Authors: Ying-Hui Lin, PT, MS Pei-Fang Tang, PT, PhD Yao-Hung Wang, MD, PhD Janice J. Eng, PT/OT, PhD Keh-Chung Lin, OT, PhD Lu Lu, MD, PhD Jiann-Shing Jeng, MD, PhD Shih-Ching Chen, MD, PhD
Stroke
ORIGINAL RESEARCH ARTICLE
Affiliations: From the School and Graduate Institute of Physical Therapy, College of Medicine (Y-HL, P-FT), Graduate Institute of Brain and Mind Sciences, College of Medicine (P-FT), and School of Occupational Therapy, College of Medicine (K-CL), National Taiwan University, Taipei, Taiwan; Department of Physical Medicine and Rehabilitation (Y-HL, K-CL, LL), Physical Therapy Center (P-FT), Department of Medical Imaging (Y-HW), and Department of Neurology (J-SJ), National Taiwan University Hospital, Taipei, Taiwan; Department of Physical Therapy, University of British Columbia, Vancouver, British Columbia, Canada (JJE); and Department of Physical Medicine and Rehabilitation, Taipei Medical University Hospital, Taipei, Taiwan (S-CC).
Correspondence: All correspondence and requests for reprints should be addressed to: Pei-Fang Tang, PT, PhD, School and Graduate Institute of Physical Therapy, College of Medicine, National Taiwan University, Floor 3, No. 17, Xuzhou Rd, Zhongzheng District, Taipei, 100, Taiwan, Republic of China.
Disclosures: Supported by the National Health Research Institutes grants NHRI-EX95-9210EC and NHRI-EX96-9210EC. Presented at the Annual Conference of Taiwan Stroke Society in 2013. Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
0894-9115/14/9310-0849 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000093
Reactive Postural Control Deficits in Patients with Posterior Parietal Cortex Lesions After Stroke and the Influence of Auditory Cueing ABSTRACT Lin Y-H, Tang P-F, Wang Y-H, Eng JJ, Lin K-C, Lu L, Jeng J-S, Chen S-C: Reactive postural control deficits in patients with posterior parietal cortex lesions after stroke and the influence of auditory cueing. Am J Phys Med Rehabil 2014;93:849Y859.
Objective: The purpose of this study was to investigate the ways in which stroke-induced posterior parietal cortex (PPC) lesions affect reactive postural responses and whether providing auditory cues modulates these responses.
Design: Seventeen hemiparetic patients after stroke, nine with PPC lesions (PPCLesion) and eight with intact PPCs (PPCSpared), and nine age-matched healthy adults completed a lateral-pull perturbation experiment under noncued and cued conditions. The activation rates of the gluteus medius muscle ipsilateral (GMi) and contralateral to the pull direction, the rates of occurrence of three types of GM activation patterns, and the GMi contraction latency were investigated.
Results: In noncued pulls toward the paretic side, of the three groups, the PPCLesion group exhibited the lowest activation rate (56%) of the GMi (P G 0.05), which is the primary postural muscle involved in this task, and the highest rate of occurrence (33%) of the gluteus medius muscle contralateralYactivation-only pattern (P G 0.05), which is a compensatory activation pattern. In contrast, in cued pulls toward the paretic side, the PPCLesion group was able to increase the activation rate of the GMi to a level (81%) such that there became no significant differences in activation rate of the GMi among the three groups (P 9 0.05). However, there were no significant differences in the GM activation patterns and GMi contraction latency between the noncued and cued conditions for the PPCLesion group (P 9 0.05).
Conclusions: The PPCLesion patients had greater deficits in recruiting paretic muscles and were more likely to use the compensatory muscle activation pattern for postural reactions than the PPCSpared patients, suggesting that PPC is part of the neural circuitry involved in reactive postural control in response to lateral perturbations. The auditory cueing used in this study, however, did not significantly modify the muscle activation patterns in the PPCLesion patients. More research is needed to explore the type and structure of cueing that could effectively improve patterns and speed of postural responses in these patients. Key Words:
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Stroke, Posterior Parietal Cortex, Posture, Cues
How PPC Lesions Affect Reactive Postural Responses Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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arious studies have suggested that the posterior parietal cortex (PPC) plays an important role in multimodal sensory integration and attention.1Y3 Lesions or dysfunction of the PPC are shown to lead to deficits in directing attention and transforming sensory information into motion plans in animal and human studies.4Y8 Reactive postural control, which incorporates attention9 and multimodal sensory integration,2 likely requires an intact PPC. However, few studies have investigated the relationship between PPC lesions and postural control. Perennou and colleagues10 reported that, compared with stroke patients with structurally intact PPCs, stroke patients with lesions to the temporoparietal junction of the PPC exhibited poorer sitting balance control while sitting on a rocking board, which could tilt in the roll axis, and trying not to fall. Perennou et al.11 also found that stroke patients with temporoparietal junction lesions and visuospatial neglect demonstrated improved sitting balance in the same task after transcutaneous electric stimulation of the sternocleidomastoid muscle on the hemiplegic side. These findings suggest that temporoparietal junction lesionYinduced deficits in attention and sensorimotor integration may contribute to sitting instability in patients with PPC lesions. Furthermore, such sitting instability may be improved by providing patients with appropriate somatosensory inputs. No studies to date have investigated the exact relationship between neuromuscular postural responses and PPC lesions in human reactive postural tasks. The ways in which PPC lesions affect reactive postural responses in stance and whether providing auditory cues can modify these responses remain unclear. Therefore, the aim of the present study was to examine reactive postural responses in stroke patients with PPC lesions (PPCLesion), stroke patients with spared PPCs (PPCSpared), and healthy subjects by using a lateral-pull perturbation paradigm. Research using the lateral-push perturbation paradigm has shown that the generation of hip abductor moment or the activation of the gluteus medius muscle ipsilateral (GMi) to the push direction is the primary postural response required for balance recovery in this task.12,13 Activation of only the GMi (GMi-activation-only pattern) has been found to be the most parsimonious postural response in lateral-push perturbation paradigm.13 The authors’ own pilot studies have found that, as in lateralpush perturbation, the GMi-activation-only pattern is the most parsimonious postural response to lateralpull perturbation. The lateral-pull perturbation
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paradigm therefore allows for comparisons between the methods used by PPCLesion and PPCSpared stroke patients to organize their postural responses in the paretic and nonparetic sides of the body. In particular, two hypotheses were tested in this study. First, it was hypothesized that the PPCLesion group would present poorer reactive postural responses compared with the PPCSpared and healthy groups by showing less frequent activation of the GMi muscle and more frequent use of compensatory muscle activation patterns other than the GMi-activation-only pattern in response to lateral-pull perturbation toward the paretic side. Second, it was hypothesized that when a valid auditory cue was provided before the perturbation toward the paretic side, the PPCLesion subjects would increase their activation rate of the GMi muscle and rate of occurrence of the GMi-activation-only pattern so that they became similar to the healthy subjects and the PPCSpared stroke patients on these characteristics of their reactive postural responses.
METHODS Subjects Nine PPCLesion stroke patients, eight PPCSpared stroke patients, and nine age-matched healthy adults participated in this study (Tables 1 and 2). All 17 patients were (1) diagnosed with single-onset cerebral ischemic stroke via clinical and neuroimaging (computed tomography or magnetic resonance imaging) findings more than 30 days after onset, (2) unilaterally affected, (3) free of other neurologic diseases, and (4) able to stand independently for 20 mins without using a supporting device. Patients with hearing loss or communication problems were excluded from the study. All participants scored 24 or higher on the MiniYMental State Examination (MMSE)14 and had no other disorders that might affect standing balance. The assignment of patients to either the PPCLesion or the PPCSpared group was conducted according to readings of the patients’ brain images (Figs. 1A, B). A radiologist (Y.-H. Wang) performed image readings and determined the lesion site for all but three subjects (PPCSpared patient 2 and PPCLesion patients 1 and 2) whose images were not accessible to the authors. Their lesion sites were determined on the basis of the image readings reported by licensed radiologists at the hospitals where these patients were admitted at onset of stroke. All subjects gave informed consent, which was approved by the institutional review board, before participating in this study.
