 16 control subjectsand in the third study there were eight Parkinson's diseasesubjects and eight control subjects. Some of the subjects inStudies Two and Three had also participated in Study One.The three studies were conducted at 2 month intervals.Subjects were required to provide informed consent accordingto the Helsinki declaration (1964). To be included, subjectsalso had to be able to walk 12 m up to 18 times over a 2 hperiod without a walking aid or assistance. Parkinson'sdisease subjects were only included if their diagnosis hadbeen confirmed by a neurologist.

Subjects were excluded if they had a past history ofneurological conditions other than Parkinson's disease orcardiorespiratory, orthopaedic or visual disturbance thatimpaired walking ability. Parkinson's disease subjects werealso excluded if they were on major tranquilizers, scored<24 out of 38 on the Short Test of Mental Status dementiatest (Kokeman et al, 1987) or if they had dyskinesia, asdetermined by the neurologist.

The final sample comprised 33 males and 21 females witha mean age of 73.4 years and an age range of 59-82 years.For all experiments, testing of the Parkinson's disease subjectscommenced 45—75 min post-Parkinson's disease medication,when they were judged by a neurologist or physiotherapistto be in the 'on' state. One subject (S.I.) could not completeall of the trials in Study One due to fatigue. The clinicalcharacteristics of the Parkinson's disease subjects as well astheir medication are summarized in Tables 1-3.

The control group for Study One consisted of nine menand seven women, with a mean age of 72.7 years (range 63-

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554 M. E. Morris et al.

Table 1 Parkinson's disease subject characteristics for Study One

Subject

123

4

5

6

7

8

9

10

11

12

13

14

15

16

Age(years)

816464

67

79

76

71

70

75

78

73

73

77

69

75

72

Sex

MFM

M

F

M

F

M

M

M

F

F

F

M

F

M

Height(m)

1.751.601.78

1.76

1.58

1.71

1.54

1.73

1.69

1.66

1.61

1.55

1.54

1.70

1.57

1.68

Weight(kg)

825381

79

60

68

49

70

65

66

64

60

57

70

56

70

Websterratings

161012

9

18

24

14

16

20

11

16

15

12

13

12

20

STMS*

323623

33

31

34

33

24

24

26

29

33

25

21

33

28

Medication

SinemetMadoparMadopar MMadopar HBSParlodelSinemetSinemet CRSinemetMadopar HBSMadopar MDomperidoneSinemetParlodelMotiliumSinemetParlodelMadoparSinemet CRMadoparSinemet CREldeprylParlodelMadoparSinemetSinemet CRSinemetSinemet CRSinemetParlodelMadopar HBSParlodelEldeprylMadoparSinemet CRMotilium

(mg day ')

600/150500/125100/25100/25151000/250200/501000/250300/75300/75201200/3007.560500/12512.5800/2002000/500900/225600/1505530OA75200/501200/300100/251800/450300/757.5400/1001551250/312.5200/5030

*STMS = Short Test of Mental Status.

82 years), a mean height of 1.65 m (range 1.51-1.8 m) andmean weight 68 kg (range 49—87 kg). The 16 control subjectsfor Study Two comprised nine men and seven women of agerange 6 3 - 8 1 years (mean 73.1 years), height range 1.45—1.8m (mean 1.66 m) and weight range 45—90 kg (mean 69 kg).For Study Three the control subjects comprised four menand four women of age range 5 9 - 7 7 years (mean 70.1 years),height range 1.53-1.82 m (mean 1.66 m) and weight range4 7 - 9 9 . 2 kg (mean 70.4 kg). Control subjects were healthyand had no history of neurological , orthopaedic orcardiorespiratory disorders.

ApparatusIn each of the three studies a computerized clinical strideanalyser (CSA) (B and L Engineering, Santa Fe Springs,Calif., USA) was used to measure the temporal (timing) andspatial (distance) parameters of the footstep pattern. Thesystem consists of a set of footswitches worn as innersolesinside the shoes, a microcomputer backpack for temporary

data storage and an IBM compatible personal computer.Details of the apparatus have been documented previously(Morris et al., 7994a). Data was collected on a 12 m gaitwalkway in the Geriatric Research Unit at the KingstonCentre, Australia. The walkway was tiled in grey linoleumand purposely included 5 m of open space at either end andon each side so that Parkinson's disease subjects did not feelthat they were walking in a confined space, which can triggermotor blocks. Visual cues used in each of the experimentsconsisted of white strips of cardboard which measured 1mmX50 mmX500 mm. The visual cues were placed on thegait walkway at a distance equivalent to the step length foreach Parkinson's disease subject's age-, sex- and height-matched control.

ProcedureThe overall procedure for gait analysis was the same foreach of the experiments. Footswitches were placed inside thesole of each shoe and attached to the microcomputer backpack

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Stride length regulation in Parkinson's disease 555

Table 2 Parkinson's disease subject characteristics for Study Two

Subject

1

23

4

5

67

8

9

10

11

12

13

14

15

16

Age(years)

76

7680

65

77

7181

82

70

68

75

81

71

72

64

76

Sex

M

MF

M

F

MM

F

M

M

F

M

F

M

M

F

Height(m)

1.71

1.701.51

1.52

1.54

1.681.70

1.60

1.73

1.75

1.57

1.69

1.54

1.68

1.78

1.69

Weight(kg)

68

8058

62

57

8580

57

70

82

56

72

49

70

81

70

Websterratings

24

1611

21

17

713

10

16

9

11

12

13

17

14

14

STMS*

34

2830

26

25

3032

28

24

30

33

32

33

28

23

26

Medication

Madopar MMotiliumMadoparSinemet MMadopar HBSEldeprylParlodelSinemet CRSinemet MParlodelSinemetSinemet CRSinemet MSinemet CRSinemetMadoparMotiliumSinemet CRParlodelMadoparSinemet CREldeprylSinemet CRSinemet CREldeprylMadopar HBSPergolideSinemetSinemet CRPergolideSinemetParlodelMotiliumSinemet CRMadoparMadopar MMadopar HBSParlodelMadopar Q

(mg day ')

30OA7560900/225100/10400/100515800/200100/1015250/25500/125500/50800/200150/37.5450/112.520500/12512.5600/150200/5010800/200300/7510400/100100 meg250/25800/200375 meg1250/1257.560200/50600/150100/25300/7515150/37.5

*STMS = Short Test of Mental Status.

storage unit, worn on a belt at the waist. A hand-held trigger

which was used to signal the start and end of each trial was

then attached to the backpack. For each gait, trial subjects

walked the full length of the 12 m walkway and data was

collected for the final 10 m of each walk. After each trial

the data was down loaded onto an I B M compat ible P C

and analysed using C S A software version 6 (B and L

Engineer ing) .

The primary dependent variables analysed were the gait

velocity (m min"1) , walking cadence (steps min"1) , mean

stride length (m) which is equal to the length of two

consecut ive steps, and the percentage of the gait cycle spent

in the double l imb support (DS) phase during which both

feet are in contact with the ground. Al though Park inson ' s

disease subjects can somet imes exhibit a forward flexed

posture and a plantargrade gait, these disorders were not

present in our subjects as reflected by the finding that none

of the subjects had a score > 2 on the posture or gait i tems

of the Webster (1968) scale.

