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Research Reports |
S O'Shea, BPhty(Hons), is Staff Physiotherapist, Wodonga Regional Health Service, Wodonga, Victoria, Australia
ME Morris, PhD, MappSc, BappSc(PT), Grad Dip (Gerontology), is Professor and Head, School of Physiotherapy, La Trobe University, Victoria 3086, Australia (m.morris{at}latrobe.edu.au). Address all correspondence to Dr Morris
R Iansek, PhD, FRACP, is Neurologist and Director, Movement Disorders Program, Kingston Centre, Cheltenham, Victoria, Australia
Submitted August 20, 2001;
Accepted March 19, 2002
 | Abstract |
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Key Words: Aging • Dual tasks • Gait • Locomotion • Parkinson disease • Physical therapy
| Introduction |
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Whether secondary motor tasks lead to greater deterioration in gait than secondary cognitive tasks of similar complexity has not been investigated. Physical therapists should know whether the type of secondary task affects gait so that they can educate patients with PD about likely consequences and risks of performing motor or cognitive activities while walking.
In people with PD, dual task interference is a particularly noticeable problem because of the disruption of the motor functions of the basal ganglia.4 The basal ganglia play a major role in the control of learned, repetitive movement sequences through their outputs to the supplementary motor area and brain-stem locomotor regions (see Iansek et al4 for a review). In the early stages of motor skill acquisition, the cortical regions of the brain are believed to play a major role in movement regulation. As movements become learned and automatic, they are thought to be controlled by the basal ganglia.5 When a movement is controlled by the basal ganglia, a person, in theory, can direct attention to controlling more novel or attention-demanding tasks through the use of the frontal cortical regions. In people with PD, normal movement patterns can be generated when attention is focused on performance; attention is thought to lead to a bypassing of the basal ganglia and the use of cortical regions to drive outputs.2,6 In dual task situations, cortical resources may be engaged in maintaining the performance of the secondary task, leaving responsibility for regulating the performance of the more automatic task to the defective basal ganglia circuitry.
Most of the evidence for impaired dual task performance in people with PD has come from studies of upper-extremity performance.7–12 Talland and Schwab12 studied people with and without PD during tasks requiring them to press a counter with one hand while they transferred beads with the other hand. They also assessed sequential (unitask) performance of these actions. Although both groups showed reduced movement speed in the dual task condition, those with PD showed a much greater performance decrement. Similarly, Dalrymple-Alford et al9 studied the effects of adding a cognitive task (digit recall) when subjects performed an upper-extremity tracking task. Subjects without PD were able to maintain similar levels of skill on the tracking task while recalling the digits. Subjects with PD increased the number of tracking errors when they focused their attention on reciting the digits. Based on previous research, therefore, people with PD appear to have difficulty performing simultaneous upper-extremity motor tasks as well as motor tasks coupled with cognitive tasks.
The dual task interference effects seen in the studies of upper-extremity performance may not necessarily apply to gait. Arm and hand movements are mainly controlled by the motor cortical regions, whereas locomotion is thought to be regulated mainly at brain-stem, spinal, and cerebellar regions, with descending input from the cortex.13 Gait consists of highly preprogrammed movements, whereas some upper-extremity movements are more novel and are thought to require attention, visual guidance, and somatosensory feedback to control their performance. Only 3 investigations have examined the effect of dual task performance on gait in people with PD. Morris and colleagues2 investigated the effect of a secondary verbal-cognitive task on the gait of 16 subjects with PD and a matched comparison group. Using visual cues and attentional strategies such as visualization and mental rehearsal, people with PD were trained to walk with normal stride length, cadence, walking speed, and double support. Normal gait values were determined by first collecting data for age- and sex-matched control subjects. Gait patterns in people with PD were then assessed while sentences of increasing complexity were recited. There was a decrease in stride length and walking speed in subjects with PD that was proportional to the difficulty of the sentence recited.
