The Interaction Between Executive Attention and Postural Control in ...

11 downloads 4322 Views 440KB Size Report
velocity of center of pressure displacement in the mediolateral and anteroposterior ...... interaction between the development of postural control and the executive .... The MathWorks Inc, 3 Apple Hill Dr, Natick, MA 01760-2098. b. Version 2.04 ...
834

ORIGINAL ARTICLE

The Interaction Between Executive Attention and Postural Control in Dual-Task Conditions: Children With Cerebral Palsy Dinah S. Reilly, PhD, PT, Marjorie H. Woollacott, PhD, Paul van Donkelaar, PhD, Sandra Saavedra, MS, PT ABSTRACT. Reilly DS, Woollacott MH, van Donkelaar P, Saavedra S. The interaction between executive attention and postural control in dual-task conditions: children with cerebral palsy. Arch Phys Med Rehabil 2008;89:834-42. Objective: To investigate the interference between a secondary task and a postural task in children with cerebral palsy (CP). Design: In this exploratory study, a dual-task paradigm was used in which children stood in either a wide or a narrow stance position while simultaneously performing a visual working memory task calibrated to be of equitable attentional demand between groups. Setting: Study data were gathered in a university motor control laboratory. Participants: Children with CP (n⫽8; age range, 10⫺14y) were compared with typically developing older children (n⫽6; age range, 7⫺12y), and typically developing young children (n⫽5; age range, 4⫺6y). Interventions: Not applicable. Main Outcome Measures: Proficiency in postural control was measured by the range and root mean square of the velocity of center of pressure displacement in the mediolateral and anteroposterior directions, calculated from forceplate data. Accuracy of response was used as a measure of cognitive task performance. Capacity of the executive attention system was determined by assessing visual working memory capacity. Results: Children with CP, like the typically developing young children, were more unstable and had less executive attention capacity compared with older children, and like the typically developing young children, experienced dual-task interference in postural control in both stance positions. Children with ataxic CP also experienced decreased cognitive task performance in narrow stance. Conclusions: In designing therapeutic interventions for children with CP, it would be beneficial for clinicians to assess postural control in both single- and dual-task environments. Key Words: Cerebral palsy; Rehabilitation. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation

From the Department of Human Physiology, University of Oregon, Eugene, OR. Supported by the National Institutes of Health (grant no. 5R01NS038714-07). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Correspondence to Dinah S. Reilly, PhD, PT, 4048 S Iriondo Way, Boise, ID 83706, e-mail: [email protected]. Reprints are not available from the author. 0003-9993/08/8905-00737$34.00/0 doi:10.1016/j.apmr.2007.10.023

Arch Phys Med Rehabil Vol 89, May 2008

URING THE PAST 20 YEARS, research has indicated D that the emerging difficulties of postural control in children with cerebral palsy (CP) were due to impairments in the neuromuscular, sensory integrative, and musculoskeletal systems.1-4 Though postural control was once thought to be automatic, studies have shown that in both adults and children it is attentionally demanding; thus it is adversely affected by conditions in which the person is asked to balance and simultaneously perform a second attentionally demanding cognitive task (defined as a dual-task condition).5-11 Thus an additional contributing factor to postural constraints in children with CP could be that the attentional requirements of balancing and performing a second cognitive task simultaneously cause reduced attention to balance control and an increased risk of falls. As defined by Posner and Rothbart,12 a component of the attentional network is executive attention, which underlies the allocation of attention for resolving conflict between 2 stimuli competing for processing, for correction of errors, and for selection of thought. Van Zomeren and Brouwer13 further divide selectivity into focused and divided attention. Executive attention in conflict resolution matures significantly between the ages of 5 and 10 years14-17 with the most substantial changes occurring between the ages of 6 and 8 years.15-17 The efficiency and coordination of the allocation of attention between the performance of 2 tasks in a dual-task condition (divided attention) matures into adulthood.18,19 Neuroimaging studies have shown that the dorsilateral prefrontal cortex and the dorsal anterior cingulate gyrus are strongly active during tasks requiring the allocation of attention.20-23 In addition, neurophysiologic studies involving children and adults with cerebellar lesions have shown the cerebellum to be crucial for tasks requiring divided attention,24,25 specifically, in coordinating shifts between attentional sets.26,27 These are thus potential pathways involved in the central bottleneck of information processing and/or attentional allocation in these people and deficits in these areas could cause decreased performance in dual-task situations. Children with spastic diplegia CP due to periventricular leukomalacia sustain lesions in the white matter affecting neural pathways connecting the prefrontal cortex with other brain regions.28 Christ et al29 showed that children with spastic diplegia CP experienced deficits in their ability to inhibit irrelevant stimuli when performing a task. Three conflict tasks, the Stroop, antisaccade, and stimulus-reversal tasks, assessed the capacity of the executive function of attention in 13 children with bilateral spastic CP, ages 6 to 18 years. Compared with age-matched norms, children with bilateral spastic CP had greater limitations in executive attention. Developmental studies in typically developing children have shown that the maturation of postural control in quiet stance, measured by body sway, occurs late in childhood, between the ages of 7 and 10 years.30-34 Two studies examining postural stability of children with spastic CP in static stance have shown them to be equally as stable as their age-matched peers.2,35 However, in a study by Rose et al,35 8 of the 23 children with