The procedure , statistical analysis , results and a brief

discussion of the results of each study are next presented

separately, followed by a general discussion at the end of

the paper.

Study OneAim and procedureThe primary aim of the first study was to explore whetherthe effect of training Parkinson's disease subjects to walk tonormal gait parameters with external cues utilized a differentor similar mechanism to training Parkinson's disease subjects

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556 M. E. Morris et al.

Table 3 Parkinson's disease subject characteristics for Study Three

Subject Age(years)

Sex Height(m)

Weight(kg)

Websterratings

Medication (mg day ')

34

5

6

68

71

7669

75

75

64

70

M

FM

M

F

M

M

1.75

1.54

1.691.68

1.68

1.57

1.78

1.73

82

49

7070

65

56

81

70

13

1413

20

12

14

16

MadoparSinemet CREldeprylSinemetParlodelMotiliumMadopar QSinemetParlodelMadoparSinemet CRMadopar HBSParlodelEldeprylMadopar MMadopar HBSParlodelSinemetParlodel

600/150200/50101200/3007.560150/37.5300/757.5800/2002000/500400/100155100/25300/7515500/12512.5

to walk to normal gait parameters with a specific attentionalstrategy. This was addressed by measuring the extent towhich normal gait parameters were attained with the twotraining strategies and by measuring the duration ofmaintenance of normal gait once the training strategies wereremoved. The external cues were visual cues set on the floorat a distance equivalent to the mean stride length of eachParkinson's disease subject's age-, sex- and height-matchedcontrol. These floor markers were laminated strips of whitecardboard that measured 1 mmX50 mmX500 mm. For theattentional strategy, subjects were trained to focus theirattention consciously on walking with steps of the same sizeas their matched control. They were shown the optimal steplength by placing a tape measure and two white lines on thefloor at the desired distance and were instructed to 'try towalk with steps this size'. They were also instructed to standnext to the lines and to 'measure up' their step length priorto each trial until they had developed 'a mental picture ofthe correct step size'.

Prior to measurement of Parkinson's disease subjects,baseline data for the preferred gait pattern of control subjectswere collected for two trials spaced 2 min apart. The meandata for each of the parameters was used as a criterionagainst which Parkinson's disease performance could laterbe compared. These criterion parameters are represented asa dotted horizontal line on Figs 1-3. The criterion wasobtained in order to identify a normative standard againstwhich parkinsonian gait data could be interpreted. In concertwith the literature on human locomotion (e.g. Winter, 1991)we assumed that normal gait parameters in control subjectswould remain stable over brief durations, such as theexperimental 3 h period.

Study One comprised three experiments which documentedthe effects of visual cue training, attentional strategy training

TRAJMNQ(CUE8)

RETENTION (NO CUES)

SO SO 100 120 140 160

Jkm (min)

RETENTION (NO CUES)

Tima (min)100 120 140 160

2 0"

1.5-

1 0-

0.5-

BA3E1JNE

D-

• M M

TRW WHO(CUES)

RETENTION (NO CUES)

Tbne (min)100 120 HO

TRAWJNQ(CUES)

RETENTION (NO CUES)

20 40 60 SO 100 120 140 160

Fig. 1 Mean stride length, cadence, velocity and DS duration forthe Parkinson's disease group (closed circles) for baseline, visualcue training (cues) and retention phases, compared with thebaseline control values (open circle).

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Stride length regulation in Parkinson's disease 557

TRAMNQ(Ml

RETtNTCK (NO STRATEGY)

SO SO

Time (min)

150-

5 0 -

n-

BASB>E TWUHWG(AS)

RETINTIOH (HO STRAfEOY)

00 SOTime (min)

\jy-

OJ-

BAS£U«

*

TRAJMMQ(AS)

u' 60

RETBmON (HO STBATHJY)

>o ido ii> 1*0 160

Time (min)

so-

40-

S>0-

0

BAMLM TftAlMNQ(AS)

RETENTION {NO ffTRATWY)

I*1 "«C- " ^ ^ = - % * * • # • * • * " *

so so

Tlm*(niln)

Fig. 2 Mean stride length, cadence, velocity and DS duration forthe Parkinson's disease group (closed circles) for baseline,attentional strategy training and retention phases, compared withthe baseline control values (open circle).

and an extended baseline condition without training. Thethree experiments were conducted on separate days over a9-week period, with average intervals of 3 weeks betweeneach experiment. To control for series effects, the order oftesting for the three experiments was randomized for all ofthe subjects. For the visual cue condition, baseline datawere first collected every 2 min for a 20-min period. Theinstructions for baseline measurement trials were simply to'Walk to the end of the walkway'. Visual cues spaced at themean stride length of each Parkinson's disease subject'sassigned control were then placed on 10 m of the walkwayand subjects were instructed to 'Step over the markers andwalk to the end of the walkway'. Trials of visual cue walkingwere performed at 2-min intervals for 20 min to completethe training programme and measures of gait performancewere obtained simultaneously. Finally, in the retention phasesubjects performed two gait trials every 15 min for 2 h.Subjects were instructed to 'Walk to the end of the walkway'.Between trials subjects sat in a chair and rested.

For the attentional strategy condition Parkinson's diseasesubjects were again first tested under baseline conditionsevery 2 min for 20 min. Then they were familiarized withthe target stride length using the attentional strategy outlined

oo-

W l -

0 _

BASSJKE

60-

1.3

10

0.5

40-

20-

(1

BASELINE

?-

BABEUNE

BA8ELME

BASZLKE

20

BASELINE

20

BASELM

120

BASSJHE

40

40

40

60

SO

1SO

BASELME

SO 100 120

Ttne (mtn)

BASEUTC

1 1 1SO 100 120

Tina (min)

BASELHE

SO 100 120

Tlm«(m(n)

BASELINE

140

140

140

- - 0

ISO

- - 0

ISO

- - O

ISO

- - -o

20 40 00 80 100 120 140

Fig. 3 Mean stride length, cadence, velocity and DS duration forthe Parkinson's disease group (closed circles) and the controlgroup (open circle) for baseline conditions.

above. Parkinson's disease subjects performed gait trialsevery 2 min for 20 min during which they were instructedto focus their attention on walking with the criterion stridelength. Between each of the intervention trials they were re-familiarized with the criterion. To determine retention oftraining, subjects were then tested twice every 15 min for 2h without re-exposure to the criterion stride length. Betweentrials, subjects sat in a chair and rested.

One final condition, an extended baseline, was incorporatedinto Study One to investigate the temporal stability of thegait pattern in Parkinson's disease. The spatial and temporalparameters of gait were measured every 2 min for 40 minand then twice every 15 min for 2 h. During these 10 m gaittrials subjects were instructed to 'Walk to the end of thewalkway' and between each trial they were instructed to sitdown and rest.

