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Anticipatory postural adjustments in individuals with multiple sclerosis
Neuroscience Letters 506 (2012) 256–260
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Anticipatory postural adjustments in individuals with multiple sclerosis Vennila Krishnan, Neeta Kanekar, Alexander S. Aruin ∗ Department of Physical Therapy, University of Illinois at Chicago, IL 60612, United States
a r t i c l e
i n f o
Article history: Received 10 June 2011 Received in revised form 9 November 2011 Accepted 10 November 2011 Keywords: Multiple sclerosis Balance Anticipatory postural control
a b s t r a c t Individuals with multiple sclerosis (MS) frequently exhibit difficulties in balance maintenance. It is known that anticipatory postural adjustments (APAs) play an important role in postural control. However, no information exists on how people living with MS utilize APAs for control of posture. A group of individuals with MS and a group of healthy control subjects performed rapid arm flexion and extension movements while standing on a force platform. Electromyographic (EMG) activity of six trunk and leg muscles and displacement of center of pressure (COP) were recorded and quantified within the time intervals typical of APAs. Individuals with MS demonstrated diminished ability to produce directional specific patterns of anticipatory EMGs as compared to control subjects. In addition, individuals with MS demonstrated smaller magnitudes of anticipatory muscle activation. This was associated with larger displacements of the COP during the balance restoration phase. These results suggest the importance of anticipatory postural control in maintenance of vertical posture in individuals with MS. The outcome of the study could be used while developing rehabilitation strategies focused on balance restoration in individuals with MS. © 2011 Elsevier Ireland Ltd. All rights reserved.
Introduction Impairment of balance control is a significant problem experienced by individuals with multiple sclerosis (MS). Even at an early stage of the disease, patients are affected by visual, vestibular and somatosensory impairments [8,11,12,27,28] with muscle weakness that leads to deficits in their balance [5] and postural control [6,20]. Thus, in these individuals, balance deficits and the associated heightened fear of falling result in significant declines in their mobility and activity levels, decreased social contact, and a lowered sense of empowerment [25]. It is known that the central nervous system (CNS) maintains balance using two main strategies: (i) Feedforward (anticipatory) postural adjustments (APAs) control the position of the center of mass (COM) and COP of the body by activating the trunk and leg muscles prior to a forthcoming body perturbation, thus minimizing the danger of losing equilibrium [reviewed in [16]]. (ii) Compensatory postural adjustments (CPAs) are initiated by the sensory feedback signals and serve as a mechanism of restoration of the position of the COM and COP after a perturbation has already occurred [1,19,21]. It was demonstrated recently that utilization of robust APAs in healthy young individuals is associated with significantly smaller compensatory muscle activation and smaller
∗ Corresponding author at: Department of Physical Therapy (MC 898), University of Illinois at Chicago, 1919 W. Taylor St., Chicago, IL 60612, United States. Tel.: +1 312 355 0904; fax: +1 312 996 4583. E-mail address: [email protected] (A.S. Aruin). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.11.018
COM–COP displacements. However, an absence of APAs results in large compensatory muscle activation and greater COM–COP displacements, thereby indicating reduced body stability [23,24]. This signifies the importance of APAs in control of posture and a need to investigate their role in balance restoration of individuals with neurological disorders. Past studies have shown that APAs are associated with direction specific patterns of activation or inhibition of postural muscles in healthy adults [3] and in typically developing children [10]. It was also shown that individuals with Down syndrome [2], cerebral palsy (CP) [9], and Parkinson disease [4,14] exhibit directionalspecific APA patterns. However, individuals with Down syndrome showed only anticipatory co-activation of trunk muscles [2] and individuals with CP showed smaller magnitudes of APA muscle activity [9]. To the best of our knowledge, no data exists on the ability of individuals with MS to generate anticipatory postural adjustments. In addition, the availability of directional specific APAs in MS has not been recorded so far. It is likely that impaired generation of APAs in individuals with MS may predispose them to increased risks of losing balance. Therefore, we hypothesized that individuals with MS will (1) demonstrate diminished ability to produce directionally specific APAs, (2) show smaller APA magnitudes, and (3) as a consequence, demonstrate larger center of pressure (COP) displacements while restoring balance, when compared to healthy controls. Eleven individuals (2 males and 9 females) with remittingrelapsed MS (age 52 ± 13 years, height 169.8 ± 10.3 cm, weight 68 ± 12 kg, EDSS score 2.3 ± 0.9) and eleven age and