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TABLE 1 Clinical findings of individual stroke patients Subject
FM-Motor FM-Sensation Lesion Lesion Territory (0Y34) (0Y24) Hemisphere (and Size in Area)
PPCSpared group 1 34 2 31 3 34
24 17 22
R L R
4
27
21
R
5
17
16
R
6
32
22
L
7
32
22
L
8
32
24
R
PPCLesion group 1 23 2 32 3 31
12 18 22
L R R
4
30
18
R
5
31
14
R
6
32
24
L
7
34
22
R
8
33
22
L
9
27
20
L
ACA territory V MCA territory (G1/3) MCA territory (G1/3) MCA territory (92/3) MCA territory (G1/3) MCA territory (G1/3) ACA territory V V MCA territory (G1/3) MCA territory (92/3), PCA MCA territory (1/3~2/3) MCA territory (1/3~2/3), PCA MCA territory (G1/3), ACA MCA territory (1/3~2/3) MCA territory (G 1/3)
Lesion Site in the PPC
Other Brain Lesion Sites
None None None
PFC, SMA F, P T, BG, IC, CR
None
PMC, PFC, BG
None
PMC, M1, T, BG, CR
None
Medial F, BG
None
PMC, T, BG
None
PMC, PFC, M1
Inferior PPC Inferior PPC Inferior PPC
BG, CR, CP BG, CR PMC, M1, S1, CR
Inferior PPC
PMC, M1, S1, O, BG, CR
Inferior PPC
PMC, PFC, M1, S1, O
Inferior PPC
PMC, Broca area, O
Superior and PMC, PFC, M1, S1, O inferior PPC Inferior PPC PMC, M1, S1, Inferior PPC
Insula, opercular regions, anterior T, BG
Em dash indicates unavailable information. ACA, anterior cerebral artery; BG, basal ganglia; CP, cerebral peduncle; CR, corona radiata; F, frontal lobe; FM-Motor, motor component of the Fugl-Meyer Assessment; FM-Sensation, sensory component of the Fugl-Meyer Assessment; IC, internal capsule; L, left; M1, primary motor area; O, occipital lobe; P, parietal lobe; PCA, posterior cerebral artery; PFC, prefrontal cortex; PMC, premotor cortex; R, right; S1, primary sensory cortex; SMA, supplementary motor area; T, temporal lobe.
TABLE 2 Demographics of all three subject groups
Age Sex (male/female) Footedness (L/R) Lesion hemisphere (L/R) Time after stroke onset, days MMSE FM-Motor (0Y34) FM-Sensation (0Y24) FM-ROM (0-20) Berg Balance Scale (0Y56) Neglect (with/without)
Healthy Group (n = 9)
PPCSpared Group (n = 8)
PPCLesion Group (n = 9)
67.9 (13.7) 4/5 0/9 V V 29.1 (1.4) V V V 55.7 (0.7) V
68.6 (10.2) 6/2 V 3/5 345.9 (387.0) 28.6 (1.4) 30.0 (5.6) 21.0 (3.0) 19.5 (0.8) 52.1 (5.6) 1/7
60.8 (13.9) 5/4 V 4/5 331.3 (381.5) 26.6 (2.2) 30.0 (3.4) 19.1 (4.0) 18.8 (1.1) 53.3 (2.6) 1/8
Values are expressed as mean (standard deviation) or number. Em dash indicates not applicable. FM-Motor, motor component of the Fugl-Meyer Assessment; FM-ROM, range of motion component of the Fugl-Meyer Assessment; FM-Sensation, sensory component of the Fugl-Meyer Assessment; L, left; R, right.
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FIGURE 1 Brain images of the PPCSpared subjects (A) and the PPCLesion subjects (B). Fluid attenuation inversion recovery magnetic resonance images were available for most subjects, but two PPCSpared subjects (patients 1 and 8) had only diffusion-weighted images, and one PPCSpared subject (patient 6) had only computed tomography images. Four subjects (PPCSpared: patients 2 and 4; PPCLesion: patients 1 and 2) had only hard copy images and did not have digital image files available. The PPC areas involved are indicated using red ovals; other brain lesion areas are indicated with red arrows. The two images of PPCLesion subject 7 indicate superior (image on the left) and inferior (image on the right) PPC lesions.
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Equipment A Multi-directional Human Pulling System (Advance Instrument Inc, Taipei, Taiwan) was used to provide lateral-pull perturbation at the subject’s waist. The system uses servomotors and cables to deliver pull forces. In this study, the amplitude, maximum velocity, and acceleration of the perturbation were set to 3 cm, 12 cm/sec, and 48 cm/sec2, respectively, using a one-quarter sinusoidal wave displacement profile. These parameters were chosen because the authors’ pilot study revealed that most stroke patients could withstand the perturbation generated by these settings without losing standing balance. A Multi-stimuli Generator (Advance Instrument Inc, Taipei, Taiwan) was used to deliver a prerecorded auditory cue (explicitly saying Bleft[ or Bright[) that lasted 1.5 secs to inform subjects of the pull direction before perturbation. A Bagnoli-8 surface electromyography (EMG) system (DelSys Inc, Boston, MA) was used to collect electrical activity from the bilateral gluteus medius (GM) muscles. Two force plates (AMTI OR6-7; Advanced Mechanical Technology, Inc, Watertown, MA) were used to record forces underneath the feet. Pull perturbation signals (onset, displacement, and velocity), the onset of the auditory cue, EMG signals, and force signals were simultaneously collected at 1000 Hz using the DATAPAC 2000 Data Acquisition Module; these signals were later digitized and analyzed using the DATAPAC 2000 Data Analysis Module (Run Technologies, Mission Viejo, CA).
Procedures All subjects were clinically assessed before pull experiments. The Fugl-Meyer Assessment15 was used to examine sensation (FM-Sensation), motor function (FM-Motor), and passive range of motion (FMROM) of the affected lower extremity of stroke patients. The presence of neglect was assessed using the following tests: line bisection (deviation 9 14% of line length from the midpoint),16 star cancellation (925% small stars missed),17 and figure copying (scored Q1 of 8).18 A positive result on any of these tests indicated neglect. The MMSE and the Berg Balance Scale19 were used to examine cognition and balance, respectively. Footedness of healthy subjects was determined using the Waterloo Footedness QuestionnaireYRevised.20 A trained and experienced licensed physical therapist (Y.-H. Lin) performed the clinical assessments. Lateral-pull experiments were conducted in noncued and cued conditions. There were a total of 12 trials (6 noncued and 6 cued) for each participant. www.ajpmr.com
In each cue condition, there were three rightward and three leftward pull trials. The noncued and cued conditions were counterbalanced, and the pull directions were randomized in each cue condition. Each pull perturbation lasted 0.5 secs. In the cued condition, the foreperiod (the time interval between the cue onset and the perturbation onset) varied between 5, 5.5, and 6 secs. All cues were valid and consistent with the pull direction of the trial. The subjects were given a 3-min rest period after every six trials. In each trial, the subjects initially stood upright with equal weight bearing on both feet. The feet were placed 20 cm apart and externally rotated 15 degrees. To prevent anticipatory responding in both the cued and noncued conditions, the participants were instructed not to move until they felt the pull. The subjects were also instructed to maintain postural stability and minimize stepping as much as possible during and after perturbation.
Data Analyses EMG signals were band pass filtered (20Y250 Hz) and rectified. To characterize each subject group’s postural responses to each perturbation direction and cue condition, the authors investigated the activation rates of the GM muscle ipsilateral (GMi) and contralateral (GMc) to the pull direction and the rates of occurrence of three GM activation patterns among all subjects in the same group. The activation rates of the GMi and GMc for each group in a given perturbation direction and cue condition were calculated as the total number of trials in which the muscle was activated, divided by the total number of trials in the given condition for the subject group. In each trial, onset of muscle activation was defined as muscle activity that started to exceed 2 SD beyond the baseline EMG activity for at least 30 milliseconds.21 Baseline EMG activity was calculated by averaging the signal from 500 milliseconds to 150 milliseconds before pull onset. Three GM activation patterns were observed in this study: (1) GMi-activation-only, (2) GMi/GMc coactivation, and (3) GMc-activation-only (Figs. 2AYC). The rate of occurrence of each activation pattern for each group in a given perturbation direction and cue condition was defined as the total number of trials in which the pattern occurred, divided by the total number of trials in the given condition for the subject group. Because GMi is the primary postural muscle in this task, the authors also analyzed the mean contraction latency of GMi activation for the trials in which this muscle was activated in each perturbation direction and cue condition for each group. In each trial, GMi activation latency was How PPC Lesions Affect Reactive Postural Responses
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FIGURE 2 Representative EMG signals of pattern 1 (GMi-activation-only) muscle activation pattern from a healthy subject (A), pattern 2 (GMi/GMc coactivation) from a PPCSpared subject (B), and pattern 3 (GMc-activation-only) from a PPCLesion subject (C). Time zero and the vertical dashed line indicate perturbation onset. The upward direction for the lateral force data indicates the pull direction.
defined as the time interval from pull perturbation onset to the GMi activation onset.
Statistical Analyses The authors first used the Kolmogorov-Smirnov test and the Levene test to assess the normality of the data and homogeneity of variance, respectively, for continuous variables. Because the normality and homogeneity of variance assumptions were violated for all variables except GMi contraction latency, nonparametric tests were applied in most of the statistical analyses. The Mann-Whitney U test was used to
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analyze differences in the time after stroke onset and the FM-Motor, FM-Sensation, and FM-ROM scores between the patient groups. The Kruskal-Wallis test was used to analyze differences in age, MMSE, and Berg Balance Scale scores among the three groups. The W2 test was used to analyze group differences in sex, lesion side, and the presence of neglect. For the dependent variables characterizing postural responses, the W2 test was used to test between-group differences in GMi and GMc activation rates and the rates of occurrence of GM activation patterns, for each perturbation direction and condition. To further
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test the effects of cueing, the W2 test was also used to test within-group differences in these variables for each perturbation direction across the two cue conditions. A 3 (group) 2 (cue) two-way mixed-effects analysis of variance was applied to test the effects of group, cue condition, and group cue interaction on the GMi activation contraction latency. Because the lesion side (right vs. left) did not cause differences in the dependent variables, the data were not subdivided according to lesioned hemisphere. The patients’ postural responses to perturbations toward the nonparetic and paretic sides were compared with the healthy subjects’ postural responses to rightward (dominant-foot side) and leftward perturbations, respectively. The level of statistical significance was set at P G 0.05 for all comparisons. Significant KruskalWallis test results were followed by the Mann-Whitney U test for multiple comparisons. Bonferroni corrections were made for significant analysis of variance results. All statistical analyses were performed using the Statistical Package for the Social Sciences for Windows (version 17.0).