Bond and Morris3 examined dual task interference using a tray-carrying task. Subjects with PD and matched comparison subjects walked under 3 conditions along a 10-m walkway: (1) free walking, (2) walking carrying an empty tray, and (3) walking carrying a tray with 4 plastic, long-stemmed empty glasses. In the subjects without PD, no deterioration in walking performance was found across the 3 conditions. In contrast, the group with PD showed a mean reduction in stride length of 0.13 m and a mean reduction in gait speed of 7.56 m/min when changing from preferred walking to walking while carrying a tray with glasses. Thus, a critical level of task complexity was required before walking performance deteriorated in people with PD.
Camicioli et al1 provided the only other investigation into the effect of a verbal cognitive secondary task on walking in people with PD. They examined the effects of talking while walking in people with motor freezing, people without motor freezing, and a comparison group. Motor freezing is an abrupt cessation of movement in which a person subsequently finds it difficult to initiate movement.1 It affects the performance of well-learned motor skills. When patients with motor freezing were instructed to maintain verbal fluency while reciting words during gait, they showed a decrease in step size and greater slowing of gait than subjects in the other groups. Measures of verbal fluency during number recital were not documented, making it difficult to determine the trade-off between primary and secondary task performance that resulted from dual task interference. In addition, there was no attempt to examine the effects of task complexity or task type on gait.
The literature contains no reports where motor and cognitive secondary tasks were studied within the same investigation. The aim of this investigation was to further examine the effects of simultaneous task performance on walking in people with PD by clarifying whether the type of secondary task (motor or cognitive) was a major determinant of the severity of dual task interference.
| Method |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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All gait trials also were videotaped using a Panasonic WVCL350 video camera
mounted on a tripod. For the secondary motor task (coin transference), 2 pockets made of calico (denim-like) material (16.5 x 14.5 cm) were attached by calico loops to a black leather belt (size: 44 in/112 cm). The midpoints of the pockets were situated over the anterior aspect of the right and left hip joints, respectively. This required the subjects' arms to cross from the dominant side to the nondominant side repeatedly when transferring the coins. A total of 12 Australian 20-cent coins were used.
For the secondary cognitive task condition, a digit subtraction task was used. Subjects were asked to count backward aloud by threes from a starting number, which was determined by selecting a card with a randomly generated number from 125 to 250 written on it. For each gait trial in this condition, a different card was randomly selected from a pack of 15 cards. The card was shown to the subject for 5 seconds before walking began. This task was created to diminish the impact of response synchronization, whereby a person times his or her footsteps with the spoken word, as observed during standard digit span (forward/backward) tests used in previous dual task studies (N Georgiou, personal communication, 2000). To minimize the likelihood that subjects would learn the secondary task, no practice or familiarization trials of the additional tasks were permitted.
Procedure
All testing was conducted in the Gait Laboratory at Kingston Centre. Prior to testing, all subjects were interviewed about their medical history and had the research procedure explained to them. The STMS14 was completed, and measurements of height, weight, and leg length were taken. Subjects with PD also were examined using the Modified Webster Scale, which provides a measure of disability.15
Gait trials were performed on a 14-m-long gray linoleum walkway, with the middle 10 m used for data collection. Subjects with PD were tested during the self-determined peak or "on" phase of their medication cycle. We did this because greater consistency of gait performance has been demonstrated for people with PD when medication levels are optimal.16 The walking patterns of all subjects were tested under 3 conditions: (1) free walking ("free"), (2) coin transference while walking ("coin"), and (3) digit subtraction while walking ("digit"). Subjects walked 3 times under each condition, and the order of conditions was randomly allocated.
For all 3 conditions, subjects were instructed to walk at their preferred pace. During the coin condition, the belt with the pockets was fitted to the subject and the coins were placed in the pocket on the side of their dominant hand. Subjects reported their dominant hand by indicating which hand they would use to catch a small ball. Subjects were then instructed to use their dominant hand to transfer as many coins as they could, one at a time, from the starting pocket to the pocket on the opposite side. For the digit subtraction condition, subjects were asked to count backward aloud by threes as described earlier.