V. Krishnan et al. / Neuroscience Letters 506 (2012) 256–260
gender matched healthy subjects (age 51 ± 14 years, height 167.8 ± 10.0 cm, weight 73 ± 12 kg) participated in the study. The inclusion criteria for the individuals with MS were independent standing and walking, and the presence of normal or corrected to normal vision. The patients were excluded if they had a history of other illnesses or if they were unable to perform the experimental tasks. The experimental procedure was approved by the Institutional Review Board of the University of Illinois at Chicago and the participants provided their informed consent. Individuals with MS were tested in the morning to minimize the effects of fatigue commonly reported later in the day. The subjects were required to perform rapid bilateral shoulder flexion and extension movements at 30 degrees while standing on a force platform (AMTI, OR-5, USA) with their feet shoulder width apart [3]. Disposable self-adhesive electrodes (Red Dot 3M) were used to record the surface electromyographic activity (EMG) of the following muscles: tibialis anterior (TA), soleus (SOL), rectus femoris (RF), biceps femoris (BF), rectus abdominis (RA), and erector spinae (ES). An accelerometer (Model 208CO3, PCB Piezotronics Inc., USA) oriented in the direction of the movement was taped to the participant’s right wrist. All the signals were sampled at 1000 Hz frequency with a 16-bit resolution. For all experimental trials, the participants were instructed to look straight ahead at a marker placed on the wall and to perform the required movement at a ‘as fast as possible’ speed, in a self-paced manner after the go signal. The 30 degrees of flexion and extension final positions were marked by a pointer. 2 practice trials were given prior to each task. For each flexion and extension task, the participants performed 5 trials with a 5 second interval between each trial. In addition the subjects were given a rest break whenever they asked for. Both the tasks were randomized across the subjects. Additionally, after the completion of the experimental tasks, balance of the subjects in both groups was assessed with the Balance Master® (NeuroCom, USA). The limits of stability (LOS) test was used to quantify the subjects’ ability to voluntarily move their center of gravity (COG) to their stability limits in eight different directions without losing balance. The test measures movement distance, movement directional control, movement velocity, and movement reaction time for each direction and also gives a composite score (average score over the 8 directions) and is considered as a valid clinical test of balance [15]. All signals were processed offline using customized Matlab 7.6 software (MathWorks, Natick, MA). EMG signals were rectified and filtered with a 50 Hz low-pass, 2nd order, zero-lag Butterworth filter, while the force platform signals were filtered with a 20 Hz low-pass, 2nd order, zero-lag Butterworth filter. The ‘time-zero’ (T0 = 0) or the initiation of arm movement was calculated from the accelerometer signal as a point in time at which the signal exceeded 5% of the maximum acceleration. This value was confirmed by visual inspection by an experienced researcher. Data in the range from −600 ms (before T0 ) to +500 ms (after T0 ) were selected for further analysis. Aligned trials within each task were averaged for each subject. The averaged EMG signals were integrated within 150 ms time windows [17]. The anticipatory adjustments, APAs were quantified from −100 ms to +50 ms with respect to T0 [23,26]. This was corrected by the averaged 150 ms baseline activity time window of EMG integral from −600 ms to −450 ms in relation to T0 and normalized by peak activity across both the flexion and extension tasks. The above was done for each muscle for each subject. Due to the normalization, all the integral values were within the range from +1 to −1 [13]. Positive values indicate an activation of the muscle, while negative values indicate a decrease in the background activity (inhibition). Time-varying COP displacement in the anterior–posterior direction was calculated using the force platform signals [29]. The COP