835

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly Table 1: Group Demographics Groups

Sex M/F

Age (y/mo)

Height (m)

Weight (kg)

Foot Length (m)

Foot Width (m)

Wide Stance Width (m)

Narrow Stance Width (m)

PBS

TDO SD TDY SD Spastic CP SD Ataxic CP SD

4/2 NA 1/4 NA 2/2 NA 2/2 NA

9/3 2 5 1/0 10/9 1/6 12 2/0

1.37 0.13 1.10 0.05 1.32 0.06 1.43 0.13

35.1 11.0 18.3 0.9 26.9 5.0 36.6 14.2

.21 .02 .17 .01 .20 .02 .23 .02

.079 .003 .07 .00 .077 .010 .08 .01

.23 .04 .21 .06 .27 .04 .30 .03

.09 .01 .08 .01 .12 .03 .10 .03

56 0 55.4 0.89 47.2 9.5 48.5 6.24

NOTE. Values are mean and standard deviation (SD). Abbreviations: F, female; M, male; NA, not applicable; PBS, Pediatric Balance Scale; TDO, typically developing older; TDY, typically developing younger.

bilateral spastic cerebral palsy had abnormal center of pressure (COP) values compared with their typically developing peers. Nashner et al4 also showed that when children were asked to stand with their feet together, body sway in the anteroposterior (AP) direction was much greater in children with ataxic CP than either children with spastic CP or age-matched norms. Recently there has been an increasing number of studies showing the attentional requirements of young and older children during postural tasks.8-11 Laufer et al9 showed that young children aged 5 years increased body sway, measured by the path-length of the COP displacement, when simultaneously performing a simple task of naming objects. Blanchard et al8 assessed the attentional requirements of postural control in static stance of older children ages 8 to 9 years. Postural sway increased with the simultaneous performance of either of the 2 cognitive tasks (reading, counting backward). In a dual-task condition, Olivier et al10 found that postural sway in children 7 years of age increased when the attentional load of the second task, the Stroop task, increased. A developmental study by Reilly et al11 showed that younger children (age range, 4 – 6y), having less developed executive attention and postural control compared with older children (age range, 7–12y) and adults, experienced postural control interference when an attentionally demanding cognitive task was performed in static stance. In addition, for the younger children, the attentional demands of postural control increased when the posture task increased in difficulty from wide stance (feet shoulder width apart) to modified tandem Romberg stance. The purpose of this exploratory study was to investigate the dual-task effects on postural control in children with CP. Due to impairments in both the postural control and executive attention network systems, it was expected that children with CP, like younger typically developing children, would undergo postural

control interference in both wide and narrow stance positions with the greatest interference occurring in narrow stance. METHODS All experimental procedures, health questionnaires, and recruitment of subjects were approved by the Committee for the Protection of Human Subjects. Participants A total of 19 children, ranging in age from 4 to 14 years, participated in the study. Of the 19 children, 8 were diagnosed with CP. Children were recruited through faculty and staff at the University of Oregon, the Eugene School District, and private rehabilitation clinics through public advertisement. To compare all children with CP with typically developing children, we divided participants into 4 groups; typically developing older children, ages 7 to 12 years (mean ⫾ standard deviation [SD], 9y 8mo⫾2y 1mo), typically developing young children ages 4 to 6 years (mean, 5y 6mo⫾1y 1mo) and children with either spastic CP or ataxic CP ages 10 to 14 (mean, 12y 3mo⫾2y) (table 1). The mean age of the group of typically developing older children is slightly lower (9y 8mo) than that of the CP group (12y 3mo). We believe this slight difference in mean age of the older typically developing children and children with CP should minimally contribute to differences in results of the study, because postural control typically matures at 7 to 10 years of age and executive function shows most maturation between 5 and 10 years.14-16,30,33 Diagnosis, Gross Motor Functional Classification System (GMFCS) levels, range of motion, and degree of spasticity were determined by a board-certified pediatric neurologist (table 2). Parents of typically developing children completed a

Table 2: Musculoskeletal Exam Ankle

Knee

Hip

Subject

Class

GMFCS*

Left

Right

Left

Right

Left

Right

CP 4 CP 6 CP 7 CP 2 CP 8 CP 3 CP 10 CP 9

Spastic CP Spastic CP Spastic CP Spastic CP Ataxic CP Ataxic CP Ataxic CP Ataxic CP

1 1 2 3 1 3 1 3

2⫹ 2 2–3† 2† 0 1† 2 1–2

1 1 2⫹† 2† 0 1† 1 1–2

3 2/1† 2⫹/1 1/1⫹† 0 1/1 1/1† 1/1

1 1/1† 2⫹/2 1/1⫹† 0 1/1 1/1† 1/1†

1† 1⫹ 2† 2⫹† 0 1 1 1

1† 1 2† 2⫹† 0 1 1 1

*Ashworth Scale of spasticity grading: 0, no increase in tone; 1, slight increase in tone; 2, moderate increase with no movement restrictions; 3, increase in tone with restrictions of movement. † Restricted range of motion.