Statistical analysisTime series analysis was used to test for change in Parkinson'sdisease gait parameters across each condition, given that thedata could be fitted using a linear model. Regression analysesand confidence intervals were used to examine for statisticallysignificant differences between gait parameters for baseline,

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558 M. E. Morris et al.

Table 4 Means and 95% confidence intervals (in brackets) for gait velocity, stride length, cadence and DS duration forpreferred walking in control subjects and for baseline, visual cue training and retention conditions in Parkinson's diseasesubjects

Parkinson's disease

Parameter Control Baseline VisuaJ cues Retention

Velocity (m min ')

Stride length (m)

Cadence (steps min"1)

DS (% gait cycle)

73.7 (67.8-79.5)

1.31 (1.23-1.39)

112.2(107.8-116.6)

31.7 (29.7-33.8)

49.7 (49.4-50.0)

0.% (0.95-0.97)

1044 (103.8-105.0)

35.9 (35.6-36.2)

72.2 (70.7-73.7)

1.30(1.30-1.31)

108.5 (104.9-112.0)

30.2 (29.5-30.9)

76.2 (75.8-76.7)

1.30(1.29-1.30)

116.9(115.8-117.9)

31.0(30.8-31.3)

intervention and retention phases. After linear fits of eachphase, the slope and phase transition intercepts were used ina series of planned comparisons using the t test for correlatedsamples. Because the linear models in each condition wereconsistently found to have zero slope, and because there wasno evidence of serial dependence on computing individualautocorrelograms for lags 1-5 (Box and Jenkins, 1976), themean performance for each of the phases could be comparedby computing 95% confidence intervals. The presence ofdifferent inter-trial intervals from trials 23 onwards wasaccommodated in the linear regression by using exact startingtimes for the abscissa and by confining the estimation ofautocorrelograms to the first 20 points which were spaced ateven inter-trial intervals.

ResultsFigure 1 illustrates the mean time series for baseline stridelength, cadence, velocity and double limb support durationfor preferred walking, visual cue gait and retention trials inthe Parkinson's disease group, compared with the criteriongait pattern for preferred walking in the control group. Thefigure shows that during the baseline phase Parkinson'sdisease subjects walked with a short-stepped, slow velocitygait pattern and the percentage of the gait cycle spent indouble limb support duration was increased relative to normal.Analysis of the residuals from the linear model for the baselinedata showed no statistically significant autocorrelation forany of the Parkinson's disease subjects, indicating stabilityof performance. Figure 1 also shows that visual cue trainingled to normalization of the gait pattern in Parkinson's diseaseand the effects of training were retained for a 2 h period.

Table 4 summarizes the 95% confidence intervals for eachof the gait parameters for preferred walking in the controlgroup as well as the 95% confidence intervals for baseline,visual cue walking and retention trials in the Parkinson'sdisease group. Planned comparisons revealed a significantdifference in Parkinson's disease stride length, cadence,velocity and DS from baseline to intervention phases, yet nosignificant change in the walking pattern from interventionto retention phases. For stride length, the mean intercept forParkinson's disease baseline performance (0.96) obtained onregression analysis was significantly different at the phase

transition from the intervention intercept (1.33) [?(14) = 13.2,P = 0.0001] even though the difference in slopes acrossphases was not statistically significant (-0.0005 comparedwith -0.0008). The retention phase stride length intercept(1.30) and slope (-0.0001) were not significantly differentfrom the intervention phase intercept and slope. The resultsfor Parkinson's disease velocity and DS closely mirrored thetrends for stride length. There was a significant increase invelocity intercept from baseline (49.8) to intervention phases(63.8) [r(14) = 4.7, P = 0.001] and a significant decrease inDS intercept from baseline (35.7) to intervention phases(27.4) [f(14) = ^ . 7 , P = 0.001), although no significantchange in the parameters from intervention to retentionphases occurred. In contrast, the differences in cadence slopeand intercepts from baseline to intervention phases andfrom intervention to retention phases were not statisticallysignificant.

Figure 1 also illustrates that Parkinson's disease stridelength for the baseline phase was significantly less than forthe control group [f(14) = -12.82, P = 0.0001], as wasvelocity [/(14) = -8.99, P = 0.0001]. However, thedifference between groups for cadence and DS at baselinewas not statistically significant. Visual cues elicited normalgait velocity, cadence, stride length and DS duration in themajority of subjects. As illustrated by Fig. 1, none of theparameters were significantly different from normal undervisual cue conditions. The figure also shows that duringthe retention phase, these parameters were not statisticallydifferent from criterion.

One of the unexpected findings of Study One was thatgait training using an attentional strategy produced similarresults to visual cue training (Fig. 2). This finding is detailedin Table 5 which lists 95% confidence intervals for each ofthe gait parameters for preferred walking in the control groupcompared with the 95% confidence intervals for baselinewalking, attentional strategy walking and retention trials inthe Parkinson's disease group. On regression analysis it wasapparent that the baseline Parkinson's disease stride lengthintercept (0.98) was significantly different from theintervention intercept (1.32) [r(14) = 5.5, P = 0.001] eventhough the difference in slopes across phases was notstatistically significant [-0.001 compared with 0.0003). Theretention stride length intercept (1.33) and slope (-0.0002)

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Table 5 Means and 95% confidence inten>als (in brackets) for gait velocity, stride length, cadence and DS duration forpreferred walking in control subjects and for baseline, attentional strategy training and retention conditions in Parkinson'sdisease subjects

Parkinson's disease

Parameter Control Baseline Attentional strategy Retention

Velocity (m min ')

Stride length (m)

Cadence (steps min~')

DS (% gait cycle)

73.7 (67.8-79.5)

1.31 (1.23-1.39)

112.2 (107.8-116.6)

31.7 (29.7-33.8)

52.3 (51.9-52.6)

0.97 (0.96-0.98)

107.4(106.9-108)

35.9 (35.6-36.3)

71.4(70.1-72.7)

1.32 (1.32-1.33)

110.5 (108.7-112.4)

29.9 (29.6-30.3)

75.5 (74.3-76.7)

1.33 (1.32-1.34)

115 (114.3-115.8)

29.7 (29.4-30.1)

were not significantly different from intervention. Similarly,there was a statistically significant increase in the Parkinson'sdisease velocity slope from baseline (52.4) to intervention(64.1) [t{ 14) = 3.9, P = 0.001 ] and a decrease in DS interceptfrom baseline (35.6) to intervention trials (30.6) [/(12) =-3.68, P = 0.01], although no significant difference fromintervention to retention trials was evident. For cadence, thedifferences in slope and intercept from baseline to interventionand from intervention to retention phases were not statisticallysignificant.