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data was averaged for each participant and for each task. We calculated the magnitude of COP displacement at T0 (A-COP), which is anticipatory in nature and the peak displacement of the COP (CCOP) that is compensatory in nature [13,17]. Please note that the greater the value of peak displacement during the compensatory postural control, the larger the postural instability. All the participants were able to perform the two experimental tasks. There were no significant differences in the magnitudes of arm acceleration in both MS patients and healthy controls suggesting that all the subjects generated perturbations of similar magnitude. EMG patterns for RA and ES muscles obtained from a representative individual with MS and a control subject are shown in Fig. 1. The subjects in both groups showed directionally specific changes in the anticipatory activation of muscles. Thus, during arm flexion (Fig. 1A), burst of activity was seen in ES and no activation in RA. When the direction of the movement was changed to extension (Fig. 1B), RA showed anticipatory activation while there was no activation of ES prior to the onset of the movement. Similar but less pronounced patterns were observed in RF-BF and TA-SOL muscles. Integrals of EMG activity for APAs of all the muscles (TA, RF, RA, SOL, BF, ES) are shown in Fig. 2. The directional specific pattern could be observed in RA, ES and BF muscles in both the MS and control groups of subjects. Note, however, that no directional specific patterns were observed in RF, SOL, and TA in individuals with MS when compared to healthy controls. In general, individuals with MS showed smaller magnitudes of APAs as compared to healthy controls. This could be seen as smaller anticipatory burst of ES activity in flexion and RA in extension movements in individuals with MS (Fig. 1). Fig. 2 shows such smaller integrals of EMG in MS in all the muscles except RF (shoulder flexion) and in RF, RA, BF and ES muscles (shoulder extension). Mixed design 2-way MANOVA (group × direction) was applied to all the six muscles, where group (MS and HC) and direction (flexion and extension) had 2 levels. The MANOVA results revealed a significant effect of group × direction interaction [Wilks’ Lambda = .37, F(6,15) = 4.3, p < .05] and a main effect of direction [Wilks’ Lambda = .03, F(6,15) = 80.5, p < .001], with no significant effect of group. In the subsequent univariate analyses of the interaction, SOL (F(1,20) = 6.7, p < .05) and RF (F(1,20) = 11.6, p < .01) showed a significant contrast pattern between MS and controls. For example, control subjects used activation and inhibition of SOL in flexion and extension movement respectively, while the individuals with MS used activation of SOL in both the tasks. The individuals with MS and the control subjects demonstrated similar directional specific changes in the center of pressure. In addition, comparable anticipatory COP displacements (A-COP) were seen in both the groups in each of the movements (Fig. 3). However, the individuals with MS showed larger COP peak displacement (C-COP) in both the tasks as compared to the healthy controls. A 3-way mixed design ANOVA (group × direction × displacement), with group (2 levels: MS and HC), direction (2 levels: flexion and extension) and displacement (A-COP and C-COP) revealed a significant main effect of group (F(1,20) = 4.4, p < .05), main effect of direction (F(1,20) = 156.1, p < .001), and significant interaction direction × displacement (F(1,20) = 68.3, p < .001). All subjects in the MS group except one could perform the LOS test. To compare the two groups, a two-tailed independent t-test was applied for the composite score of each of the four outcome measures of the LOS. As compared to healthy controls, individuals with MS showed significantly reduced endpoint excursion (the mean and standard deviation for healthy controls were 75.18 ± 12.61% of maximum LOS and for individuals with MS were 57.8 ± 16.43% of maximum LOS, p = .01), significantly
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Fig. 1. EMG traces for a representative subjects (average of five trials) obtained from the rectus abdominis (RA) and erector spinae (ES) muscles during the performance of flexion and extension movements. The vertical line (T0 ) represents the onset of the perturbation and the point of alignment. Time scales are in milliseconds and EMG scales are in arbitrary units. EMG traces for ES are shown inverted for ease of comparison and their scales are on the right. MS- individual with MS, HC- healthy control.