RESULTS Subjects Figures 1A and B present the brain lesion sites, and Table 1 presents the clinical characteristics of individual stroke patients. The days after stroke onset ranged from 50 to 1783 and from 85 to 1300 days for the PPCSpared and PPCLesion groups, respectively. The cortical and subcortical lesion sites were generally similar between the two patient groups, except that the PPC of all PPCLesion subjects was affected,
and in some PPCLesion subjects, the primary somatosensory cortex (S1) or the occipital lobe was also affected (Table 1). None of the PPCSpared subjects had lesions of the PPC, S1, or occipital lobe. Regarding the extent of PPC lesions, eight of the PPCLesion patients had lesions in the inferior PPC; only one PPCLesion patient had lesions involving both the inferior and superior PPC (Table 1). Table 2 presents the demographic information and clinical test results for all three groups. There were no differences in age, sex, MMSE score, and Berg Balance Scale score among the three groups (P 9 0.05). The two patient groups did not differ in lesion side; time after stroke onset; presence of neglect; and FMMotor, FM-Sensation, and FM-ROM scores (P 9 0.05) (Table 2).
Group Differences in GMi and GMc Activation Rates and GM Activation Patterns in Noncued Perturbation Conditions Between-group analyses revealed that, in response to noncued perturbations toward the nonparetic/right side, all three groups similarly used the GMi as the predominant postural muscle (995% activation rate) (W2 = 0.013, P = 0.993), and the PPCLesion group demonstrated the highest GMc activation rate (W2 = 6.943, P = 0.031) (Table 3). In this condition, all three groups demonstrated activation pattern 1 (GMiactivation-only) predominantly (rate of occurrence 9 70%); however, the PPCLesion group exhibited the lowest rate of occurrence of pattern 1 (W2 = 8.328, P = 0.016) and the highest rate of occurrence
TABLE 3 Activation rates of the GMi and GMc in each condition for three subject groups Perturbation to the nonparetic/right side Noncued GMi Healthy group PPCSpared group PPCLesion group
Cued GMc a
96.3% 95.7% 96.0%
0.0% 17.4%a 24.0%a
GMi
GMc
96.3% 95.2% 88.0%
33.3%b 28.6% 20.0%
Perturbation to the paretic/left side Noncued GMi Healthy group PPCSpared group PPCLesion group a b
a
88.5% 86.4%a 56.0%a
Cued GMc
GMi
GMc
30.8% 40.9% 40.0%
92.0% 90.5% 80.8%
64.0%a,b 33.3%a 30.8%a
Significant difference among groups (P G 0.05). Significant difference between noncued and cued conditions (P G 0.05).
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TABLE 4 Rates of occurrence of three GM activation patterns in each condition for three subject groups Perturbation to the nonparetic/right side Noncued Pattern 1 Healthy group PPCSpared group PPCLesion group
Cued
Pattern 2
a
Pattern 3
a
0.0% 17.4%a 28.0%a
100.0% 82.6%a 72.0%a
0.0% 0.0% 0.0%
Pattern 1 66.7% 70.0% 77.3%
Pattern 2
b
Pattern 3
b
33.3% 30.0% 22.7%
0.0% 0.0% 0.0%
Perturbation to the paretic/left side Noncued
Healthy group PPCSpared group PPCLesion group
Cued
Pattern 1
Pattern 2
Pattern 3
Pattern 1
Pattern 2
Pattern 3
66.7% 57.1% 52.4%
29.2% 33.3% 14.3%
4.2%a 9.5%a 33.0%a
30.4%a,b 68.4%a 68.0%a
69.6%a,b 31.6%a 16.0%a
0.0%a 0.0%a 16.0%a
Pattern 1, GMi-activation-only pattern; pattern 2, GMi/GMc coactivation pattern; pattern 3, GMc-activation-only pattern. a Significant difference among groups (P G 0.05). b Significant difference between noncued and cued conditions (P G 0.05).
of pattern 2 (GMi/GMc coactivation) (W2 = 8.328, P = 0.016) among the three groups (Table 4). In response to noncued perturbations toward the paretic/left side, the PPCLesion group exhibited the lowest GMi activation rate (W2 = 9.16, P = 0.01) of all groups (Table 3) and the highest rate of occurrence of activation pattern 3 (GMc-activationonly) among the three groups (W2 = 8.17, P = 0.017) (Table 4).
activation pattern 3 (W2 = 7.147, P = 0.028) (Table 4). Furthermore, the healthy group exhibited the greatest GMc activation rate (W2 = 6.883, P = 0.032), the lowest rate of occurrence of activation pattern 1 (W2 = 8.704, P = 0.013), and the highest rate of occurrence of activation pattern 2 (W2 = 15.057, P = 0.001) among the three groups in the cued pulls toward the paretic/left side (Tables 3 and 4).
Group Differences in GMi and GMc Activation Rates and GM Activation Patterns in Cued Perturbation Conditions
Within-Group Differences in GMi and GMc Activation Rates and GM Activation Patterns Between Noncued and Cued Perturbation Conditions
In cued pulls toward the nonparetic/right side, there were no group differences in GMi and GMc activation rates (P 9 0.05) (Table 3), neither were there any group differences in the rate of occurrence of three activation patterns (P 9 0.05) (Table 4). In cued pulls toward the paretic/left side, there were also no group differences in GMi activation rates (W2 = 1.71, P = 0.425); however, the PPCLesion group still demonstrated the highest rate of occurrence of
Within-group analyses further tested the effects of cueing and showed that, in paretic side perturbations, the PPCLesion group tended to increase the GMi activation rate from noncued (56.0%) to cued (80.8%) pulls, but the increase did not reach a statistical significance (W2 = 3.632, P = 0.057) (Table 3). There was also no statistical significance in the rates of occurrence of GM activation patterns for the PPCSpared and PPCLesion groups between the noncued
TABLE 5 GMi contraction latency Perturbation to the Paretic/Left Side
Healthy group PPCSpared group PPCLesion group
Perturbation to the Nonparetic/Right Side
Noncued
Cued
Noncued
Cued
127.2 (19.1) 153.1 (48.3) 161.3 (41.5)
128.2 (30.0) 125.2 (28.7) 162.4 (36.7)
134.9 (31.7) 127.1 (13.5) 124.8 (19.0)
131.3 (30.1) 130.0 (23.0) 138.6 (35.1)
Values are expressed as mean (standard deviation) (in milliseconds).
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and cued conditions regardless of the perturbation directions (P 9 0.05) (Table 4). In the healthy group, the GMc activation rate increased from noncued to cued pulls in both perturbation directions (W2 = 10.8, P = 0.001, for rightward pulls; W2 = 5.649, P = 0.017, for leftward pulls) (Table 3). This group also demonstrated a significantly reduced rate of occurrence of activation pattern 1 but a significantly increased rate of occurrence of activation pattern 2 from the noncued to cued conditions for rightward (W2 = 10.8, P = 0.001, for patterns 1 and 2) and leftward (W2 = 6.17, P = 0.013, for pattern 1; W2 = 7.671, P = 0.006, for pattern 2) pulls (Table 4).
Group and Cue Effects on GMi Contraction Latency With regard to the contraction latency of GMi activation, the analysis of variance results revealed no significant simple main effects of group or cue or interaction (group cue) effects on contraction latency of GMi activation in both perturbation directions (Table 5) (for nonparetic/right perturbation, group: F2,21 = 0.073, P = 0.93; cue: F1,21 = 0.682, P = 0.418; group cue: F2,21 = 0.958, P = 0.4; for paretic/left perturbation, group: F2,16 = 1.889, P = 0.183; cue: F1,16 = 1.127, P = 0.304; group cue: F2,16 = 1.516, P = 0.249).
DISCUSSION The major findings of this study are that stroke patients with PPC lesions have greater difficulty recruiting the paretic GM muscle when it is typically needed and more frequently use compensatory muscle patterns for reactive postural control as compared with stroke patients whose PPC is spared and healthy controls. Among the three groups, in noncued perturbations toward the paretic side, the PPCLesion group recruited the GMi the least frequently and demonstrated the GMc-activation-only pattern most frequently. These findings support the authors’ first hypothesis, which stated that PPCLesion subjects would present poorer reactive postural control than PPCSpared and healthy subjects. These findings are also consistent with those reported by Perennou et al10,11 regarding balance control in patients with lesions of the temporoparietal junction, which is the main portion of the inferior PPC. However, the finding of only a marginal change in the activation rates of GMi and no significant changes in occurrence rates of GM activation patterns for the PPCLesion subjects from the noncued to cued conditions failed to support the www.ajpmr.com
second hypothesis, which stated that the PPCLesion subjects would benefit from valid auditory cues for organizing postural responses. The possible explanations for these findings are discussed below.