Figure 2 also illustrates that the Parkinson's disease stridelength for the baseline phase was significantly less than thecontrol group [r(14) = 10.2, P = 0.0001], as was velocity[/(14) = -6.2, P = 0.0001]. Moreover, DS was significantlygreater in the Parkinson's disease group than the controlgroup in the baseline phase [f(12) = 2.2, P = 0.05]. However,the difference between groups for cadence at baseline wasnot statistically significant. The attentional strategy producednormal gait velocity, cadence, stride length and DS durationin the majority of subjects. As shown by Fig. 2, duringattentional strategy training the Parkinson's disease stridelength, velocity, cadence and DS were not significantlydifferent from normal. Figure 2 also shows that duringthe retention phase these parameters were not statisticallydifferent from criterion.

Figure 3 depicts gait performance for the extended baselinecondition. The time series shows considerable stability overthe testing period and the data appeared to fit a linear modelwell. Analysis of the residuals from the linear model showedno statistically significant autocorrelation for any of theindividual Parkinson's disease subjects. In addition the meanslope and intercept values from regression analyses for theParkinson's disease group showed no significant changesbetween baseline and intervention phases or betweenintervention and retention conditions. Across all three phases,the mean intercept for Parkinson's disease stride length was0.95 and the mean slope was 0.004. The mean intercept forParkinson's disease cadence was 103.3 and the slope was0.002. The mean intercept for Parkinson's disease velocitywas 48.27 and the slope was 0.02. Finally the mean interceptfor Parkinson's disease DS was 35.36 and the mean slopewas 0.004.

For the extended baseline condition, group comparisons

revealed statistically significant differences between theParkinson's disease and control group for all four dependentvariables in each of the three phases. The 95% confidenceintervals for the complete time series for stride lengthwas only 0.945-0.963 m in the Parkinson's disease groupcompared with 1.24-1.39 m in the control group. In addition,the 95% confidence intervals for cadence for the Parkinson'sdisease group were only 103.2-104.2 steps min"', comparedwith 107.4-115.9 steps min"' in the control group. The 95%confidence intervals for mean velocity in the Parkinson'sdisease group (49.0-50 m min"1) also indicated that velocitywas substantially less than for controls (68.2-79.0 m min"').Mirroring the velocity results, the 95% confidence intervalsfor DS duration in the Parkinson's disease group (35.7-36.6% gait cycle) showed that DS was greater in Parkinson'sdisease subjects than controls (29.5-33.5% gait cycle).

DiscussionThree key findings emerged from Study One. The first wasthat visual cue training was effective in enhancing stridelength regulation in Parkinson's disease. This training effecttransferred to walking without visual cues and led tonormalization of stride length, velocity, cadence and DSduration for at least 2 h. The positive finding in relation tovisual cue training is consistent with previous reports in theliterature (Martin, 1967; Forssberg et ai, 1984; e.g. Bagleyet al, 1991; Morris et al., 1994a, b) which have detailedimmediate performance effects with floor markers. Thisinvestigation demonstrated that exposure to visual cuesproduces more lasting changes in the walking pattern whichoccurred even when the cues were removed.

The second key finding was that training using anattentional strategy, whereby Parkinson's disease subjectsdeveloped a mental picture of the criterion stride size andconsciously focused on walking with that stride size, producedresults that were strikingly similar to visual cue training. Theeffects of the attentional strategy also lasted for at least 2 hafter training ceased. Therefore the use of visual cues is notthe only strategy that is a useful adjunct to pharmacologicaltherapy for gait hypokinesia in Parkinson's disease. Specificattentional strategies appear to be useful in the enhancementof gait performance in Parkinson's disease. Given the practical

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560 M. E. Morris et al.

requirements for visual cue training, particularly the lack ofportability of this treatment method, attentional strategiesmight be a useful alternative for people who do not havesevere cognitive impairment, which could limit ability todevelop a mental representation of the target stride amplitude.

A third rinding was that the gait pattern of medicatedParkinson's disease subjects remained stable over a 2.5 hperiod (refer to Fig. 3). This finding, which appears to beone of the first published report of Parkinson's disease gaitstability over an extended period, seems to be contrary tothe commonly held belief that Parkinson's disease subjectsexhibit marked motor fluctuations, depending on medicationstatus and duration of Parkinson's disease (Marsden et al.,1982; Klawans, 1986). For example, Wall and Turnbull(1992, pp. 57-8) noted that 'as the disease progresses therelief obtained [from medication] becomes less predictableand walking becomes affected. The gait profile of the patientduring this stage is unpredictable; there is considerablevariability between patients at similar stages of the diseaseand in the same patient from hour to hour and day to day'.However, the locomotor stability in our Parkinson's diseasesample might have been enhanced by the exclusion criteria.Those with marked dyskinesia were excluded (a total of fivepotential subjects), and these people might have exhibitedmore marked fluctuations across time. Moreover, only peoplewho could perform repeated 10 m gait trials were included,and testing occurred when they were in the 'on' phase ofmedication, rather at the beginning or end of dose.

The results of Study One also raise important questionsregarding the mechanism of action of visual cue training.The traditionally held view was that visual cues enhance thelocomotor pattern in Parkinson's disease by triggering eachstep in the sequence (for example, see Martin, 1967).However, this explanation does not account for why theeffects of training persist for 2 h despite removal of the cuesduring the retention period. An alternative explanation is thatthe repeated performance of normal gait with cues enhancesthe motor set for the gait sequence, which in turn enhancesthe gain of the motor system for normal stride length. Thusthe repeated performance of the same motor pattern mightenable the pattern to be maintained after removal of the cues.The other possibility is that external cues may simply drawattention to the correct stride length, thereby increasing thestep size. This concept is strengthened by the finding thatthe attentional strategy also elicited normal gait parametersand enabled subjects to maintain the improvement withoutre-exposure to the criterion stride size. The similarity inbehaviour type and duration of effect post training for visualcues and the attentional strategy suggests that both strategiesmight share a similar mechanism, which may bypass thebasal ganglia—SMA interaction.

In the second study we tested this latter hypothesis byinvestigating the effects of secondary task performance onmaintenance of the gait pattern in the retention periodfollowing training. It seems plausible that use of a secondarytask removes attentional mechanisms from the most automatic

movement (gait) and directs them to the attention requiringtask (in this case a cognitive task) (see Dalrymple-Alfordet al., 1994). The result is that the automatic task wouldlikely use the basal ganglia-SMA interaction and thus gaitparameters should deteriorate. In contrast, if visual cuessimply act to 'trigger', successive steps within the sequence(i.e. to substitute for the disordered phasic basal ganglia cue)then no deterioration in gait parameters would be expectedon performance of a secondary task.

Study TwoIn this study we examined whether visual cues training andattentional strategy training had similar or different effectson gait by examining the effects of secondary taskperformance on the walking pattern during the retentionphase following training. The concept of attention is difficultto operationalize, however, for the purposes of thisinvestigation we defined attention as a limited capacityfor processing information from either memory or externalsources. Schmidt (1983, p. 133) argued that attention can beindexed by 'the degree of interference between two tasks'.In line with this viewpoint, we predicted that if attention wasdirected towards a secondary task following training, thenthe stride length would revert to baseline levels. It was alsopredicted that when the secondary task was withheld, stridelength would revert to criterion levels because the patientwould be able to direct attention back to the footstep pattern.Finally, we predicted that changes in cadence would notbe significantly different from normal because the internalregulation of cadence is not defective in Parkinson's disease(Morris et al., \994b).