reduced maximum excursion (for healthy controls: 89.63 ± 8.59% of maximum LOS and for individuals with MS: 76 ± 15.69% of maximum LOS, p = .02), and significant impairments of movement directional control (for healthy controls: 77.45 ± 5.37% and for
individuals with MS: 68.2 ± 9.7%, p = .01). Individuals with MS also demonstrated somewhat reduced movement reaction times and movement velocity as compared to healthy controls; however these values did not reach statistical significance. Thus, the overall
Fig. 2. Mean values and standard error bars of integrals for APAs (−100 to +50 ms in relation to T0 ) are shown for all the muscles in the flexion and extension movements.
V. Krishnan et al. / Neuroscience Letters 506 (2012) 256–260
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These results, the first to document the organization of APAs in individuals with MS, should be further studied to delineate the effect of different forms of MS on generation of APAs and to provide a background for development of rehabilitation strategies focused on balance restoration in individuals with MS. Acknowledgements
Fig. 3. Mean values and standard errors of the anticipatory displacement of the center of pressure (A-COP) at the time of perturbation (T0 ) and the peak of center of pressure displacement (C-COP) are shown for the flexion and extension movements. COPAP magnitudes are in mm and negative values correspond to displacements of the COPAP backwards. COP displacement for arm extension is inverted for better representation. *Significant main effect between MS and control subjects.
LOS test results suggest that balance control in individuals with MS was affected as compared to healthy control subjects. The results of the current study supported all three hypotheses. Subjects in both the groups were able to perform the experimental tasks (shoulder flexion and extension) and utilize APAs to control body posture. In general, individuals with MS demonstrated lesser directional-specific activation of muscles and smaller magnitudes of anticipatory muscle activation as compared to the control subjects. As a consequence, a larger displacement of the COP was produced during the balance restoration phase (after T0 ). It is known that large COP displacements are associated with decreased body stability and are reported to be observed in the elderly [18] and in individuals with neurological disorders [22]. As such, it is reasonable to believe that the increased displacement of COP seen in individuals with MS could exemplify their increased instability while restoring balance after the body perturbation. The increased COP displacement seen in individuals with MS could be the result of one of three factors. First, is the reduced ability of individuals with MS to utilize APAs for balance control; indeed individuals with MS in the current study utilized lesser APAs (integrals) as compared to the control subjects that resulted in larger displacements of the COP in both the tasks. Second, is the diminished ability to maintain body position commonly observed in individuals with MS: it was reported that individuals with MS experience more difficulty while standing with a reduced base of support [8]. Additionally, the outcome of our LOS test suggests that the ability of individuals with MS to voluntarily move their center of gravity to their stability limits is diminished, indicating weak balance control. Finally, the ability to use directional-specific patterns of activation of muscles was affected in individuals with MS as confirmed by the observed patterns of activation of SOL and RF. Thus, the impairments of balance control in MS described in the present study taken together with the diminished performance on the clinical tests of balance [7,27] could explain why individuals with MS showed lesser ability to generate both anticipatory and directional-specific patterns of activation of muscles. We would particularly like to point out that the individuals with MS tested in the current study were only mildly involved (averaged EDSS score 2.3 ± 0.9) with minimal motor impairment, and were able to live a professionally active life. Nevertheless, they showed an impaired balance control when compared to the healthy subjects.