In order to establish that the secondary cognitive and motor tasks were comparable in difficulty and to gain information about the coin and digit tasks without the subject walking, data also were collected for the rate of coin transference, the digit response rate, and the number of errors committed during digit subtraction while subjects were standing (Tab. 2). One trial of these baseline data was collected on the same day, immediately before gait analysis and confirmed using video analysis.
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| Results |
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Secondary Tasks
Table 2 presents the means and standard deviations for performance on the coin (motor) and digit (cognitive) tasks in both standing and walking conditions. A difference between the groups was found for the coin transference rate for standing trials (t28=–3.45, P<.005) and walking trials (t28=–6.21, P<.0001). Subjects with PD also showed a reduction in coin transference rate between the standing and walking conditions (t14=–3.60, P<.05).
For the digit subtraction task, subjects with PD responded at slower rates than the comparison subjects during both standing trials (t28=–3.65, P< 0.01) and walking trials (t28=–4.41, P<.0001). The response rate during standing was no different from the response rate during walking trials for subjects with PD (Tab. 2), whereas comparison subjects demonstrated an increase in response rate with walking trials (t14=2.96, P<.05). During walking trials, subjects with PD committed more errors in digit subtraction than did the comparison subjects (t28=3.19, P<.005).
| Discussion |
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Dual Task Interference
Camicioli et al,1 Morris et al,2 and Bond and Morris3 noted that people with PD experienced marked difficulties when they were instructed to perform a complex secondary task while walking. Older people without pathology or impairments (aged 65–74 years) exhibit diminished performance when performing attention-demanding activities at the same time as walking.17,18 Dual task interference during locomotion is also problematic for people with neurological conditions such as Alzheimer disease19 and Huntington disease.20 In our study, subjects with PD may have demonstrated interference in their walking performance because central nervous system processing mechanisms were being used to perform the coin and digit tasks. In theory, this required gait to be controlled by impaired basal ganglia. When gait is controlled by the defective basal ganglia, reduction in step size and walking speed occurs.21
Models of Dual Task Interference
The main theoretical models accounting for dual task interference in people with PD are: (1) the capacity- or resource-sharing model, (2) the bottleneck model, and (3) the cross-talk model (see Pashler22 for a detailed review). These are "attentional" models, with the term "attentional" referring to the focus of mental activity on a task. Capacity-sharing models are based on the assumption that attention resources are limited. Therefore, when people perform 2 tasks simultaneously, attention must be divided between the tasks. How attention is divided between the 2 tasks relies on several factors, including task complexity, familiarity, and importance.22 According to the capacity-sharing model, dual task interference will occur only if the available resource capacity is exceeded, resulting in a decline in performance on one or both of the tasks.22
The bottleneck and cross-talk models assume that dual task interference is affected by the type of tasks performed simultaneously, rather than the amount of attention needed to sustain performance.22 According to the bottleneck model, similar tasks performed concurrently cause "bottleneck" interference because they compete for the use of the same pathways.22 In contrast, cross-talk models assume that task similarity reduces dual task interference, because the use of the same pathway increases the efficiency of processing by using less attentional resource capacity.22
The results of our investigation lend support to the capacity-sharing model of dual task interference. For both elderly people with PD and those without PD, a large proportion of the attentional capacity appeared to be directed toward the coin and digit subtraction tasks at the expense of walking performance. Because the secondary tasks were relatively novel compared with walking, we believe that they would require more attentional resources.