ProcedureTwo experiments, conducted on consecutive days, wereperformed for Study Two. In the first experiment, we collectedtwo trials of baseline data for each Parkinson's disease subjectand then 10 trials of visual cue training followed by tworetention trials where the cues were removed and subjectswere instructed to 'walk to the end of the walkway'. Fourgait trials were then performed concomitant with a series ofsecondary cognitive tasks of graded levels of attentionaldemand. The 10 m gait trials were conducted every 2 minalthough subjects could request a longer duration rest ifrequired. During secondary task performance, subjects wereinstructed to walk normally whilst they concentrated onreciting a sentence. The Parkinson's disease data werecompared with a normative standard set by control subjects,represented by a horizontal line on the figure. The line wasobtained as a criterion level based on the average of twotrials of preferred gait, conducted 2 min apart.

In the second experiment in Study Two, which wasperformed the following morning, the same procedure wasused except visual cue training was replaced by trainingusing the attentional strategy previously described. The order

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Stride length regulation in Parkinson's disease 561

Table 6 Means and 95% confidence intervals (in brackets) for gait parameters for the control group (criterion) andParkinson's disease group under each of the secondary task conditions (T1-T4) following visual cue training

Parkinson's disease

Parameter Criterion Tl T2 T3 T4

Velocity (m min ')

Cadence (steps min"1)

Stride length (m)

DS (% gait cycle)

72.65 (66.9-78.4)

112.8 (108.1-117.5)

1.29(1.22-1.36)

32.2 (29.6-34.9)

70.8 (65-76.7)

114.7(108.9-120.6)

1.23 (1.16-1.30)

32.45 (29.3-36.5)

65.4 (59.6-71.2)

111.3 (105.4-117.1)

1.18 (1.09-1.26)

34.4 (32.3-36.5)

58.4 (52.7-63.2)

108.9(102.8-114.9)

1.07 (0.98-1.16)

35.3 (33.5-37.1)

56.3 (49.5-63.2)

104.2(97.6-110.5)

1.05 (0.95-1.15)

35.7 (33.4-38)

of experiments (visual cue training or attentional strategy)was counterbalanced using a Latin square design in order tocontrol for series effects. In a similar way, the order ofpresentation of secondary cognitive tasks in both studies wasrandomized to control for the effects of fatigue, practice andhistorical variables.

Further data was collected for eight of the control subjectswho walked at their preferred gait and under each of thesecondary task conditions. The purpose of collecting thisdata was to ascertain whether the gait patterns of healthyelderly people remain stable when they perform dual tasksof increasing levels of complexity. These control subjectscomprised four men and four women of age range 59-77years (mean 70.1 years), height range 1.53-1.82 m (mean1.66 m) and weight range 47-99.2 kg (mean 70.4 kg).

The secondary tasks used in Study Two were three itemsselected from the Benton and Hamsher (1983) sentencerepetition stimuli and one additional cognitive task. TheBenton and Hamsher stimuli provide a selection of verbaltasks with increasing levels of complexity that presumablyplace increasing levels of demand on the attentional system.For the easiest secondary task (Tl), subjects were asked torecite repeatedly, 'Where is the child?' as they walked. Thesecond level of complexity (T2) was to recite repeatedly,'Work in the garden until you have picked all the beans'.The third task (T3) was to recite, "The members of thecommittee have agreed to hold their meeting on the firstTuesday of each month'. In the most difficult cognitive task(T4) subjects were requested to repeat the days of the weekbackwards as they walked.

Statistical analysisThe strategy for data analysis for Study Two was similar tothe first study. Visual inspection of the individual data foreach subject confirmed that the trends in baseline andintervention stages in Study Two were very similar to thetrends in baseline and intervention stages in Study One.Because a linear model was appropriate for the data in eachphase, means and 95% confidence intervals for stride length,velocity, cadence and DS duration could be calculated foreach of the conditions for the experimental group and thencompared with the criterion values established for the controlgroup. A series of planned comparisons employing the /

statistic for correlated samples was used to address thefollowing key issues: (i) whether there was a statisticallysignificant difference between the Parkinson's disease groupand criterion for baseline gait, visual cue gait, retentionperformance and secondary task performance following visualcue training; (ii) whether there was a statistically significantdifference between the Parkinson's disease group and criterionfor baseline gait, attentional strategy gait, retentionperformance and secondary task performance followingattentional strategy training.

ResultsFigure 4 shows the mean values for stride length, cadence,velocity and DS in the Parkinson's disease group comparedwith the control group for the visual cue training study. Assuggested by the figure, in the baseline phase there was astatistically significant difference between the groups forstride length [f(14) = 8.9, P = 0.0001], velocity [r(15) =8.62, P = 0.0001], cadence [/ (15) = 3.09, P = 0.007] andDS duration [r(15) = -2.67, P = 0.017]. However, for visualcue training and the retention tests (Rl, R2, R3) there wasno significant difference between groups for any of thedependent variables.

During secondary task performance following visual cuetraining, significant changes in stride length and velocitywere obtained (Table 6). For the easiest secondary task (Tl)where subjects simply repeated 'Where is the child' as theywalked, the results for stride length for the Parkinson'sdisease group were not significantly different from thepreferred gait of controls. However, the mean stride lengthfor the Parkinson's disease group was less than criterion forT2 [r(14) = 2.66, P = 0.02], T3 [/(15) = 5.51, P = 0.0001]and T4 [f(15) = 5.88, P = 0.0001]. Likewise, the meanvelocity for the Parkinson's disease group was significantlyless than normal forT2 [f(14) = 3.11,/' = 0.008], T3 M15) =5.47, P = 0.0001] and T4 [/(15) = 5.17, P = 0.0001]. Incontrast, the mean cadence for the Parkinson's disease groupwas not significantly different from criterion at Tl, T2 orT3, even though it was significantly slower than the controlgroup at T4 [t(\5) = 3.12, P = 0.007].