We thank the individuals with MS and the control subjects for their exceptional cooperation. We are grateful to the Greater Illinois Chapter of the National Multiple Sclerosis Society for the assistance in the recruitment of the study participants. This work was supported in part by NIDRR grant H133P060003. We thank Sambit Mohapatra for the help in data collection. References [1] A.V. Alexandrov, A.A. Frolov, F.B. Horak, P. Carlson-Kuhta, S. Park, Feedback equilibrium control during human standing, Biological Cybernetics 93 (2005) 309–322. [2] A. Aruin, G. Almeida, A coactivation strategy in anticipatory postural adjustment in persons with Down syndrome, Motor Control 2 (1997) 178–191. [3] A.S. Aruin, M.L. Latash, Directional specificity of postural muscles in feed-forward postural reactions during fast voluntary arm movements, Experimental Brain Research 103 (1995) 323–332. [4] A.S. Aruin, I. Neyman, J.J. Nicholas, M.L. Latash, Are there deficits in anticipatory postural adjustments in Parkinson’s disease? Neuroreport 7 (1996) 1794–1796. [5] M.H. Cameron, F.B. Horak, R.R. Herndon, D. Bourdette, Imbalance in multiple sclerosis: a result of slowed spinal somatosensory conduction, Somatosensory & Motor Research 25 (2008) 113–122. [6] M. Finlayson, L. Guglielmello, K. Liefer, Describing and predicting the possession of assistive devices among persons with multiple sclerosis, The American Journal of Occupational Therapy 55 (2001) 545–551. [7] C. Fjeldstad, G. Pardo, D. Bemben, M. Bemben, Decreased postural balance in multiple sclerosis patients with low disability, International Journal of Rehabilitation Research 34 (2011) 53–58. [8] D. Frzovic, M.E. Morris, L. Vowels, Clinical tests of standing balance: performance of persons with multiple sclerosis, Archives of Physical Medicine and Rehabilitation 81 (2000) 215–221. [9] G. Girolami, T. Shiratori, A. Aruin, Anticipatory postural adjustments in children with hemiplegia and diplegia, Journal of Electromyography and Kinesiology 21 (2011) 988–997. [10] G.L. Girolami, T. Shiratori, A.S. Aruin, Anticipatory postural adjustments in children with typical motor development, Experimental Brain Research 205 (2010) 153–165. [11] V. Grigorova, I. Ivanov, K. Stambolieva, Effect of sensory inputs alteration and central sensory disinteraction on postural sway and optokinetic reflex maintaining simultaneously body balance, Acta Physiologica et Pharmacologica Bulgarica 26 (2001) 177–180. [12] A.M. Kraft, H.C. Wessman, Pathology and etiology in multiple sclerosis: a review, Physical Therapy 54 (1974) 716–720. [13] V. Krishnan, A.S. Aruin, Postural control in response to a perturbation: role of vision and additional support, Experimental Brain Research 212 (2011) 385–397. [14] M.L. Latash, A.S. Aruin, I. Neyman, J.J. Nicholas, Anticipatory postural adjustments during self inflicted and predictable perturbations in Parkinson’s disease, Journal of Neurology, Neurosurgery and Psychiatry 58 (1995) 326–334. [15] R.A. Liston, B.J. Brouwer, Reliability and validity of measures obtained from stroke patients using the Balance Master, Archives of Physical Medicine and Rehabilitation 77 (1996) 425–430. [16] J. Massion, Movement, posture and equilibrium: interaction and coordination, Progress in Neurobiology 38 (1992) 35–56. [17] S. Mohapatra, V. Krishnan, A.S. Aruin, The effect of decreased visual acuity on control of posture, Journal of Clinical Neurophysiology (2011), doi:10.1016/j.clinph.2011.06.008 (Epub ahead of print). [18] H. Nakamura, T. Tsuchida, Y. Mano, The assessment of posture control in the elderly using the displacement of the center of pressure after forward platform translation, Journal of Electromyography and Kinesiology 11 (2001) 395–403. [19] L.M. Nashner, P.J. Cordo, Relation of automatic postural responses and reactiontime voluntary movements of human leg muscles, Experimental Brain Research 43 (1981) 395–405. [20] S.R. Nelson, R.P. Di Fabio, J.H. Anderson, Vestibular and sensory interaction deficits assessed by dynamic platform posturography in patients with multiple sclerosis, The Annals of Otology, Rhinology and Laryngology 104 (1995) 62–68.