Role of PPC in Reactive Postural Responses to Lateral Perturbation The authors reasoned that patients’ clinical characteristics, including the time after stroke onset, deficits in sensorimotor function, the side of the lesioned hemisphere, and the presence of neglect, were unlikely to explain poorer postural responses in the PPCLesion subjects observed in noncued conditions because both patient groups were similar in these characteristics. The primary differences between these two patient groups are the brain lesion sites with regard to PPC lesions and that, in some PPCLesion subjects, the S1 or the occipital lobe was also affected. The inferior branch of the middle cerebral artery (MCA) supplies the PPC, S1, and the occipital lobe. The PPCLesion subjects may have exhibited poorer reactive postural responses because of lesions of the PPC and the occipital lobe or S1. However, further analysis revealed that, among the PPCLesion subjects, those with S1 or occipital lesions (patients 3Y8) demonstrated higher GMi activation rates (80%Y85% vs. 25%Y40%) and used the GMi-activation-only pattern more frequently (82%Y88% vs. 20%Y31%) than those who did not have these lesions (patients 1, 2, and 9). Therefore, poorer postural responses in PPCLesion subjects are unlikely to be caused by lesions of the occipital lobe and/or S1. Rather, they are more likely the direct result of PPC lesions, especially the inferior PPC lesions, because all of the PPCLesion subjects had lesions in the inferior PPC and only one of them had lesions in both the superior and inferior PPC. The PPC is known to be involved in directing attention toward stimuli, integrating multimodality sensory information, and performing sensorimotor transformation.1,3 PPC lesionYinduced deficits in these cognitive and sensorimotor information processing functions may have contributed to the poorer lateral reactive postural responses in the PPCLesion subjects. In the studies reported by Perennou and colleagues,10,11 stroke patients with lesions to the temporoparietal junction of the PPC exhibited poorer self-regulated lateral sitting balance than stroke patients with structurally intact PPCs. Their sitting balance task required both proactive and reactive control. This study was the first one that focused on the role of PPC in reactive balance control in standing. Furthermore, the authors found no significant differences How PPC Lesions Affect Reactive Postural Responses
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in the reactive postural responses between the subjects with right and left PPC lesions in noncued perturbation toward the paretic side (activation rate of the GMi: 61.5% and 50%, respectively; P = 0.561) and the nonparetic side (activation rate of the GMi: 92.3% and 100%, respectively; P = 0.327). The authors speculate that the PPC regions of both hemispheres contribute to the neural circuitry responsible for reactive postural control in standing. More research will be needed to understand whether the PPC is also crucial in reactive balance control in other directions.
Influence of Auditory Cueing on Reactive Postural Responses to Lateral Perturbation In the current study, a marginal positive effect of cueing was found on paretic GM recruitment for the PPCLesion group, and this marginal effect may have contributed to the similarity of GMi activation rates among the three subject groups in the cued pulls toward the paretic side. However, this effect was not large enough to result in statistically significant within-group differences in GMi activation rate. There were also no significant cue effects on occurrence rates of GM activation patterns or the contraction latency of GMi activation for both the PPCLesion and PPCSpared groups. These findings differed from those reported by Badke and colleagues,22 which demonstrated that stroke patients exhibited improved postural response organization and shortened muscle contraction latency after receiving correct visual and auditory cues regarding the timing and direction of upcoming platform perturbation. Although these authors did not provide information regarding patients’ brain lesion sites, it is unlikely that the differences in brain lesion sites contribute to the discrepancies between their findings and those of this study because there were no significant cue effects on investigated postural response measures for this study’s PPCSpared group either. The power analysis of this study showed that the power for within-group comparisons to investigate cue effects was mostly between 0.2 and 0.9 for the healthy group, less than 0.2 for the PPCSpared group, and less than 0.5 for the PPCLesion group in this study. Thus, one of the reasons for the lack of within-group cue effects for the patient groups could be the small sample and the low statistical power. This study’s further analysis showed that either double the number of subjects (to 18) or double the number of trials for each condition (to 6 trials of pulls toward each direction in each cue condition) for each patient group will allow the power
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to reach 0.8 for the within-group comparisons. Further studies using a larger sample of patients or a greater number of trials per condition will be needed for testing cueing effects on postural response organization in PPCLesion stroke patients. The other alternative explanation for the lack of cue effects could be the long foreperiods of the cues used in this study. McChesney et al.23 found that a directionally valid auditory cue given 500 milliseconds before a platform perturbation shortened the contraction latency of postural muscle activation in healthy adults. It has been suggested that when the time difference between cue onset and stimulus onset, known as the foreperiod, exceeds 500 milliseconds, the effect of a cue may decay.24 The authors chose the long foreperiod (5~6 secs) in the present study in consideration of its applicability in clinical setting. However, its length may have reduced the effects of the cue. Further studies are needed to explore the optimal foreperiod of cues that is not only clinically applicable but also effective in improving reactive postural responses of patients with PPC lesions. Different from the stroke patients, in the cued condition, the healthy subjects exhibited increased GMc activation rates and occurrence of the GMi/GMc coactivation pattern. The cue may have increased the healthy subjects’ anxiety levels, leading to a cocontraction strategy for postural control.25
Limitations One primary limitation of this study was that lesion size was not measured in the two stroke patient groups. It is possible that larger brain lesions led to poorer postural responses. However, given the heterogeneity in lesion areas (among the 14 patients with known lesion territories, 2 had lesions in only the anterior cerebral artery territory, 9 had lesions in only the MCA territory, 2 had lesions in both the anterior cerebral artery and MCA territories, and 1 had lesions in both the MCA and posterior cerebral artery territories) and the types of available brain images, it was difficult and less meaningful to quantify total brain lesion volumes. To rule out potential confounding variables on postural responses that were related to lesion severity, the participants were matched on motor deficits between groups. Therefore, it is unlikely that poorer reactive postural responses of the PPCLesion group were caused by differences in brain lesion severity. However, future studies may be needed to investigate whether brain lesion size in the PPC area affects the organization of reactive postural responses. Another limitation of the
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study relates to its small sample size. As mentioned previously, the small sample and the low statistical power may be one of the reasons for the nonsignificant within-group findings for the cue effect.
CONCLUSIONS
ward reinterpreting optic ataxia. Nat Neurosci 2000;3: 729Y36 9. Redfern MS, Muller ML, Jennings JR, et al: Attentional dynamics in postural control during perturbations in young and older adults. J Gerontol A Biol Sci Med Sci 2002;57:B298Y303 10. Perennou DA, Leblond C, Amblard B, et al: The polymodal sensory cortex is crucial for controlling lateral postural stability: Evidence from stroke patients. Brain Res Bull 2000;53:359Y65
The authors found that the PPCLesion patients had greater deficits in recruiting paretic muscles and were more likely to use compensatory muscle activation patterns for postural reactions than the PPCSpared patients. These findings suggest that PPC is part of the neural circuitry involved in reactive postural control in response to lateral perturbations. Accurate auditory cueing with long foreperiods did not seem to effectively improve paretic muscle recruitment and the organization of muscle activation patterns in PPCLesion patients in response to unexpected lateral pulls. More research is needed to explore the type and structure of cueing that could effectively improve muscle recruitment, muscle organization patterns, and speed of postural responses in these patients.