Of note, the reduction in stride length and velocity overthe secondary task conditions was proportional to thecomplexity of the secondary task. In addition, when

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Table 7 Means and 95% confidence intervals (in brackets) for gait parameters for the control group (criterion) andParkinson's disease group under each of the secondary task conditions (T1-T4) following attentional strategy training

Parkinson's disease

Parameter Criterion Tl T2 T3 T4

Velocity (m min"1) 72.7 (66.9-78.4)

Cadence (steps min"1) 112.8 (108.1-117.5)

Stride length (m) 1.29 (1.22-1.36)

DS (% gait cycle) 32.2 (29.6-34.9)

73.6 (66-81.2)

114.5 (107.4-121.6)

1.28 (1.20-1.35)

31.2 (28.3-34)

70.7 (62.6-78.8)

112.6(105.7-119 6)

1.25 (1.16-1.33)

31.4(28.8-34.1)

64 (55.4-66.9)

111.1 (103.8-118.5)

1.15 (1.05-1.24)

32.9 (30.2-35.7)

58.9 (50.9-66.9)

106 (99 4-112.7)

1.10(1.00-1.20)

33.4 (30.8-36)

(Order randomized)

ISO

100-

50-

B

r—•-

Visual Cuts

<i " * • • *

R1 Secondary Task

(Order randomized)

T1 T2 T3 T4

R2

J»-e-

H3

-e-f,

B Visual Cues R1 Stcondaiy Task R2 R3

? 0.5-

(Oder randomized)

T3 T4

B Visual Cues fll Secondary Task R2 B3

(Order randomized)

Tl T2 T3 T4

B VHmdCuo Ri Secono»ry Task R2 R3

Fig. 4 Mean stride length, cadence, velocity and DS duration forthe Parkinson's disease group (closed circles) for baseline, visualcue training, secondary task and retention (R) phases, comparedwith the baseline control values (open circle).

Parkinson's disease subjects ceased the secondary tasks andperformed retention trials, all of the gait parameters revertedto values that were not significantly different from criterion.

In the second experiment in Study Two we replicated theprocedure except that the visual cues were replaced bytraining with the attentional strategy described in Study One(Table 7). As shown in Fig. 5, the results closely approximatedthose illustrated in Fig. 4. The main findings can besummarized as follows. For baseline walking there was astatistically significant difference between Parkinson's diseasesubjects and controls for stride length, cadence, velocity andDS. With the attentional strategy the means for the Parkinson'sdisease group for all dependent variables were not

(Order randomized)

150-

100-

B Amnttonel Strategy R l Secondary Task

(Order randomized)

- e a mT1 T! I J '

ra

j» e

R3

AoviUoivJ Strategy Ttak R2 R3

> 1 -

0 J -

(Ottor randomized)

T3 n

B AMnkKul Snta«y R1

(Order mndomtzed)

ri" "T? "

Aaansorwl Sbatogy Secondary Task

Fig. 5 Mean stride length, cadence, velocity and DS duration forthe Parkinson's disease group (closed circles) for baseline,attentional strategy training, secondary task and retention (R)phases, compared with the baseline control values (open circle).

significantly different from normal. At Tl the differencesbetween the Parkinson's disease group and controls for thefour gait variables did not reach statistical significance.However, there was a significant difference between groupsfor mean stride length at T2 [r(15) = 2.27, P = 0.04], T3[r(14) = 5.07, P = 0.0002] and T4 [f( 15) = 4.9, P = 0.0002].The mean Parkinson's disease velocity at T3 was alsosignificantly different from controls [t{ 14) = 3.35, P = 0.005]as was the mean Parkinson's disease velocity at T4 [r(15) =4.72, P = 0.0003]. However, the differences in cadence andDS between the Parkinson's disease group and the controlgroup did not reach statistical significance for T1-T4.

For the eight control subjects who performed the secondarytask conditions, there were no significant differences in any

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Table 8 Means and 95% confidence inten>als (in brackets) for gait parameters for eight control subjects for preferred gait,secondary tasks (T1-T4) of progressive difficulty and covertly monitored gait

Parameter Preferred gait Tl T2 T3 T4 Covert

Velocity Cm min ')Cadence (s>leps min"1

Stnde length (m)DS (% gait cycle)

82.9(73.8-91.9) 84.7(72-97.4) 83.4(70-5-96.3) 84.4(71.5-97.2) 78.9(68.7-89.2) 83.17(70.5-95.8)) 116.7(110.9-122.4) 117.1(107.8-126.5) 116.6(106.6-126.5) 117.5(109.1-125.8) 113.8(104.4-123.2) 117.8(109.7-125.9)

1.42(1.3-153) 1.44(1.30-1.58) 1.42(129-1.55) 1.43(1.27-1.59) 1.38(1.28-1.49) 1.4(1.27-1.54)31.9(28.4-35.4) 31.3(27.8-34.9) 31.7(27.6-35.8) 32.3(27 8-36.8) 32.3(28.3-36.2) 31.13(27.1-35.1)

of the gait parameters from preferred walking to Tl, T2, T3or T4 (see Table 8).

DiscussionThe main finding of Study Two was that secondary taskperformance during the period following training led to adecrement in Parkinson's disease stride length and velocitythat was proportional to the complexity of the task performed.However, the changes in Parkinson's disease cadence fromthe training phase to the secondary task phase were notstatistically significant, except for the most difficult task, T4.This effect was seen for both visual cues and the attentionalstrategy, suggesting that both strategies may normalize gaitby using similar mechanisms. During secondary taskperformance, one task is theoretically relegated to automaticcontrol whilst attention is directed to the other. WhenParkinson's disease subjects focused their attention on recitingsentences from the Benton and Hammer (1983) battery thewalking pattern deteriorated, presumably because it wasrelegated to automatic control processes which involve thebasal ganglia-thalamo-cortical circuitry and this circuitry isdefective in Parkinson's disease. In two Parkinson's diseasesubjects (S9 and S10) the degree of interference for the mostdifficult cognitive task was so disabling that they experiencedmotor blocks midway through some of the gait trials andcould not complete the test due to severe 'freezing'. Thefinding that the degree of performance deficit was proportionalto the difficulty of the secondary task suggests thatimprovements with training were largely due to an increasein attention on the criterion stride length, which led tonormalization of the other gait parameters. The findings arein agreement with previous studies on Parkinson's diseasewhich have shown that performance declines during dualtask conditions (e.g. Schwab et al, 1954; Talland andSchwab, 1964; Brown and Marsden, 1991; Dalrymple-Alfordetal., 1994).

Control subjects also showed a slowing of the walkingpattern accompanied by a small reduction in stride lengthand cadence in the most difficult secondary task conditions(Table 8). However, for the control group the changes in gaitparameters from preferred walking to the secondary taskconditions were not statistically significant.

Another finding of interest was that gait performance onthe second day of testing had reverted to baseline conditionsfor all Parkinson's disease subjects following bothrehabilitation methods. The reason why patients did not use

their newly acquired attentional strategy in order to generatea normal gait pattern the next day remains unclear, althoughit is interesting that our subsequent clinical observationsindicated that patients can generate the learned pattern thenext day when prompted to do so. Hence, our clinicalimpression is that patients can leam an attentional strategyfor walking more normally and can elect to use this strategywhen there is an external demand to do so, yet when left toself monitor their walking they tend to revert to a typicalhypokinetic gait pattern.

The results of Study Two also lend some support to ourhypothesis that visual cues act to enhance the gait pattern bydirecting attention to the criterion stride length rather thanby triggering sub-movements in a sequence. This conclusionis based on three main observations. First, during the retentionphase of Experiment One a normal gait pattern could begenerated even though visual cues were unavailable to'trigger' stepping. Secondly, the results for the cuesexperiment and the attentional strategy experiment were verysimilar, suggesting that similar underlying motor controlmechanisms might be responsible for the changes observed.Thirdly, when attention was apparently placed on a secondaryspeech task following visual cue training, gait performancedeteriorated. A plausible explanation for all of these findings isthat visual cue training enhanced stride length in Parkinson'sdisease by focusing attention on the criterion step size.