Arch Phys Med Rehabil Vol 89, May 2008

836

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly

medical history questionnaire to ensure the absence of any neurologic or musculoskeletal disorders and a Child Behavior Checklist36 to disqualify those with attentional deficit disorders. All typically developing children participating in the study had normative attentional profiles and an absence of neurologic or orthopedic impairments. Consent forms were signed by both the children and their parent or guardian, after an explanation of the test procedures. Anthropometric measurements of height, weight, foot length, and width were recorded for all subjects. Functional balance was assessed using the Pediatric Balance Scale37 (see table 1). Children participated in the study if they could maintain static stance for 30 seconds in a wide (shoulder width) stance and in a narrower stance position without the use of assistive devices or ankle-foot orthoses. In addition, children with CP qualified for participation if they met the functional mobility criteria described in levels I, II, or III of the GMFCS. The GMFCS classifies children with CP into 5 distinct levels of functional mobility within the home, school, and community and has an interrater reliability of 75% in children less than 12 years of age.38 Each level is based on functional mobility limitations in sitting, standing, and walking, and the need for assistive devices. The larger the level number, the greater the functional limitations and need for assistive devices. Tasks We used a dual-task paradigm in which the primary task, a postural control task, was performed simultaneously with an attentionally challenging cognitive task (secondary task). The postural control tasks consisted of either an easy position of wide stance with each bare foot on 1 of 2 adjacent forceplates or a less stable position of narrow stance with feet together on 1 forceplate. Five subjects with CP were unable to maintain stability standing with their feet together and were allowed to stand with the feet apart but with minimal spacing (1–9cm) between the 2 feet. Vertical and horizontal forces from the forceplates were collected at 360Hz and filtered at 5Hz with a low-pass fourth-order Butterworth filter using Matlab computer software.a The secondary cognitive task was modified from a visual working memory task used in a study by Vogel et al39 to test visual working memory capacity in adults by varying the attentional load.40-43 The attentional load consisted of a variable number of colored shapes (squares, hearts, or stars), presented for 300ms. An auditory tone of 28ms was generated, indicating the beginning of the load presentation. A mask consisting of a gray screen was presented for a duration of 5 seconds. After the mask presentation, a 28ms auditory tone was again generated that indicated the presentation of the probe. The probe was either the same presentation of colored shapes as the load (congruent condition), or a presentation in which the color of 1 shape had changed (incongruent condition) (fig 1). A computer with SuperLab Pro computer softwareb was used to project the targets onto a display screen located 2.8m in front of the subjects and to record verbal responses through a microphone worn by the subject. After the probe presentation, children were asked to respond yes to the congruent condition (colors were the same) and no to the incongruent condition (colors were not the same). Accuracy of response was used as a measure of cognitive task performance. Each trial lasted 38 seconds. Protocol To assess dual-task interference between subject groups, it is important to equate the attentional load level of the cognitive Arch Phys Med Rehabil Vol 89, May 2008

Fig 1. Cognitive task: temporal sequence of the visual working memory task presentation in seconds and milliseconds.

task; otherwise the comparative dual-task interference may simply be due to the differential workloads of the cognitive task between groups. To ensure an equal level of task difficulty between groups, subjects performed a set of titration trials while seated. The titration task was the same visual working memory task described above, but colored shapes varied in numbers between 1 and 6 from trial to trial. The initial trials had 1 and 2 colored shapes, and depending on accuracy, the number of colored shapes increased in the trials that followed until a reduction in accuracy of 70% was reached. This quantity of shapes was termed threshold (T) and was the criterion for selecting the number of colored shapes during the experimental dual-task trials. After the titration trials, children performed the dual-task condition in either the wide stance or narrow stance posture, the order of which was randomized across groups. A chalk outline of the feet on each of the forceplates ensured consistent foot placement for every block of trials. Subjects were instructed to stand as still as possible and to perform the cognitive task as quickly and accurately as possible. To reduce the effects of fatigue on performance, children were allowed to sit between each block of trials. The dual-task condition consisted of 4 blocks of 4 trials of the presentation for each stance condition for a total of 32 trials. A block of 4 trials consisted of 2 trials at (T) level of difficulty, and 2 trials at T-2. The T-2 trials were included to ensure that the same degree of cognitive task difficulty was performed by all groups in both stance positions. After a 15-minute rest break, the trials continued in the single-task condition. In this single-task condition, the children were instructed to watch the screen, and stand as still as possible. During this time, the same temporal sequence of the cognitive task was presented; however, the screen was blank during the load and probe presentation. Children performed 2 blocks of 4 trials for each stance condition, a total of 16 trials. The entire experimental session lasted for 1.5 hours. It was video recorded for determining trials in which subjects lost balance, took a step, or moved their arms. These trials were then eliminated from data analysis. The percentage of trials eliminated from typically developing older children was 1%, from typically developing young children 10% and from the children with CP 10.6%, and 77% of those trials were from the children with the least functional mobility (GMFCS level III). For the purpose of this study, we used T as a probe of the efficiency of the executive attention. Behavioral studies have