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[21] S. Park, F.B. Horak, A.D. Kuo, Postural feedback responses scale with biomechanical constraints in human standing, Experimental Brain Research 154 (2004) 417–427. [22] S.H. Peurala, P. Kononen, K. Pitkanen, J. Sivenius, I.M. Tarkka, Postural instability in patients with chronic stroke, Restorative Neurology and Neuroscience 25 (2007) 101–108. [23] M.J. Santos, N. Kanekar, A.S. Aruin, The role of anticipatory postural adjustments in compensatory control of posture: 1. Electromyographic analysis, Journal of Electromyography and Kinesiology 20 (2010) 388–397. [24] M.J. Santos, N. Kanekar, A.S. Aruin, The role of anticipatory postural adjustments in compensatory control of posture: 2. Biomechanical analysis, Journal of Electromyography and Kinesiology 20 (2010) 398–405.
[25] A.C. Scheffer, M.J. Schuurmans, N. van Dijk, T. van der Hooft, S.E. de Rooij, Fear of falling: measurement strategy, prevalence, risk factors and consequences among older persons, Age and Ageing 37 (2008) 19–24. [26] H. Slijper, M.L. Latash, The effects of instability and additional hand support on anticipatory postural adjustments in leg, trunk, and arm muscles during standing, Experimental Brain Research 135 (2000) 81–93. [27] F. Soyuer, M. Mirza, U. Erkorkmaz, Balance performance in three forms of multiple sclerosis, Neurological Research 28 (2006) 555–562. [28] N.P. Williams, P.S. Roland, W. Yellin, Vestibular evaluation in patients with early multiple sclerosis, The American Journal of Otology 18 (1997) 93–100. [29] D.A. Winter, F. Prince, J.S. Frank, C. Powell, K.F. Zabjek, Unified theory regarding A/P and M/L balance in quiet stance, Journal of Neurophysiology 75 (1996) 2334–2343.
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Anticipatory postural adjustments in individuals with multiple sclerosis Vennila Krishnan, Neeta Kanekar, Alexander S. Aruin ∗ Department of Physical Therapy, University of Illinois at Chicago, IL 60612, United States
a r t i c l e
i n f o
Article history: Received 10 June 2011 Received in revised form 9 November 2011 Accepted 10 November 2011 Keywords: Multiple sclerosis Balance Anticipatory postural control
a b s t r a c t Individuals with multiple sclerosis (MS) frequently exhibit difficulties in balance maintenance. It is known that anticipatory postural adjustments (APAs) play an important role in postural control. However, no information exists on how people living with MS utilize APAs for control of posture. A group of individuals with MS and a group of healthy control subjects performed rapid arm flexion and extension movements while standing on a force platform. Electromyographic (EMG) activity of six trunk and leg muscles and displacement of center of pressure (COP) were recorded and quantified within the time intervals typical of APAs. Individuals with MS demonstrated diminished ability to produce directional specific patterns of anticipatory EMGs as compared to control subjects. In addition, individuals with MS demonstrated smaller magnitudes of anticipatory muscle activation. This was associated with larger displacements of the COP during the balance restoration phase. These results suggest the importance of anticipatory postural control in maintenance of vertical posture in individuals with MS. The outcome of the study could be used while developing rehabilitation strategies focused on balance restoration in individuals with MS. © 2011 Elsevier Ireland Ltd. All rights reserved.