12. Rietdyk S, Patla AE, Winter DA, et al: Balance recovery from medio-lateral perturbations of the upper body during standing. J Biomech 1999;32:1149Y58
ACKNOWLEDGMENTS
15. Fugl-Meyer AR, Jaasko L, Leyman I, et al: The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 1975;7:13Y31
The authors thank all of the participants for their involvement in this study and Tsan-Hon Liou, MD, PhD, and Tung-Chou Li, MD, for assisting with subject recruitment. REFERENCES 1. Andersen RA, Cui H: Intention, action planning, and decision making in parietal-frontal circuits. Neuron 2009;63:568Y83
11. Perennou DA, Leblond C, Amblard B, et al: Transcutaneous electric nerve stimulation reduces neglectrelated postural instability after stroke. Arch Phys Med Rehabil 2001;82:440Y8
13. Kirker SGB, Jenner JR, Simpson DS, et al: Changing patterns of postural hip muscle activity during recovery from stroke. Clin Rehabil 2000;14:618Y26 14. Folstein MF, Folstein SE, McHugh PR: BMini-mental state[. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189Y98
16. Schenkenberg T, Bradford DC, Ajax ET: Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology 1980;30:509Y17 17. Halligan PW, Marshall JC, Wade DT: Visuospatial neglect: Underlying factors and test sensitivity. Lancet 1989;2:908Y11 18. Ogden JA: Contralesional neglect of constructed visual images in right and left brain-damaged patients. Neuropsychologia 1985;23:273Y7
2. Horak FB, Hlavacka F, Shupert CL: Vestibular-somatosensory interactions for human posture, in Mergner T, Hlavacka F (eds): Multisensory Control of Posture. New York, NY, Plenum Press, 1995, pp 237Y42
19. Berg K, Wood-Dauphinee S, Williams JI, et al: Measuring balance in the elderly: Preliminary development of an instrument. Physiother Can 1989;41:304Y11
3. Corbetta M, Shulman GL: Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 2002;3:201Y15
20. Elias LJ, Bryden MP, Bulman-Fleming MB: Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia 1998;36:37Y43
4. Buneo CA, Andersen RA: The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 2006;44:2594Y606
21. Moffroid M, Tranowski J, Ricamate A, et al: Computer solutions to identify EMG latency of automatic postural reactions. IEEE Eng Med Biol Mag 1992;11:48Y51
5. Della-Maggiore V, Malfait N, Ostry DJ, et al: Stimulation of the posterior parietal cortex interferes with arm trajectory adjustments during the learning of new dynamics. J Neurosci 2004;24:9971Y6 6. Fogassi L, Luppino G: Motor functions of the parietal lobe. Curr Opin Neurobiol 2005;15:626Y31 7. Mattingley JB, Husain M, Rorden C, et al: Motor role of human inferior parietal lobe revealed in unilateral neglect patients. Nature 1998;392:179Y82 8. Pisella L, Grea H, Tilikete C, et al: An Fautomatic pilot_ for the hand in human posterior parietal cortex: Towww.ajpmr.com
22. Badke MB, Duncan PW, Di Fabio RP: Influence of prior knowledge on automatic and voluntary postural adjustments in healthy and hemiplegic subjects. Phys Ther 1987;67:1495Y500 23. McChesney JW, Sveistrup H, Woollacott MH: Influence of auditory precuing on automatic postural responses. Exp Brain Res 1996;108:315Y20 24. Posner M, Boies S: Components of attention. Psychol Rev 1971;78:391Y408 25. Davis JR, Campbell AD, Adkin AL, et al: The relationship between fear of falling and human postural control. Gait Posture 2009;29:275Y9
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ORIGINAL RESEARCH ARTICLE
Affiliations: From the School and Graduate Institute of Physical Therapy, College of Medicine (Y-HL, P-FT), Graduate Institute of Brain and Mind Sciences, College of Medicine (P-FT), and School of Occupational Therapy, College of Medicine (K-CL), National Taiwan University, Taipei, Taiwan; Department of Physical Medicine and Rehabilitation (Y-HL, K-CL, LL), Physical Therapy Center (P-FT), Department of Medical Imaging (Y-HW), and Department of Neurology (J-SJ), National Taiwan University Hospital, Taipei, Taiwan; Department of Physical Therapy, University of British Columbia, Vancouver, British Columbia, Canada (JJE); and Department of Physical Medicine and Rehabilitation, Taipei Medical University Hospital, Taipei, Taiwan (S-CC).
Correspondence: All correspondence and requests for reprints should be addressed to: Pei-Fang Tang, PT, PhD, School and Graduate Institute of Physical Therapy, College of Medicine, National Taiwan University, Floor 3, No. 17, Xuzhou Rd, Zhongzheng District, Taipei, 100, Taiwan, Republic of China.
Disclosures: Supported by the National Health Research Institutes grants NHRI-EX95-9210EC and NHRI-EX96-9210EC. Presented at the Annual Conference of Taiwan Stroke Society in 2013. Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
0894-9115/14/9310-0849 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000093
Reactive Postural Control Deficits in Patients with Posterior Parietal Cortex Lesions After Stroke and the Influence of Auditory Cueing ABSTRACT Lin Y-H, Tang P-F, Wang Y-H, Eng JJ, Lin K-C, Lu L, Jeng J-S, Chen S-C: Reactive postural control deficits in patients with posterior parietal cortex lesions after stroke and the influence of auditory cueing. Am J Phys Med Rehabil 2014;93:849Y859.
Objective: The purpose of this study was to investigate the ways in which stroke-induced posterior parietal cortex (PPC) lesions affect reactive postural responses and whether providing auditory cues modulates these responses.
Design: Seventeen hemiparetic patients after stroke, nine with PPC lesions (PPCLesion) and eight with intact PPCs (PPCSpared), and nine age-matched healthy adults completed a lateral-pull perturbation experiment under noncued and cued conditions. The activation rates of the gluteus medius muscle ipsilateral (GMi) and contralateral to the pull direction, the rates of occurrence of three types of GM activation patterns, and the GMi contraction latency were investigated.
Results: In noncued pulls toward the paretic side, of the three groups, the PPCLesion group exhibited the lowest activation rate (56%) of the GMi (P G 0.05), which is the primary postural muscle involved in this task, and the highest rate of occurrence (33%) of the gluteus medius muscle contralateralYactivation-only pattern (P G 0.05), which is a compensatory activation pattern. In contrast, in cued pulls toward the paretic side, the PPCLesion group was able to increase the activation rate of the GMi to a level (81%) such that there became no significant differences in activation rate of the GMi among the three groups (P 9 0.05). However, there were no significant differences in the GM activation patterns and GMi contraction latency between the noncued and cued conditions for the PPCLesion group (P 9 0.05).
Conclusions: The PPCLesion patients had greater deficits in recruiting paretic muscles and were more likely to use the compensatory muscle activation pattern for postural reactions than the PPCSpared patients, suggesting that PPC is part of the neural circuitry involved in reactive postural control in response to lateral perturbations. The auditory cueing used in this study, however, did not significantly modify the muscle activation patterns in the PPCLesion patients. More research is needed to explore the type and structure of cueing that could effectively improve patterns and speed of postural responses in these patients. Key Words:
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Stroke, Posterior Parietal Cortex, Posture, Cues
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arious studies have suggested that the posterior parietal cortex (PPC) plays an important role in multimodal sensory integration and attention.1Y3 Lesions or dysfunction of the PPC are shown to lead to deficits in directing attention and transforming sensory information into motion plans in animal and human studies.4Y8 Reactive postural control, which incorporates attention9 and multimodal sensory integration,2 likely requires an intact PPC. However, few studies have investigated the relationship between PPC lesions and postural control. Perennou and colleagues10 reported that, compared with stroke patients with structurally intact PPCs, stroke patients with lesions to the temporoparietal junction of the PPC exhibited poorer sitting balance control while sitting on a rocking board, which could tilt in the roll axis, and trying not to fall. Perennou et al.11 also found that stroke patients with temporoparietal junction lesions and visuospatial neglect demonstrated improved sitting balance in the same task after transcutaneous electric stimulation of the sternocleidomastoid muscle on the hemiplegic side. These findings suggest that temporoparietal junction lesionYinduced deficits in attention and sensorimotor integration may contribute to sitting instability in patients with PPC lesions. Furthermore, such sitting instability may be improved by providing patients with appropriate somatosensory inputs. No studies to date have investigated the exact relationship between neuromuscular postural responses and PPC lesions in human reactive postural tasks. The ways in which PPC lesions affect reactive postural responses in stance and whether providing auditory cues can modify these responses remain unclear. Therefore, the aim of the present study was to examine reactive postural responses in stroke patients with PPC lesions (PPCLesion), stroke patients with spared PPCs (PPCSpared), and healthy subjects by using a lateral-pull perturbation paradigm. Research using the lateral-push perturbation paradigm has shown that the generation of hip abductor moment or the activation of the gluteus medius muscle ipsilateral (GMi) to the push direction is the primary postural response required for balance recovery in this task.12,13 Activation of only the GMi (GMi-activation-only pattern) has been found to be the most parsimonious postural response in lateral-push perturbation paradigm.13 The authors’ own pilot studies have found that, as in lateralpush perturbation, the GMi-activation-only pattern is the most parsimonious postural response to lateralpull perturbation. The lateral-pull perturbation
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paradigm therefore allows for comparisons between the methods used by PPCLesion and PPCSpared stroke patients to organize their postural responses in the paretic and nonparetic sides of the body. In particular, two hypotheses were tested in this study. First, it was hypothesized that the PPCLesion group would present poorer reactive postural responses compared with the PPCSpared and healthy groups by showing less frequent activation of the GMi muscle and more frequent use of compensatory muscle activation patterns other than the GMi-activation-only pattern in response to lateral-pull perturbation toward the paretic side. Second, it was hypothesized that when a valid auditory cue was provided before the perturbation toward the paretic side, the PPCLesion subjects would increase their activation rate of the GMi muscle and rate of occurrence of the GMi-activation-only pattern so that they became similar to the healthy subjects and the PPCSpared stroke patients on these characteristics of their reactive postural responses.
METHODS Subjects Nine PPCLesion stroke patients, eight PPCSpared stroke patients, and nine age-matched healthy adults participated in this study (Tables 1 and 2). All 17 patients were (1) diagnosed with single-onset cerebral ischemic stroke via clinical and neuroimaging (computed tomography or magnetic resonance imaging) findings more than 30 days after onset, (2) unilaterally affected, (3) free of other neurologic diseases, and (4) able to stand independently for 20 mins without using a supporting device. Patients with hearing loss or communication problems were excluded from the study. All participants scored 24 or higher on the MiniYMental State Examination (MMSE)14 and had no other disorders that might affect standing balance. The assignment of patients to either the PPCLesion or the PPCSpared group was conducted according to readings of the patients’ brain images (Figs. 1A, B). A radiologist (Y.-H. Wang) performed image readings and determined the lesion site for all but three subjects (PPCSpared patient 2 and PPCLesion patients 1 and 2) whose images were not accessible to the authors. Their lesion sites were determined on the basis of the image readings reported by licensed radiologists at the hospitals where these patients were admitted at onset of stroke. All subjects gave informed consent, which was approved by the institutional review board, before participating in this study.