837

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly Table 3: COP Group Means Wide

Narrow

Groups

COP AP Range (m/m)

COP AP RMS Velocity (m/s)

COP ML Range (m/m)

COP ML RMS Velocity (m/s)

COP AP Range (m/m)

COP AP RMS Velocity (m/s)

COP ML Range (m/m)

COP ML RMS Velocity (m/s)

TDO SD TDY SD Spastic CP SD Ataxic CP SD

.08 .03 .12 .05 .11 .05 .12 .06

.02 .01 .03 .01 .03 .01 .03 .01

.08 .03 .19 .10 .13 .13 .11 .07

.03 .01 .05 .01 .04 .02 .04 .02

.08 .03 .13 .06 .12 .07 .15 .09

.02 .01 .03 .01 .03 .01 .04 .03

.22 .08 .30 .22 .25 .14 .41 .19

.02 .01 .02 .01 .02 .01 .04 .02

Abbreviations: see Table 1.

shown a strong link between the capacity of the executive attention and visual working memory.40-42 A review of these studies can be found in Awh et al.43 A behavioral study by Cowan et al44 using a task similar to that of Vogel et al39 validates a developmental progression of the capacity of visual working memory in children ages 8 to 12 years. Data Analysis The extent and velocity of body sway in relation to the base of support is indicative of postural stability. The greater and faster the body sway, the less stable the posture and the less efficient is postural control at regulating posture stability.45 Displacement of COP was used as the determinant of body sway due to its relationship to the movement of the center of mass.46 The degree of postural control was determined by quantifying the range and the root mean square (RMS) of velocity of the COP displacement in the AP and mediolateral (ML) directions. In an effort to eliminate the effects of verbal articulation on COP displacement,47 an interval of time of 5.5 seconds (approximate time of probe presentation and mask) was selected for the analysis of COP for each block of 4 trials. Prior to statistical analysis, the range of COP displacement in the AP direction was normalized to foot length and in the ML direction by stance width (distance between the right and left second metatarsal). To compare group differences in the RMS velocity and range of COP in the ML and AP directions, a mixed linear model analysis of variance evaluated 4 levels (typically developing older children, typically developing young children, ataxic CP, spastic CP) between subjects and two 2-level within-subjects conditions (single- vs dual-task and wide vs narrow stance). The effects of task condition, group, and stance were evaluated through the F-test computations of specified contrasts of interest. Simple effects were extracted from these specific contrasts of group differences in single- and dual-task conditions and in wide and narrow stance, and singleversus dual-task conditions across groups in wide and narrow stance. These contrasts are a simpler overall set of contrasts than those implied by the usual 3-factor interaction. The reason for using this approach was to increase statistical power.48 We performed post hoc analyses when the defined contrast for the between- and within-subjects factors was significant at P equal to .05. Significant P values for the post hoc analyses for group simple effects were derived by the Bonferroni P value adjustment with an ␣ equal to .05. A post analysis was considered a trend if P ranged from .012 to .03 (adjusted) because this was an exploratory study. Accuracy of group responses on the cognitive task was compared by means of a 4-level between-subjects (typically developing older children, typically developing young chil-

dren, ataxic CP, spastic CP) and one 2-level within-subjects factor (wide stance vs narrow stance) statistical design. A logistic regression analysis was computed to determine the odds ratios of correct versus incorrect responses for each group and in each condition. RESULTS COP Movement in Single- and Dual-Task Conditions Single task (posture). In the single-task condition in wide stance position, the young typically developing children were the most unstable of the 4 groups in velocity and range of COP displacement in the ML direction. In the single-task condition in the narrower stance position, both groups of children with CP, like the young typically developing children, were less efficient in postural control in the ML direction compared with the older typically developing children. However, it was the children with ataxic CP who were the most unstable in narrow stance (AP range, RMS AP velocity, ML range, RMS ML velocity) (table 3). Dual-task, wide stance. As predicted, in the dual-task condition, both groups of children with CP, like the young typically developing children, experienced postural control interference. The difference in displacement of COP in dual versus single-task conditions was significant in AP range (F4,28⫽4.25, P⫽.008), in RMS AP velocity (F4,28⫽5.90, P⫽.001), and in RMS ML velocity (F4,28⫽3.33, P⫽.024). The post hoc analyses revealed a trend in the younger typically developing children to sustain dual-task effects in AP range (P⫽.03) and the children with spastic and ataxic CP to have significantly faster AP velocities (P⫽.005, P⫽.002, respectively), in dual- versus single-task conditions (fig 2). Children with ataxic CP had an additional dual-task effect in RMS ML velocity (P⫽.009) (fig 3B). When comparisons were made for the COP data between the younger and older typically developing children and the children with CP, children with spastic CP were significantly more unstable compared with the older typically developing children, indicated by a faster RMS ML velocity (F2,28⫽3.89, P⫽.032), but only in the dual-task condition (P⫽.01). Children with ataxic CP also showed a trend in having a faster RMS ML velocity (F2,28⫽3.29, P⫽.052), compared with the older typically developing children, but only in the dual-task condition (P⫽.028) (see fig 3B). Dual-task, narrow stance. As expected, the 2 groups of children with CP, like the younger typically developing children, experienced dual-task interference in postural control when in the narrower stance position. The simple effect of dual- versus single-task condition was significant in ML range of COP displacement (F4,28⫽4.55, P⫽.006), in RMS ML veArch Phys Med Rehabil Vol 89, May 2008