Introduction Impairment of balance control is a significant problem experienced by individuals with multiple sclerosis (MS). Even at an early stage of the disease, patients are affected by visual, vestibular and somatosensory impairments [8,11,12,27,28] with muscle weakness that leads to deficits in their balance [5] and postural control [6,20]. Thus, in these individuals, balance deficits and the associated heightened fear of falling result in significant declines in their mobility and activity levels, decreased social contact, and a lowered sense of empowerment [25]. It is known that the central nervous system (CNS) maintains balance using two main strategies: (i) Feedforward (anticipatory) postural adjustments (APAs) control the position of the center of mass (COM) and COP of the body by activating the trunk and leg muscles prior to a forthcoming body perturbation, thus minimizing the danger of losing equilibrium [reviewed in [16]]. (ii) Compensatory postural adjustments (CPAs) are initiated by the sensory feedback signals and serve as a mechanism of restoration of the position of the COM and COP after a perturbation has already occurred [1,19,21]. It was demonstrated recently that utilization of robust APAs in healthy young individuals is associated with significantly smaller compensatory muscle activation and smaller
∗ Corresponding author at: Department of Physical Therapy (MC 898), University of Illinois at Chicago, 1919 W. Taylor St., Chicago, IL 60612, United States. Tel.: +1 312 355 0904; fax: +1 312 996 4583. E-mail address: [email protected] (A.S. Aruin). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.11.018
COM–COP displacements. However, an absence of APAs results in large compensatory muscle activation and greater COM–COP displacements, thereby indicating reduced body stability [23,24]. This signifies the importance of APAs in control of posture and a need to investigate their role in balance restoration of individuals with neurological disorders. Past studies have shown that APAs are associated with direction specific patterns of activation or inhibition of postural muscles in healthy adults [3] and in typically developing children [10]. It was also shown that individuals with Down syndrome [2], cerebral palsy (CP) [9], and Parkinson disease [4,14] exhibit directionalspecific APA patterns. However, individuals with Down syndrome showed only anticipatory co-activation of trunk muscles [2] and individuals with CP showed smaller magnitudes of APA muscle activity [9]. To the best of our knowledge, no data exists on the ability of individuals with MS to generate anticipatory postural adjustments. In addition, the availability of directional specific APAs in MS has not been recorded so far. It is likely that impaired generation of APAs in individuals with MS may predispose them to increased risks of losing balance. Therefore, we hypothesized that individuals with MS will (1) demonstrate diminished ability to produce directionally specific APAs, (2) show smaller APA magnitudes, and (3) as a consequence, demonstrate larger center of pressure (COP) displacements while restoring balance, when compared to healthy controls. Eleven individuals (2 males and 9 females) with remittingrelapsed MS (age 52 ± 13 years, height 169.8 ± 10.3 cm, weight 68 ± 12 kg, EDSS score 2.3 ± 0.9) and eleven age and
V. Krishnan et al. / Neuroscience Letters 506 (2012) 256–260
gender matched healthy subjects (age 51 ± 14 years, height 167.8 ± 10.0 cm, weight 73 ± 12 kg) participated in the study. The inclusion criteria for the individuals with MS were independent standing and walking, and the presence of normal or corrected to normal vision. The patients were excluded if they had a history of other illnesses or if they were unable to perform the experimental tasks. The experimental procedure was approved by the Institutional Review Board of the University of Illinois at Chicago and the participants provided their informed consent. Individuals with MS were tested in the morning to minimize the effects of fatigue commonly reported later in the day. The subjects were required to perform rapid bilateral shoulder flexion and extension movements at 30 degrees while standing on a force platform (AMTI, OR-5, USA) with their feet shoulder width apart [3]. Disposable self-adhesive electrodes (Red Dot 3M) were used to record the surface electromyographic activity (EMG) of the following muscles: tibialis anterior (TA), soleus (SOL), rectus femoris (RF), biceps femoris (BF), rectus abdominis (RA), and erector spinae (ES). An accelerometer (Model 208CO3, PCB Piezotronics Inc., USA) oriented in the direction of the movement was taped to the participant’s right wrist. All the signals were sampled at 1000 Hz frequency with a 16-bit resolution. For all experimental trials, the participants were instructed to look straight ahead at a marker placed on the wall and to perform the required movement at a ‘as fast as possible’ speed, in a self-paced manner after the go signal. The 30 degrees of flexion and extension final positions were marked by a pointer. 