In our opinion, gait changes occurring during dual task situations may be the result of compensations undertaken by people with PD to reduce the risk of falling. Fast walking speeds require greater balance control because of the rapidly changing accelerations of the center of mass and the reduction in double support time.23 We argue that, by slowing walking speed and reducing stride length during secondary tasks, people with PD may be attempting to decrease the balance requirements for gait. Paradoxically, slow walking speeds also can increase balance demands because greater time must be devoted to balancing the head, arms, and trunk over the stance leg.23 Increases in double support time are thought to negate this effect during slow walking.23 In our study, comparison subjects who were instructed to walk at their preferred speed demonstrated an increase in their double support time in the dual task conditions (Tab. 3), which may indicate that they were able to accurately compensate for the reductions in stride length and walking speed. By contrast, subjects with PD in our study and in other studies2,3 did not increase double support times during dual task performance when walking at their preferred speed. We believe that these results may indicate that people with PD have an impaired ability to modulate double support to compensate for the reductions in stride length and walking speed. This impaired ability may increase the risk of falls.
Clinical Implications and Limitations
A major goal of physical therapy for people with PD is to help them walk with normal step size and speed in order to reduce the risk of trips and falls.24 One strategy is to teach people with PD to avoid simultaneous tasks whenever possible,24 to prevent attention being directed away from generating long strides or responding to unexpected perturbations. This way people can perform tasks in isolation when they need to walk with long, fast strides, such as when they cross a busy road. Doing one task at a time, however, is not always practical and, in our opinion, carries a high cognitive demand by necessitating continuous conscious attention to the task. It is thus likely that people with PD will sometimes revert to dual task performance. Therefore, we believe that it is advisable to teach people with PD about the safety risks associated with doing more than one task at a time. Some therapists might argue that teaching people with PD about the safety risks associated with simultaneous task performance should include engaging them in other tasks during gait training, while they are under close supervision. Whether people with PD have the capacity to learn how to perform dual tasks during walking safely and independently has not been established. Research is also needed to determine whether people with PD can learn how to safely and independently switch from doing several tasks to only walking when needed.
Our study had several limitations. First, the findings cannot be generalized to all people with PD, because only subjects with gait hypokinesia and mild to moderate impairments were included. Further research is needed to examine the effects of dual task performance during walking for subjects with other movement disorders such as akinesia, dyskinesia, and postural instability. The secondary tasks used were what we call "semifunctional" tasks. Investigation of the effects of functional tasks during gait in more real-world settings during activities of daily living is needed. In addition, all patients were tested at peak dose in the levodopa medication cycle, and it is not clear whether the results could be generalized to "off" phase performance.
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| Footnotes |
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This research was conducted in fulfillment of the requirements for Ms O'Shea's honors program at the School of Physiotherapy, La Trobe University.
This study was approved by the ethics committees at La Trobe University and Kingston Centre.
* B7L Engineering, Santa Fe Springs, CA 90670. 
IBM Corp, New Orchard Rd, Armonk, NY 10504.
Panasonic Australia, Austlink Corporate Park, 1 Garigal Rd, Belrose, New South Wales 2085, Australia.
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This article has been cited by other articles:
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  T Wu and M Hallett Neural correlates of dual task performance in patients with Parkinson's disease J. Neurol. Neurosurg. Psychiatry, July 1, 2008; 79(7): 760 - 766. [Abstract] [Full Text] [PDF]
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 C. G Canning, L. Ada, and E. Woodhouse Multiple-task walking training in people with mild to moderate Parkinson's disease: a pilot study Clinical Rehabilitation, March 1, 2008; 22(3): 226 - 233. [Abstract] [PDF]
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 M. E Morris Locomotor Training in People With Parkinson Disease Physical Therapy, October 1, 2006; 86(10): 1426 - 1435. [Abstract] [Full Text] [PDF]
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 J. P. Regnaux, D. David, O. Daniel, D. B. Smail, M. Combeaud, and B. Bussel Evidence for Cognitive Processes Involved in the Control of Steady State of Walking in Healthy Subjects and after Cerebral Damage Neurorehabil Neural Repair, June 1, 2005; 19(2): 125 - 132. [Abstract] [PDF]
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