838

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly

the number of colored shapes in short-term memory was significantly greater for older typically developing children than for children with spastic (P⫽.001) and ataxic CP (P⫽.001) and the younger typically developing children (P⫽.012) (fig 5). The relationship between the executive attentional capacity, determined by the T in the titration trials of the visual working memory task, and the effects of the dual-task condition on postural control (COP displacement in single- vs dual-task condition) for both stance positions was computed using correlation analyses. There was a robust relationship between visual working memory capacity and dual-task effect on RMS AP velocity in wide stance (Pearson r⫽⫺.67) and on RMS ML velocity in narrow stance (Pearson r⫽⫺.66) (table 4). Across all the children, the greater the visual working memory the smaller the dual-task effects on postural control. DISCUSSION The purpose of this study was to investigate the effects of dual-task conditions on postural control in children with CP and to determine changes in attentional requirements when shifting from wide stance to the less stable position of narrow stance. In the wide stance single-task condition, neither the children with spastic nor ataxic CP (10 –14y) differed significantly in posture stability from the typically developing older children (7–12y). This has been documented previously in children with bilateral spastic CP.2,4,35 In the narrower stance position, however, the children with CP, like the typically developing young children (4 – 6y), were more unstable in the ML direction than the typically developing older children. The children with ataxic

Fig 2. Group means ⴞ1 SD of COP displacement in (A) the AP range and (B) RMS AP velocity. Abbreviations: ACP, ataxic CP; D, dual; NS, narrow stance; S, single; SCP, spastic CP; WS, wide stance.

locity (F4,28⫽3.41, P⫽.022), and in RMS AP velocity (F4,28⫽ 6.08, P⫽.001). Compared with the older typically developing children, children with spastic CP experienced a greater ML range of COP displacement (P⫽.003). A similar trend (P⫽.03) was seen in the younger typically developing children when compared with the older typically developing children (fig 3A). Individual COP tracings in single- versus dual-task conditions illustrate the dual-task effect on ML range (fig 4). In addition, the children with spastic CP experienced a faster RMS ML velocity (P⫽.003) and children with ataxic CP a significant increase in RMS AP velocity (P⫽.001) (see figs 3B, 2B). Rate of Accuracy There was a significant stance effect in the rate of accuracy on the cognitive task (␹2⫽6.12, P⫽.047), but no significant group by stance effect. The children with ataxic CP showed the greatest decrement in performance, being 2.4 times more likely to have the correct answer in wide versus narrow stance than children with spastic CP (1.47), older typically developing children (1.46), and younger typically developing children (.73). A single factor analysis of variance computed group differences in the maximum number of colored shapes recalled with a 70% accuracy rate, determined by the titration trials of the visual memory task. There was a significant group effect in the number of colored shapes recalled with a 70% accuracy rate (threshold) (F3,15⫽15.68, P⬎.001). The threshold for retaining Arch Phys Med Rehabil Vol 89, May 2008

Fig 3. Group means ⴞ1 SD of COP displacement in (A) the ML range and (B) RMS ML velocity.

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly

839

Fig 4. Individual COP tracings (in meters) in 1 block of trials (38s), in narrow stance, singleversus dual-task condition in: (A) typically developing older child; (B) typically developing young child; (C) child with spastic cerebral palsy; and (D) child with ataxic cerebral palsy. NOTE. The x axis is the AP direction; the y axis is the ML direction.