Alternatively, it could be argued that deterioration in gaitperformance during dual task conditions resulted from non-attentional mechanisms. Speech tasks, such as those used inthe present investigation, might interfere with gaitperformance because they share a common timing mecha-nism, or because the timing of locomotion entrains to thenatural speech rhythm. There is some evidence to suggest apredisposition for the rhythmicities evident in cyclical actionssuch as walking to become synchronized with the naturalrhythm of speech, either because there is a coupling betweenneural oscillators or because there is a central timingmechanism that regulates both actions (Summers and Burns,1990). Because the present investigation did not incorporatemeasures of speech performance for each secondary taskcondition, this possibility cannot be discounted. However,the finding that control subject's gait performance did notshow significant change according to the complexity of thespeech task condition reduces the strength of this line ofargument. Furthermore, secondary task performance has beenused in non-speech domains in Parkinson's disease and hasbeen shown to produce a similar deterioration in motor

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performance for the non-attentional task as shown in ourstudy (Schwab et al, 1954; Benecke et al, 1986). Therefore,it is unlikely that the explanation for the phenomenon canbe due to a linking of stepping to the frequency of syllableproduction of the speech task. In this regard, we used thesecondary task technique as an already established tool toexplore the role of attention in training with visual cuescompared with the attentional strategy.

Study ThreeAim and procedureGiven that gait training with visual cues appears to work ina similar manner to cognitive strategies that utilize attentionalmechanisms, effective gait performance in Parkinson'sdisease may be very dependent on the encouragement of abystander or therapist to remind the patient to concentrateon stride regulation. Unfortunately, people with Parkinson'sdisease have to function without such continual remindersand therefore it would be of interest to determine if trainingeffects persist if subjects believe that no recording is actuallytaking place. Study Three was designed to assess this influenceof placebo behaviour on the maintenance of stride length inthe retention phase, as demonstrated in Studies One and Two.

Eight Parkinson's disease subjects and eight age-, height-and sex-matched controls were recruited from the KingstonCentre Movement Disorders Clinic. Each subject was testedin a single session using the procedure for gait analysisoutlined previously. The gait patterns of control subjectswere first recorded, to be used as the criterion for Parkinson'sdisease gait. The mean of two trials of preferred gait incontrol subjects was used as a criterion reference againstwhich Parkinson gait performance could be compared and isrepresented by dotted horizontal lines in Fig. 6.

Parkinson's disease subjects then performed two baseline10 m walks, eight trials with visual cues and eight retentiontrials. In half of the visual cue trials, data were gathered assubjects walked over the cues and in the remaining trialsdata were covertly obtained as subjects walked back to thecomputer along an adjacent walkway without cues. Similarly,in half of the retention trials data were obtained when subjectsbelieved that they were being tested and in the other halfdata were collected on the way back to the computer whensubjects did not know that they were being measured. Theorder of overt measurement and covert measurement trialswere randomized to control for series effects. The effects ofthe attentional strategy were not evaluated in this experiment.

Eight control subjects were also tested under overt andcovert gait measurement conditions to determine whetherexpectancy effects related to the measurement processaffected the walking pattern. The eight subjects who wereused to control for the secondary task conditions in StudyTwo were recruited for this purpose.

Statistical analysisThe mean values for Parkinson's disease subjects and their95% confidence intervals were expressed as a percentage of

S - Strid* LengthV • VotodtyC > Cadence

• B*Mlnab VhtulCuuc Visual C U M (Covert)d Ratontkxi• Retention (Covtrt)

S V

Fig. 6 Means and limits for the 95% confidence intervals for gaitvelocity, cadence and stride length for Parkinson's diseasesubjects expressed as a percentage of the values for matchedcontrols.

the values obtained for control subjects and a series of pairwise comparisons between the control group and Parkinson'sdisease groups were conducted using the t statistic forcorrelated samples.

ResultsFigure 6 depicts the mean values and 95% confidenceintervals for stride length, velocity and cadence in theParkinson's disease subjects, expressed as a percentage ofthe values obtained for age-matched controls for each of theconditions.

For baseline walking, the mean Parkinson's disease stridelength was significantly less than normal [r(7) = -6.7, P =0.0003]. The mean velocity was also less than criterion[^7) = -4.12, P = 0.004] (Fig. 6A). The mean baseline DSduration for the Parkinson's disease group was significantlyhigher than normal [f(7) = 2.63, P = 0.034]. However, themean cadence at baseline for the Parkinson's disease groupwas not significantly different from the control group.

When Parkinson's disease subjects were measured duringperformance of the visual cue trials, the values for all fourdependent variables were not significantly different from

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normal (Fig. 6B). However, when Parkinson's diseasesubjects were covertly monitored on their walk back to thecomputer after each visual cue trial, the gait patterndeteriorated (Fig. 6C). There was a statistically significantdecrease in mean stride length of Parkinson's disease subjectsfrom the overtly monitored visual cue trials to the covertlymonitored visual cue trials [/(7) = 4.99, P = 0.002]. Themean velocity was also significantly less than the covertlymonitored visual cue trials [t{l) = 3.02, P = 0.019]. Themean cadence and DS did not show significant change.

For the standard retention test (Fig. 6D) none of thegait parameters were significantly different from criterion.However, the difference in stride length from the overtlymonitored retention trials to the covertly monitored retentiontrials was statistically significant [t{l) = 4.8, P = 0.002]. Themean velocity was also significantly less than the velocityfor the overtly monitored retention trials [t{l) = 3.22, P =0.015]. The mean Parkinson's disease cadence and DS werenot significantly different from the overtly monitored trials.

For the eight control group subjects there were nostatistically significant differences in stride length, velocity,cadence or DS from the overt to the covert measurementtrials (Table 8).

DiscussionThe results for Study Three clearly show that whenParkinson's disease subjects attended to their walking, anormal gait could be achieved with visual cues and could beretained after the cues were removed. However, when therewas not a perceived requirement for normal gait performance(e.g. a researcher instructing the patient to perform ameasurement trial), the stride length decreased in six of theeight subjects. People with Parkinson's disease were able togenerate the criterion gait at will with training. However,when they did not perceive that the walking pattern wasbeing tested, it appears that they did not direct their fullattention to their stepping pattern, with a resultantperformance decrement, primarily in relation to stride length.These results reinforce our previous hypothesis that thepositive effects of visual cues were due to increased attentionon the criterion stride size. The results also reinforce the ideathat Parkinson's disease subjects can learn an attentionalstrategy to elicit a normal gait pattern and can use thisstrategy at will to normalize walking, particularly when theyare prompted by an external source to do so. However, overprolonged periods of time without continual encouragementthe effect of training may wane to pre-training levels.