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TABLE 1 Clinical findings of individual stroke patients Subject
FM-Motor FM-Sensation Lesion Lesion Territory (0Y34) (0Y24) Hemisphere (and Size in Area)
PPCSpared group 1 34 2 31 3 34
24 17 22
R L R
4
27
21
R
5
17
16
R
6
32
22
L
7
32
22
L
8
32
24
R
PPCLesion group 1 23 2 32 3 31
12 18 22
L R R
4
30
18
R
5
31
14
R
6
32
24
L
7
34
22
R
8
33
22
L
9
27
20
L
ACA territory V MCA territory (G1/3) MCA territory (G1/3) MCA territory (92/3) MCA territory (G1/3) MCA territory (G1/3) ACA territory V V MCA territory (G1/3) MCA territory (92/3), PCA MCA territory (1/3~2/3) MCA territory (1/3~2/3), PCA MCA territory (G1/3), ACA MCA territory (1/3~2/3) MCA territory (G 1/3)
Lesion Site in the PPC
Other Brain Lesion Sites
None None None
PFC, SMA F, P T, BG, IC, CR
None
PMC, PFC, BG
None
PMC, M1, T, BG, CR
None
Medial F, BG
None
PMC, T, BG
None
PMC, PFC, M1
Inferior PPC Inferior PPC Inferior PPC
BG, CR, CP BG, CR PMC, M1, S1, CR
Inferior PPC
PMC, M1, S1, O, BG, CR
Inferior PPC
PMC, PFC, M1, S1, O
Inferior PPC
PMC, Broca area, O
Superior and PMC, PFC, M1, S1, O inferior PPC Inferior PPC PMC, M1, S1, Inferior PPC
Insula, opercular regions, anterior T, BG
Em dash indicates unavailable information. ACA, anterior cerebral artery; BG, basal ganglia; CP, cerebral peduncle; CR, corona radiata; F, frontal lobe; FM-Motor, motor component of the Fugl-Meyer Assessment; FM-Sensation, sensory component of the Fugl-Meyer Assessment; IC, internal capsule; L, left; M1, primary motor area; O, occipital lobe; P, parietal lobe; PCA, posterior cerebral artery; PFC, prefrontal cortex; PMC, premotor cortex; R, right; S1, primary sensory cortex; SMA, supplementary motor area; T, temporal lobe.
TABLE 2 Demographics of all three subject groups
Age Sex (male/female) Footedness (L/R) Lesion hemisphere (L/R) Time after stroke onset, days MMSE FM-Motor (0Y34) FM-Sensation (0Y24) FM-ROM (0-20) Berg Balance Scale (0Y56) Neglect (with/without)
Healthy Group (n = 9)
PPCSpared Group (n = 8)
PPCLesion Group (n = 9)
67.9 (13.7) 4/5 0/9 V V 29.1 (1.4) V V V 55.7 (0.7) V
68.6 (10.2) 6/2 V 3/5 345.9 (387.0) 28.6 (1.4) 30.0 (5.6) 21.0 (3.0) 19.5 (0.8) 52.1 (5.6) 1/7
60.8 (13.9) 5/4 V 4/5 331.3 (381.5) 26.6 (2.2) 30.0 (3.4) 19.1 (4.0) 18.8 (1.1) 53.3 (2.6) 1/8
Values are expressed as mean (standard deviation) or number. Em dash indicates not applicable. FM-Motor, motor component of the Fugl-Meyer Assessment; FM-ROM, range of motion component of the Fugl-Meyer Assessment; FM-Sensation, sensory component of the Fugl-Meyer Assessment; L, left; R, right.
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FIGURE 1 Brain images of the PPCSpared subjects (A) and the PPCLesion subjects (B). Fluid attenuation inversion recovery magnetic resonance images were available for most subjects, but two PPCSpared subjects (patients 1 and 8) had only diffusion-weighted images, and one PPCSpared subject (patient 6) had only computed tomography images. Four subjects (PPCSpared: patients 2 and 4; PPCLesion: patients 1 and 2) had only hard copy images and did not have digital image files available. The PPC areas involved are indicated using red ovals; other brain lesion areas are indicated with red arrows. The two images of PPCLesion subject 7 indicate superior (image on the left) and inferior (image on the right) PPC lesions.
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Equipment A Multi-directional Human Pulling System (Advance Instrument Inc, Taipei, Taiwan) was used to provide lateral-pull perturbation at the subject’s waist. The system uses servomotors and cables to deliver pull forces. In this study, the amplitude, maximum velocity, and acceleration of the perturbation were set to 3 cm, 12 cm/sec, and 48 cm/sec2, respectively, using a one-quarter sinusoidal wave displacement profile. These parameters were chosen because the authors’ pilot study revealed that most stroke patients could withstand the perturbation generated by these settings without losing standing balance. A Multi-stimuli Generator (Advance Instrument Inc, Taipei, Taiwan) was used to deliver a prerecorded auditory cue (explicitly saying Bleft[ or Bright[) that lasted 1.5 secs to inform subjects of the pull direction before perturbation. A Bagnoli-8 surface electromyography (EMG) system (DelSys Inc, Boston, MA) was used to collect electrical activity from the bilateral gluteus medius (GM) muscles. Two force plates (AMTI OR6-7; Advanced Mechanical Technology, Inc, Watertown, MA) were used to record forces underneath the feet. Pull perturbation signals (onset, displacement, and velocity), the onset of the auditory cue, EMG signals, and force signals were simultaneously collected at 1000 Hz using the DATAPAC 2000 Data Acquisition Module; these signals were later digitized and analyzed using the DATAPAC 2000 Data Analysis Module (Run Technologies, Mission Viejo, CA).
Procedures All subjects were clinically assessed before pull experiments. The Fugl-Meyer Assessment15 was used to examine sensation (FM-Sensation), motor function (FM-Motor), and passive range of motion (FMROM) of the affected lower extremity of stroke patients. The presence of neglect was assessed using the following tests: line bisection (deviation 9 14% of line length from the midpoint),16 star cancellation (925% small stars missed),17 and figure copying (scored Q1 of 8).18 A positive result on any of these tests indicated neglect. The MMSE and the Berg Balance Scale19 were used to examine cognition and balance, respectively. Footedness of healthy subjects was determined using the Waterloo Footedness QuestionnaireYRevised.20 A trained and experienced licensed physical therapist (Y.-H. Lin) performed the clinical assessments. Lateral-pull experiments were conducted in noncued and cued conditions. There were a total of 12 trials (6 noncued and 6 cued) for each participant. www.ajpmr.com
In each cue condition, there were three rightward and three leftward pull trials. The noncued and cued conditions were counterbalanced, and the pull directions were randomized in each cue condition. Each pull perturbation lasted 0.5 secs. In the cued condition, the foreperiod (the time interval between the cue onset and the perturbation onset) varied between 5, 5.5, and 6 secs. All cues were valid and consistent with the pull direction of the trial. The subjects were given a 3-min rest period after every six trials. In each trial, the subjects initially stood upright with equal weight bearing on both feet. The feet were placed 20 cm apart and externally rotated 15 degrees. To prevent anticipatory responding in both the cued and noncued conditions, the participants were instructed not to move until they felt the pull. The subjects were also instructed to maintain postural stability and minimize stepping as much as possible during and after perturbation.
Data Analyses EMG signals were band pass filtered (20Y250 Hz) and rectified. To characterize each subject group’s postural responses to each perturbation direction and cue condition, the authors investigated the activation rates of the GM muscle ipsilateral (GMi) and contralateral (GMc) to the pull direction and the rates of occurrence of three GM activation patterns among all subjects in the same group. The activation rates of the GMi and GMc for each group in a given perturbation direction and cue condition were calculated as the total number of trials in which the muscle was activated, divided by the total number of trials in the given condition for the subject group. In each trial, onset of muscle activation was defined as muscle activity that started to exceed 2 SD beyond the baseline EMG activity for at least 30 milliseconds.21 Baseline EMG activity was calculated by averaging the signal from 500 milliseconds to 150 milliseconds before pull onset. Three GM activation patterns were observed in this study: (1) GMi-activation-only, (2) GMi/GMc coactivation, and (3) GMc-activation-only (Figs. 2AYC). The rate of occurrence of each activation pattern for each group in a given perturbation direction and cue condition was defined as the total number of trials in which the pattern occurred, divided by the total number of trials in the given condition for the subject group. Because GMi is the primary postural muscle in this task, the authors also analyzed the mean contraction latency of GMi activation for the trials in which this muscle was activated in each perturbation direction and cue condition for each group. In each trial, GMi activation latency was How PPC Lesions Affect Reactive Postural Responses
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FIGURE 2 Representative EMG signals of pattern 1 (GMi-activation-only) muscle activation pattern from a healthy subject (A), pattern 2 (GMi/GMc coactivation) from a PPCSpared subject (B), and pattern 3 (GMc-activation-only) from a PPCLesion subject (C). Time zero and the vertical dashed line indicate perturbation onset. The upward direction for the lateral force data indicates the pull direction.
defined as the time interval from pull perturbation onset to the GMi activation onset.