Arch Phys Med Rehabil Vol 89, May 2008

840

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly

Fig 5. Titration curve for (A) number of colored shapes recalled with a 70% accuracy rate: typically developing older children ), typically developing young children ( ), and chil( ); and (B) children with spastic CP ( ) dren with CP ( ). and children with ataxic CP (

CP were the most unstable in both the ML and AP directions. A similar finding was documented by Nashner et al4 comparing posture stability in children with ataxic and spastic CP in narrow stance. The 2 groups of children with CP (children with spastic diplegia and ataxia), like the typically developing young children, had significantly less visual working memory capacity than the typically developing older children The children with CP also showed less of a visual working memory capacity than the typically developing young children, though this difference was smaller. Due to the link between the 2 constructs of visual working memory and executive attention and the comparative posture instability in children with CP, this suggests this group of children had the least ability to allocate attentional resources to the processing of these 2 tasks, each with a large attentional load. It was expected that children with CP, having impairments in both the postural control and executive attention network systems, would have postural control interference in dual-task conditions, similar to the typically developing young children. Our study confirmed that children with CP and the typically developing young children experienced a decrement in posture stability in both stance positions with the simultaneous performance of the secondary cognitive task. Although posture stability of the children with CP did not significantly differ from that of typically developing older children in wide stance when performed in isolation, adding the performance of the cognitive task caused a significant difference in RMS ML velocity of body sway between the typically developing older children and children with spastic CP and to Arch Phys Med Rehabil Vol 89, May 2008

a lesser extent between the typically developing children and those with ataxic CP. In the dual-task condition, children with both types of CP, like the typically developing young children, experienced significant instability in the AP direction. In addition, the children with ataxic CP experienced a significant decrement in controlling the RMS ML velocity of body sway. With the additional performance of the secondary cognitive task in the narrower stance position, only the children with CP and to a lesser degree the young typically developing children experienced interference in postural control in the ML direction. In addition, the children with ataxic CP experienced a faster RMS AP velocity and had the greatest deficit in the cognitive task performance. The interference in postural control in wide and narrow stance and in the dual-task condition experienced by the typically developing young children and children with CP may have been due to limitations in the capacity of their executive component of attention. The correlation between the executive attention capacity (visual working memory) and the dual-task effects on RMS AP velocity in wide stance and RMS ML velocity in narrow stance suggests a strong relationship between the executive attention capacity and the degree of postural control interference in the dual-task condition. The typically developing young children (memory capacity of 2–3 shapes) may not have experienced as large an interference in narrow stance as the children with CP (1–2 shapes) due to their comparatively greater executive attention capacity. Likewise, the typically developing older children with the largest visual working memory (4 –5 shapes) and, thus, the largest capacity of executive attention could allocate sufficient attentional resources to the processing of both tasks and not experience a decrement to postural control in either stance position. An additional explanation for group differences in postural control interference may have been the attentional requirement of postural control in the less stable posture of narrow stance. Because the older typically developing children were more stable in narrow stance than the children with CP and the younger typically developing children, their attentional requirement for maintaining posture stability may have been much less than for the children with CP and younger typically developing children, allowing them to perform both tasks efficiently. When the children with spastic CP performed the 2 tasks simultaneously, it appeared that they directed their attentional resources primarily to the performance of the cognitive task, resulting in a decrement in the secondary task of postural control. Similar results have been documented in a study by Brauer et al5 involving adults with post-traumatic brain injury, and in a study by Laufer et al9 involving children with developmental coordination disorder. The children with ataxic CP had the greatest instability in narrow stance of all the groups of children. Because they experienced the greatest decrement in accuracy on the cognitive task and had interference in postural control it implies that

Table 4: Correlation of T/COP Displacement COP

Wide

Narrow

AP range RMS AP velocity ML range RMS ML velocity

⫺.37 ⫺.67 ⫺.06 ⫺.14

⫺.55 ⫺.42 ⫺.29 ⫺.66

NOTE. Pearson r computed from the correlation analysis between short-term memory capacity (threshold derived from titration trials) and displacement of the COP.

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly

the attentional demands of maintaining stability were greater for children with ataxic CP than for the typically developing children and the children with spastic CP. To maintain stability in the dual-task condition, the children with ataxic CP had to divide their reduced attentional resources between postural control and performance of the cognitive task, thus experiencing an interference in the performance of both tasks. In addition, this suggests that controlling posture stability in narrow stance versus wide stance is more attentionally demanding for children with ataxic CP. Studies have shown that children and adults with neocerebellar damage have deficits in the shifting of attention between tasks.26,27 Although the exact location of the cerebellar lesion in our sample of children with ataxic CP is unknown, it is possible that the area responsible for attentional shifts, the superior posterior cerebellum49 is involved. Study Limitations There are specific limitations of the study that should be considered in the interpretation of the results. First, the level of task difficulty may not have been equal between the groups of children with CP and between the children with CP and typically developing children. Several children with CP had a ceiling effect of 1 and 2 shapes at a threshold of 70% accuracy, and therefore, did not have the easier task of T-2 interspersed in the block of trials. In addition, though it is considered important to equate the difficulty of attentional tasks when comparing different age groups and people with different medical conditions such that each person performs at the same level (in this case at 70% accuracy), this does not allow the comparison of performance when people are asked to do equally difficult tasks, as occurs in activities of daily living. Thus all dual-task performance differences between groups are minimized. Finally, in this current study the large performance variability and small sample size may have affected significant P values in the differences between groups in several of the measurements of body sway. Variability in body sway among the populations of young children and children with CP has been documented.4,31,34 Variability was not only evident within a group but within the performance of individual children. Further studies with larger sample sizes are needed to substantiate these findings. CONCLUSIONS When evaluating or improving functional motor and/or cognitive abilities, clinicians and educators must consider the dual-task effects that can interfere in the performance of one or both tasks for both younger children and children with CP. If an educator is assessing cognitive abilities, then providing external support to assist posture stability may reduce the attentional requirement of postural control and increase cognitive abilities. When the clinician evaluates postural control in a child with CP, it would be beneficial to assess stability in a single- and dual-task condition in order to determine the attentional requirements of postural control for that child. It is also of interest that a study by Craft et al50 showed that children with spastic CP improved in attentional and cognitive abilities after undergoing a selective dorsal rhizotomy (SDR) surgery. Further investigation with a similar dual-task paradigm to that used in this study may show that the improvement in attentional and cognitive abilities secondary to SDR may result from an improvement in posture stability, and therefore, a reduction in the need for attentional resources during sitting or standing.