General discussionThe main finding to be highlighted by this series of studieswas that Parkinson's disease subjects could generate normalstride length by use of visual cues or an attentional strategy.Study One revealed that maintenance of normal gaitparameters persisted once training ceased for both strategies

and that a normal stepping pattern could be generated forthe 2 h of measurement that occurred after training. Thisfinding suggested that both strategies may have utilizedsimilar mechanisms to enhance the walking pattern. In StudyTwo we examined this point further by the use of simultaneoustask performance during the retention phase. Again, verysimilar patterns of deterioration in gait parameters occurredfor visual cues and the attentional strategy and thedeterioration in gait parameters was graded according to thelevel of attention required for secondary task performance.Study Three demonstrated that factors which remindedParkinson's disease subjects to use attentional mechanismsfacilitated the maintenance of normal gait parameters, andwaning of attention resulted in deterioration of performance.This latter study highlighted the need for vigilance in theeffective use of attentional strategies in normalizingparkinsonian gait.

These findings suggest that people with Parkinson's diseaserely heavily on attentional processes to modulate their walkingpatterns. Although there is prior literature on attentionalfactors in relation to motor control in Parkinson's disease,this has been obtained in studies of upper limb activities(e.g. Schwab etal., 1954; Talland and Schwab, 1964; Beneckeet ai, 1986; Bradshaw et al, 1993). To our knowledge, theseresults represent the first example of research in which therole of attentional processes in the regulation of locomotionin Parkinson's disease has been examined. We do not believethat the upper limb results could have been automaticallyextended to cover lower limb function given the extensiveliterature on the differences in CNS mechanisms that applyto gait control. For example, the greater emphasis on spinaland brainstem structures in the generation of locomotion(Grillner et al, 1986; Pearson and Rossignol, 1991) raisessufficient doubt to require original data rather than rely onextrapolation from upper limb movements.

The finding that Parkinson's disease subjects relied heavilyon attentional resources to control stride length followingtraining might suggest that the preferred gait pattern hadnot been properly learned, possibly because they had notundertaken sufficient practice to allow the new pattern tobecome automatic. One theory of motor learning put forwardby Fitts (1964) is that people pass through three stages whenacquiring a new skill. The first stage is known as the cognitivephase, during which the person gains an understanding ofthe global requirements of the task. During the second stage,known as the fixation stage, specific requirements such asthe speed, amplitude and force are refined through largeamounts of practice. During the fixation stage the personusually needs to closely attend to the movement duringperformance. By the third stage, known as the automaticphase, the motor skill is well established and can be performedautomatically in a range of contexts with limited demandson attentional resources. The pattern of results obtained inthis series of investigations might lead some to suggest thatParkinson's disease subjects were in the second stage ofmotor skill acquisition and the preferred gait pattern had not

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yet become automatic. The counter argument is that learningthe skill of walking takes place at a very young age and inadults this skill would have progressed to Fitts Stage Threelong ago. Moreover, in Parkinson's disease automatic skilledmovements cannot be executed normally due to the defectivebasal ganglia cue which, we have hypothesized, normallyinteracts with the SMA to string submovements together(Iansek et al., 1995). Consequently, motor mechanisms inParkinson's disease might revert to more primitive controlstrategies which place the level of skill acquisition at StageTwo of the Fitts model. We believe our results are consistentwith this latter explanation.

This explanation raises the question of whether Parkin-son's disease subjects can ever leam to walk permanentlywith normal stride length, velocity and cadence withoutconsciously focusing on their stepping pattern. Even thoughwe showed short-term performance effects, we also observedthat walking had defaulted to baseline levels by the followingmorning, indicating that the gait changes had not becomefully automatic. One possibility is that Parkinson's diseasesubjects might never be able to generate normal stride lengthautomatically, even though they can learn strategies to elicita normal stepping pattern consciously at will. Evidence isaccumulating that the basal ganglia play a key role inmaintaining movement automaticity (Iansek et al., 1995) andwhen the basal ganglia are disrupted Parkinson's diseasesubjects cannot properly perform automatic sequentialmovements such as writing, speaking, swallowing andwalking. In a well-known study by Seitz and Roland (1992)the results of PET studies demonstrated that during the earlystages of learning a novel finger movement sequence, thecortex, PMA and SMA were metabolically active, whereasthe basal ganglia activity was minimal. With repeated practice,the skill eventually became automatic and this was associatedwith a marked increase in the activity of the basal gangliaactivity and a decline in the cortical regions. These resultsprovide some indication that the basal ganglia play a primaryrole in allowing movement performance to shift fromconscious control to automaticity. Whether other areas of thebrain also participate in this control process remains open toquestion. It also remains to be established whether otheralternative regions of the CNS can substitute for the basalganglia in controlling automatic movements such as walking,given optimal practice conditions.

The lack of understanding regarding the neural correlatesof movement automaticity is mirrored by an incompleteunderstanding of the role of the basal ganglia in the controlof human locomotion, and in particular, stride lengthregulation. As outlined in the Introduction, we havehypothesized that the basal ganglia play two key roles inmotor control. First, they provide a phasic cue to the SMAthat is timed to terminate set related activity in the SMAand, therefore, they play a role in maintenance of adequatemovement preparation for submovements performed in asequence (Brotchie et al., 1991a, b). Secondly, the basalganglia contributes to motor set for whole movement

sequences and the absent basal ganglia contribution may leadto inadequate gain in motor execution mechanisms whichcould result in an underscaling of successive steps duringgait {see Hallett and Khoshbin, 1980). The fact that stridelength was responsive to the attentional strategies providessome indication that stride length deficits in Parkinson'sdisease relate to problems in motor set rather than a deficitin the internal cueing of human locomotion.

This investigation provides the first data in the literatureon the effects of attentional mechanisms in relation to traininglocomotor function in Parkinson's disease. As such, theresults carry implications for clinical practice. In agreementwith previous reports we showed that practice with visualcues has an immediate performance effect (Bagley et al.,1991; Weissenborn, 1993). Moreover, a cognitive strategy,whereby Parkinson's disease subjects focused their attentionon walking with a specified stride length, was equallyeffective as visual cues. The gains achieved with trainingwere depleted during secondary task performance andlocomotion was optimal under supervision. Thus, whenpatients do not focus their attention on walking with a morenormal stride, or when a bystander is not present to remindthem to concentrate on their walking pattern, there might bea tendency to revert to habitual movement patterns.

To summarize, these investigations confirm that the abilityto generate a normal stepping pattern is not lost in Parkinson'sdisease, and that gait hypokinesia reflects a difficulty inactivating the locomotor control system. Normal stride lengthcan be elicited in Parkinson's disease using attentionalstrategies and visual cues, possibly because both of thesemethods focus attention on the criterion stride size.

AcknowledgementsWe wish to thank all of the subjects who gave so freely oftheir time for these experiments, the reviewers for theirvaluable comments which guided us to revise the manuscriptand Cameron Grant for his technical assistance. This researchwas supported by grants from the Sandoz Foundation forGerontological Research and from La Trobe University.

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Received November 29, 1994. Revised September 15, 1995.Accepted November 6, 1995

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