Statistical Analyses The authors first used the Kolmogorov-Smirnov test and the Levene test to assess the normality of the data and homogeneity of variance, respectively, for continuous variables. Because the normality and homogeneity of variance assumptions were violated for all variables except GMi contraction latency, nonparametric tests were applied in most of the statistical analyses. The Mann-Whitney U test was used to
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analyze differences in the time after stroke onset and the FM-Motor, FM-Sensation, and FM-ROM scores between the patient groups. The Kruskal-Wallis test was used to analyze differences in age, MMSE, and Berg Balance Scale scores among the three groups. The W2 test was used to analyze group differences in sex, lesion side, and the presence of neglect. For the dependent variables characterizing postural responses, the W2 test was used to test between-group differences in GMi and GMc activation rates and the rates of occurrence of GM activation patterns, for each perturbation direction and condition. To further
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test the effects of cueing, the W2 test was also used to test within-group differences in these variables for each perturbation direction across the two cue conditions. A 3 (group) 2 (cue) two-way mixed-effects analysis of variance was applied to test the effects of group, cue condition, and group cue interaction on the GMi activation contraction latency. Because the lesion side (right vs. left) did not cause differences in the dependent variables, the data were not subdivided according to lesioned hemisphere. The patients’ postural responses to perturbations toward the nonparetic and paretic sides were compared with the healthy subjects’ postural responses to rightward (dominant-foot side) and leftward perturbations, respectively. The level of statistical significance was set at P G 0.05 for all comparisons. Significant KruskalWallis test results were followed by the Mann-Whitney U test for multiple comparisons. Bonferroni corrections were made for significant analysis of variance results. All statistical analyses were performed using the Statistical Package for the Social Sciences for Windows (version 17.0).
RESULTS Subjects Figures 1A and B present the brain lesion sites, and Table 1 presents the clinical characteristics of individual stroke patients. The days after stroke onset ranged from 50 to 1783 and from 85 to 1300 days for the PPCSpared and PPCLesion groups, respectively. The cortical and subcortical lesion sites were generally similar between the two patient groups, except that the PPC of all PPCLesion subjects was affected,
and in some PPCLesion subjects, the primary somatosensory cortex (S1) or the occipital lobe was also affected (Table 1). None of the PPCSpared subjects had lesions of the PPC, S1, or occipital lobe. Regarding the extent of PPC lesions, eight of the PPCLesion patients had lesions in the inferior PPC; only one PPCLesion patient had lesions involving both the inferior and superior PPC (Table 1). Table 2 presents the demographic information and clinical test results for all three groups. There were no differences in age, sex, MMSE score, and Berg Balance Scale score among the three groups (P 9 0.05). The two patient groups did not differ in lesion side; time after stroke onset; presence of neglect; and FMMotor, FM-Sensation, and FM-ROM scores (P 9 0.05) (Table 2).
Group Differences in GMi and GMc Activation Rates and GM Activation Patterns in Noncued Perturbation Conditions Between-group analyses revealed that, in response to noncued perturbations toward the nonparetic/right side, all three groups similarly used the GMi as the predominant postural muscle (995% activation rate) (W2 = 0.013, P = 0.993), and the PPCLesion group demonstrated the highest GMc activation rate (W2 = 6.943, P = 0.031) (Table 3). In this condition, all three groups demonstrated activation pattern 1 (GMiactivation-only) predominantly (rate of occurrence 9 70%); however, the PPCLesion group exhibited the lowest rate of occurrence of pattern 1 (W2 = 8.328, P = 0.016) and the highest rate of occurrence
TABLE 3 Activation rates of the GMi and GMc in each condition for three subject groups Perturbation to the nonparetic/right side Noncued GMi Healthy group PPCSpared group PPCLesion group
Cued GMc a
96.3% 95.7% 96.0%
0.0% 17.4%a 24.0%a
GMi
GMc
96.3% 95.2% 88.0%
33.3%b 28.6% 20.0%
Perturbation to the paretic/left side Noncued GMi Healthy group PPCSpared group PPCLesion group a b
a
88.5% 86.4%a 56.0%a
Cued GMc
GMi
GMc
30.8% 40.9% 40.0%
92.0% 90.5% 80.8%
64.0%a,b 33.3%a 30.8%a
Significant difference among groups (P G 0.05). Significant difference between noncued and cued conditions (P G 0.05).
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TABLE 4 Rates of occurrence of three GM activation patterns in each condition for three subject groups Perturbation to the nonparetic/right side Noncued Pattern 1 Healthy group PPCSpared group PPCLesion group
Cued
Pattern 2
a
Pattern 3
a
0.0% 17.4%a 28.0%a
100.0% 82.6%a 72.0%a
0.0% 0.0% 0.0%
Pattern 1 66.7% 70.0% 77.3%
Pattern 2
b
Pattern 3
b
33.3% 30.0% 22.7%
0.0% 0.0% 0.0%
Perturbation to the paretic/left side Noncued
Healthy group PPCSpared group PPCLesion group
Cued
Pattern 1
Pattern 2
Pattern 3
Pattern 1
Pattern 2
Pattern 3
66.7% 57.1% 52.4%
29.2% 33.3% 14.3%
4.2%a 9.5%a 33.0%a
30.4%a,b 68.4%a 68.0%a
69.6%a,b 31.6%a 16.0%a
0.0%a 0.0%a 16.0%a
Pattern 1, GMi-activation-only pattern; pattern 2, GMi/GMc coactivation pattern; pattern 3, GMc-activation-only pattern. a Significant difference among groups (P G 0.05). b Significant difference between noncued and cued conditions (P G 0.05).
of pattern 2 (GMi/GMc coactivation) (W2 = 8.328, P = 0.016) among the three groups (Table 4). In response to noncued perturbations toward the paretic/left side, the PPCLesion group exhibited the lowest GMi activation rate (W2 = 9.16, P = 0.01) of all groups (Table 3) and the highest rate of occurrence of activation pattern 3 (GMc-activationonly) among the three groups (W2 = 8.17, P = 0.017) (Table 4).
activation pattern 3 (W2 = 7.147, P = 0.028) (Table 4). Furthermore, the healthy group exhibited the greatest GMc activation rate (W2 = 6.883, P = 0.032), the lowest rate of occurrence of activation pattern 1 (W2 = 8.704, P = 0.013), and the highest rate of occurrence of activation pattern 2 (W2 = 15.057, P = 0.001) among the three groups in the cued pulls toward the paretic/left side (Tables 3 and 4).
Group Differences in GMi and GMc Activation Rates and GM Activation Patterns in Cued Perturbation Conditions
Within-Group Differences in GMi and GMc Activation Rates and GM Activation Patterns Between Noncued and Cued Perturbation Conditions
In cued pulls toward the nonparetic/right side, there were no group differences in GMi and GMc activation rates (P 9 0.05) (Table 3), neither were there any group differences in the rate of occurrence of three activation patterns (P 9 0.05) (Table 4). In cued pulls toward the paretic/left side, there were also no group differences in GMi activation rates (W2 = 1.71, P = 0.425); however, the PPCLesion group still demonstrated the highest rate of occurrence of
Within-group analyses further tested the effects of cueing and showed that, in paretic side perturbations, the PPCLesion group tended to increase the GMi activation rate from noncued (56.0%) to cued (80.8%) pulls, but the increase did not reach a statistical significance (W2 = 3.632, P = 0.057) (Table 3). There was also no statistical significance in the rates of occurrence of GM activation patterns for the PPCSpared and PPCLesion groups between the noncued
TABLE 5 GMi contraction latency Perturbation to the Paretic/Left Side
Healthy group PPCSpared group PPCLesion group
Perturbation to the Nonparetic/Right Side
Noncued
Cued
Noncued
Cued
127.2 (19.1) 153.1 (48.3) 161.3 (41.5)
128.2 (30.0) 125.2 (28.7) 162.4 (36.7)
134.9 (31.7) 127.1 (13.5) 124.8 (19.0)
131.3 (30.1) 130.0 (23.0) 138.6 (35.1)
Values are expressed as mean (standard deviation) (in milliseconds).
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and cued conditions regardless of the perturbation directions (P 9 0.05) (Table 4). In the healthy group, the GMc activation rate increased from noncued to cued pulls in both perturbation directions (W2 = 10.8, P = 0.001, for rightward pulls; W2 = 5.649, P = 0.017, for leftward pulls) (Table 3). This group also demonstrated a significantly reduced rate of occurrence of activation pattern 1 but a significantly increased rate of occurrence of activation pattern 2 from the noncued to cued conditions for rightward (W2 = 10.8, P = 0.001, for patterns 1 and 2) and leftward (W2 = 6.17, P = 0.013, for pattern 1; W2 = 7.671, P = 0.006, for pattern 2) pulls (Table 4).