841

References 1. Burtner PA, Qualls C, Woollacott MH. Muscle activation characteristics of stance balance control in children with spastic cerebral palsy. Gait Posture 1998;8:163-74. 2. Cherng RJ, Su FC, Chen JJ, Kuan TS. Performance of static standing balance in children with spastic diplegic cerebral palsy under altered sensory environments. Am J Phys Med Rehabil 1999;78:336-42. 3. Lowes LP, Westcott SL, Palisano RJ, Effgen SK, Orlin MN. Muscle force and range of motion as predictors of standing balance in children with cerebral palsy. Phys Occup Ther Pediatr 2004;24:57-77. 4. Nashner LM, Shumway-Cook A, Marin O. Stance posture control in select groups of children with cerebral palsy: deficits in sensory organization and muscular coordination. Exp Brain Res 1983;49: 393-409. 5. Brauer SG, Broome A, Stone C, Clewett S, Herzig P. Simplest tasks have greatest dual task interference with balance in brain injured adults. Hum Mov Sci 2004;23:489-502. 6. Pellecchia G. Postural sway increases with attentional demands of concurrent cognitive task. Gait Posture 2003;18:29-34. 7. Woollacott MH, Shumway-Cook A. Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 2002;16:1-14. 8. Blanchard Y, Carey S, Coffey J, et al. The influence of concurrent cognitive tasks on postural sway in children. Pediatr Phys Ther 2005;17:189-93. 9. Laufer Y, Ashkenazi T, Josman N. The effects of a concurrent cognitive task on postural control of young children with and without developmental coordination disorder. Gait Posture 2008; 27:347-51. 10. Olivier I, Cuisinier R, Vaugoyeau M, Nougier V, Assaiante C. Dual-task study of cognitive and postural interference in 7-yearolds and adults. Neuroreport 2007;18:817-21. 11. Reilly DS, van Donkelaar P, Saavedra S, Woollacott MH. The interaction between the development of postural control and the executive function of attention. J Mot Behav 2008;40:90-102. 12. Posner M, Rothbart M. Attention, self-regulation and consciousness. Philos Trans R Soc Lond B Biol Sci 1998;353:1915-27. 13. Van Zomeren AH, Brouwer WH. Clinical neuropsychology of attention. New York: Oxford Univ Pr; 1994. 14. Mezzacappa E. Alerting, orienting, executive attention: developmental properties and sociodemographic correlates in an epidemiological sample of young, urban children. Child Dev 2004;75: 1373-86. 15. Ridderinkhof KR, van der Molen MW, Band GP, Bashore TR. Sources of interference from irrelevant information: a developmental study. J Exp Child Psychol 1997;65:315-41. 16. Rueda RM, Fan J, McCandliss BD, et al. Development of attentional networks in childhood. Neuopsychologia 2004;42:1029-40. 17. Diamond A, Taylor C. Development of an aspect of executive control: development of the abilities to remember what I said and “do as I say, not as I do.” Dev Psychobiol 1996;29:315-34. 18. Cepeda NJ, Kramer AF, Gonzalez de Sather JC. Changes in executive control across the life span: examination of taskswitching performance. Dev Psychol 2001;37:715-30. 19. Irwin-Chase H, Burns B. Developmental changes in children’s abilities to share and allocate attention in a dual task. J Exp Child Psychol 2000;77:61-85. 20. Bush G, Luu P, Posner MI. Cognitive and emotional influences in the anterior cingulated cortex. Trends Cogn Sci 2000;4:215-22. 21. Casey BJ, Giedd JN, Thomas KM. Structural and functional brain development and its relation to cognitive development. Biol Psychol 2000;54:241-57. Arch Phys Med Rehabil Vol 89, May 2008

842

EXECUTIVE ATTENTION AND POSTURAL CONTROL, Reilly

22. Fan J, Flombaum JI, McCandliss BD, Thomas KM, Posner MI. Cognitive and brain consequences of conflict. NeuroImage 2002; 18:42-57. 23. Seidman LJ, Valera EM, Makris N, et al. Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biol Psychiatry 2006;60:1071-80. 24. Gottwald B, Mihajlovic A, Wilde B, Mehdorn HM. Does the cerebellum contribute to specific aspects of attention? Neuropsychologia 2003;1452-60. 25. Ravizza SM, Ivry RB. Comparison of the basa ganglia and cerebellum in shifting attention. J Neuro Cogn Sci 2001;13:285-97. 26. Akshoomoff NA, Courchesne E. ERP evidence for a shifting attention deficit in patients with damage to the cerebellum. J Cogn Neuro Sci 1994;6:388-99. 27. Courchesne E, Townsend J, Akshoomoff NA, et al. Impairment in shifting attention in autistic and cerebellar patients. Behav Neurosci 1994;108:848-65. 28. Okoshi Y, Itoh M, Takashima S. Characteristic neuropathology and plasticity in periventricular leukomalacia. Pediatr Neurol 2001;25:221-6. 29. Christ SE, White DA, Brunstrom JE, Abrams RA. Inhibitory control following perinatal brain injury. Neuropsychology 2003; 17:171-8. 30. Cherng RJ, Lee HY, Su FC. Frequency spectral characteristics of standing balance in children and young adults. Med Eng Phys 2003;25:509-15. 31. Forssberg H, Nashner L. Ontogenetic development of postural control in man: adaptation to altered support and visual conditions during stance. J Neurosci 1982;2:545-52. 32. Riach CL, Hayes KC. Maturation of postural sway in young children. Dev Med Child Neurol 1987;29:650-8. 33. Sakaguchi M, Taguchi K, Miyashita Y, Katsuno S. Changes with aging in head and center of foot pressure sway in children. Int J Pediatr Otorhinolaryngol 1994;29:101-9. 34. Shumway-Cook A, Woollacott M. The growth of stability: postural control from a developmental perspective. J Mot Behav 1985;17:131-47. 35. Rose J, Wolff DR, Jones VK, Bloch DA, Oehlert JW, James GG. Postural balance in children with cerebral palsy. Dev Med Child Neurol 2002;44:58-63. 36. Achenbach, T. Child behavior checklist. Burlington: Univ Vermont; 2001. 37. Franjoine MR, Gunther JS, Taylor MJ. Pediatric Balance Scale: a modified version of the Berg balance scale for the school age child

Arch Phys Med Rehabil Vol 89, May 2008

38.

39.

40.

41.

42. 43. 44.

45.

46.

47.

48. 49.

50.

with mild to moderate motor impairment. Pediatr Phys Ther 2003;15:114-28. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997;39:214-23. Vogel EK, Woodman GF, Luck SJ. Storage of features, conjunctions, and objects in visual working memory. J Exp Psychol Hum Percep Perform 2001;27:92-114. Kane MJ, Bleckley MK, Conway AR, Engle RW. A controlledattention view of working memory capacity: individual differences in memory span and the control of visual orienting. J Exp Psychol Gen 2001;130:169-83. Kane MJ, Engle RW. Working memory capacity and the control of attention: the contributions of goal-neglect, response competition, and task set to Stroop interference. J Exp Psychol Gen 2003;132:47-70. Awh E, Jonides J. Overlapping mechanisms of attention and working memory. Trends Cogn Sci 2001;5:119-26. Awh E, Vogel EK, Oh SH. Interactions between attention and working memory. Neuroscience 2006;139:201-8. Cowan N, Naveh-Benjamin M, Kilb A, Saults JS. Life span development of visual working memory: when is feature binding difficult? Dev Psychol 2006;42:1089-102. Shumway-Cook A, Woollacott MH. Motor control: translating research into clinical practice. Philadelphia: Lippincott Williams & Wilkins; 2006. Winter DA, Eng P. Kinetics: our window into the goals and strategies of the central nervous system. Behav Brain Res 1995; 67:111-20. Yardley L, Gardner M, Leadbetter A, Lavie N. Effect of articulatory and mental tasks on postural control. NeuroReport 1999; 10:215-9. Rosenthal R, Rosnow RL, Rubin DB. Contrasts and effect sizes in behavioral research. Cambridge: Cambridge Univ Pr; 2000. Allen G, Buxton RB, Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement. Science 1997;1940-3. Craft S, Park TS, White DA, Schatz J, Noetzel M, Arnold S. Changes in cognitive performance in children with spastic diplegic cerebral palsy following selective dorsal rhizotomy. Pediatr Neurosurg 1995;23:68-75.

Suppliers a. The MathWorks Inc, 3 Apple Hill Dr, Natick, MA 01760-2098. b. Version 2.04; Cedrus Inc, 1121 S Meyler St, San Pedro, CA 90731.