Group and Cue Effects on GMi Contraction Latency With regard to the contraction latency of GMi activation, the analysis of variance results revealed no significant simple main effects of group or cue or interaction (group cue) effects on contraction latency of GMi activation in both perturbation directions (Table 5) (for nonparetic/right perturbation, group: F2,21 = 0.073, P = 0.93; cue: F1,21 = 0.682, P = 0.418; group cue: F2,21 = 0.958, P = 0.4; for paretic/left perturbation, group: F2,16 = 1.889, P = 0.183; cue: F1,16 = 1.127, P = 0.304; group cue: F2,16 = 1.516, P = 0.249).
DISCUSSION The major findings of this study are that stroke patients with PPC lesions have greater difficulty recruiting the paretic GM muscle when it is typically needed and more frequently use compensatory muscle patterns for reactive postural control as compared with stroke patients whose PPC is spared and healthy controls. Among the three groups, in noncued perturbations toward the paretic side, the PPCLesion group recruited the GMi the least frequently and demonstrated the GMc-activation-only pattern most frequently. These findings support the authors’ first hypothesis, which stated that PPCLesion subjects would present poorer reactive postural control than PPCSpared and healthy subjects. These findings are also consistent with those reported by Perennou et al10,11 regarding balance control in patients with lesions of the temporoparietal junction, which is the main portion of the inferior PPC. However, the finding of only a marginal change in the activation rates of GMi and no significant changes in occurrence rates of GM activation patterns for the PPCLesion subjects from the noncued to cued conditions failed to support the www.ajpmr.com
second hypothesis, which stated that the PPCLesion subjects would benefit from valid auditory cues for organizing postural responses. The possible explanations for these findings are discussed below.
Role of PPC in Reactive Postural Responses to Lateral Perturbation The authors reasoned that patients’ clinical characteristics, including the time after stroke onset, deficits in sensorimotor function, the side of the lesioned hemisphere, and the presence of neglect, were unlikely to explain poorer postural responses in the PPCLesion subjects observed in noncued conditions because both patient groups were similar in these characteristics. The primary differences between these two patient groups are the brain lesion sites with regard to PPC lesions and that, in some PPCLesion subjects, the S1 or the occipital lobe was also affected. The inferior branch of the middle cerebral artery (MCA) supplies the PPC, S1, and the occipital lobe. The PPCLesion subjects may have exhibited poorer reactive postural responses because of lesions of the PPC and the occipital lobe or S1. However, further analysis revealed that, among the PPCLesion subjects, those with S1 or occipital lesions (patients 3Y8) demonstrated higher GMi activation rates (80%Y85% vs. 25%Y40%) and used the GMi-activation-only pattern more frequently (82%Y88% vs. 20%Y31%) than those who did not have these lesions (patients 1, 2, and 9). Therefore, poorer postural responses in PPCLesion subjects are unlikely to be caused by lesions of the occipital lobe and/or S1. Rather, they are more likely the direct result of PPC lesions, especially the inferior PPC lesions, because all of the PPCLesion subjects had lesions in the inferior PPC and only one of them had lesions in both the superior and inferior PPC. The PPC is known to be involved in directing attention toward stimuli, integrating multimodality sensory information, and performing sensorimotor transformation.1,3 PPC lesionYinduced deficits in these cognitive and sensorimotor information processing functions may have contributed to the poorer lateral reactive postural responses in the PPCLesion subjects. In the studies reported by Perennou and colleagues,10,11 stroke patients with lesions to the temporoparietal junction of the PPC exhibited poorer self-regulated lateral sitting balance than stroke patients with structurally intact PPCs. Their sitting balance task required both proactive and reactive control. This study was the first one that focused on the role of PPC in reactive balance control in standing. Furthermore, the authors found no significant differences How PPC Lesions Affect Reactive Postural Responses
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in the reactive postural responses between the subjects with right and left PPC lesions in noncued perturbation toward the paretic side (activation rate of the GMi: 61.5% and 50%, respectively; P = 0.561) and the nonparetic side (activation rate of the GMi: 92.3% and 100%, respectively; P = 0.327). The authors speculate that the PPC regions of both hemispheres contribute to the neural circuitry responsible for reactive postural control in standing. More research will be needed to understand whether the PPC is also crucial in reactive balance control in other directions.
Influence of Auditory Cueing on Reactive Postural Responses to Lateral Perturbation In the current study, a marginal positive effect of cueing was found on paretic GM recruitment for the PPCLesion group, and this marginal effect may have contributed to the similarity of GMi activation rates among the three subject groups in the cued pulls toward the paretic side. However, this effect was not large enough to result in statistically significant within-group differences in GMi activation rate. There were also no significant cue effects on occurrence rates of GM activation patterns or the contraction latency of GMi activation for both the PPCLesion and PPCSpared groups. These findings differed from those reported by Badke and colleagues,22 which demonstrated that stroke patients exhibited improved postural response organization and shortened muscle contraction latency after receiving correct visual and auditory cues regarding the timing and direction of upcoming platform perturbation. Although these authors did not provide information regarding patients’ brain lesion sites, it is unlikely that the differences in brain lesion sites contribute to the discrepancies between their findings and those of this study because there were no significant cue effects on investigated postural response measures for this study’s PPCSpared group either. The power analysis of this study showed that the power for within-group comparisons to investigate cue effects was mostly between 0.2 and 0.9 for the healthy group, less than 0.2 for the PPCSpared group, and less than 0.5 for the PPCLesion group in this study. Thus, one of the reasons for the lack of within-group cue effects for the patient groups could be the small sample and the low statistical power. This study’s further analysis showed that either double the number of subjects (to 18) or double the number of trials for each condition (to 6 trials of pulls toward each direction in each cue condition) for each patient group will allow the power
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to reach 0.8 for the within-group comparisons. Further studies using a larger sample of patients or a greater number of trials per condition will be needed for testing cueing effects on postural response organization in PPCLesion stroke patients. The other alternative explanation for the lack of cue effects could be the long foreperiods of the cues used in this study. McChesney et al.23 found that a directionally valid auditory cue given 500 milliseconds before a platform perturbation shortened the contraction latency of postural muscle activation in healthy adults. It has been suggested that when the time difference between cue onset and stimulus onset, known as the foreperiod, exceeds 500 milliseconds, the effect of a cue may decay.24 The authors chose the long foreperiod (5~6 secs) in the present study in consideration of its applicability in clinical setting. However, its length may have reduced the effects of the cue. Further studies are needed to explore the optimal foreperiod of cues that is not only clinically applicable but also effective in improving reactive postural responses of patients with PPC lesions. Different from the stroke patients, in the cued condition, the healthy subjects exhibited increased GMc activation rates and occurrence of the GMi/GMc coactivation pattern. The cue may have increased the healthy subjects’ anxiety levels, leading to a cocontraction strategy for postural control.25
Limitations One primary limitation of this study was that lesion size was not measured in the two stroke patient groups. It is possible that larger brain lesions led to poorer postural responses. However, given the heterogeneity in lesion areas (among the 14 patients with known lesion territories, 2 had lesions in only the anterior cerebral artery territory, 9 had lesions in only the MCA territory, 2 had lesions in both the anterior cerebral artery and MCA territories, and 1 had lesions in both the MCA and posterior cerebral artery territories) and the types of available brain images, it was difficult and less meaningful to quantify total brain lesion volumes. To rule out potential confounding variables on postural responses that were related to lesion severity, the participants were matched on motor deficits between groups. Therefore, it is unlikely that poorer reactive postural responses of the PPCLesion group were caused by differences in brain lesion severity. However, future studies may be needed to investigate whether brain lesion size in the PPC area affects the organization of reactive postural responses. Another limitation of the
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study relates to its small sample size. As mentioned previously, the small sample and the low statistical power may be one of the reasons for the nonsignificant within-group findings for the cue effect.
CONCLUSIONS
ward reinterpreting optic ataxia. Nat Neurosci 2000;3: 729Y36 9. Redfern MS, Muller ML, Jennings JR, et al: Attentional dynamics in postural control during perturbations in young and older adults. J Gerontol A Biol Sci Med Sci 2002;57:B298Y303 10. Perennou DA, Leblond C, Amblard B, et al: The polymodal sensory cortex is crucial for controlling lateral postural stability: Evidence from stroke patients. Brain Res Bull 2000;53:359Y65
The authors found that the PPCLesion patients had greater deficits in recruiting paretic muscles and were more likely to use compensatory muscle activation patterns for postural reactions than the PPCSpared patients. These findings suggest that PPC is part of the neural circuitry involved in reactive postural control in response to lateral perturbations. Accurate auditory cueing with long foreperiods did not seem to effectively improve paretic muscle recruitment and the organization of muscle activation patterns in PPCLesion patients in response to unexpected lateral pulls. More research is needed to explore the type and structure of cueing that could effectively improve muscle recruitment, muscle organization patterns, and speed of postural responses in these patients.
12. Rietdyk S, Patla AE, Winter DA, et al: Balance recovery from medio-lateral perturbations of the upper body during standing. J Biomech 1999;32:1149Y58
ACKNOWLEDGMENTS
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