2 practice trials were given prior to each task. For each flexion and extension task, the participants performed 5 trials with a 5 second interval between each trial. In addition the subjects were given a rest break whenever they asked for. Both the tasks were randomized across the subjects. Additionally, after the completion of the experimental tasks, balance of the subjects in both groups was assessed with the Balance Master® (NeuroCom, USA). The limits of stability (LOS) test was used to quantify the subjects’ ability to voluntarily move their center of gravity (COG) to their stability limits in eight different directions without losing balance. The test measures movement distance, movement directional control, movement velocity, and movement reaction time for each direction and also gives a composite score (average score over the 8 directions) and is considered as a valid clinical test of balance [15]. All signals were processed offline using customized Matlab 7.6 software (MathWorks, Natick, MA). EMG signals were rectified and filtered with a 50 Hz low-pass, 2nd order, zero-lag Butterworth filter, while the force platform signals were filtered with a 20 Hz low-pass, 2nd order, zero-lag Butterworth filter. The ‘time-zero’ (T0 = 0) or the initiation of arm movement was calculated from the accelerometer signal as a point in time at which the signal exceeded 5% of the maximum acceleration. This value was confirmed by visual inspection by an experienced researcher. Data in the range from −600 ms (before T0 ) to +500 ms (after T0 ) were selected for further analysis. Aligned trials within each task were averaged for each subject. The averaged EMG signals were integrated within 150 ms time windows [17]. The anticipatory adjustments, APAs were quantified from −100 ms to +50 ms with respect to T0 [23,26]. This was corrected by the averaged 150 ms baseline activity time window of EMG integral from −600 ms to −450 ms in relation to T0 and normalized by peak activity across both the flexion and extension tasks. The above was done for each muscle for each subject. Due to the normalization, all the integral values were within the range from +1 to −1 [13]. Positive values indicate an activation of the muscle, while negative values indicate a decrease in the background activity (inhibition). Time-varying COP displacement in the anterior–posterior direction was calculated using the force platform signals [29]. The COP
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data was averaged for each participant and for each task. We calculated the magnitude of COP displacement at T0 (A-COP), which is anticipatory in nature and the peak displacement of the COP (CCOP) that is compensatory in nature [13,17]. Please note that the greater the value of peak displacement during the compensatory postural control, the larger the postural instability. All the participants were able to perform the two experimental tasks. There were no significant differences in the magnitudes of arm acceleration in both MS patients and healthy controls suggesting that all the subjects generated perturbations of similar magnitude. EMG patterns for RA and ES muscles obtained from a representative individual with MS and a control subject are shown in Fig. 1. The subjects in both groups showed directionally specific changes in the anticipatory activation of muscles. Thus, during arm flexion (Fig. 1A), burst of activity was seen in ES and no activation in RA. When the direction of the movement was changed to extension (Fig. 1B), RA showed anticipatory activation while there was no activation of ES prior to the onset of the movement. Similar but less pronounced patterns were observed in RF-BF and TA-SOL muscles. Integrals of EMG activity for APAs of all the muscles (TA, RF, RA, SOL, BF, ES) are shown in Fig. 2. The directional specific pattern could be observed in RA, ES and BF muscles in both the MS and control groups of subjects. Note, however, that no directional specific patterns were observed in RF, SOL, and TA in individuals with MS when compared to healthy controls. In general, individuals with MS showed smaller magnitudes of APAs as compared to healthy controls. This could be seen as smaller anticipatory burst of ES activity in flexion and RA in extension movements in individuals with MS (Fig. 1). Fig. 2 shows such smaller integrals of EMG in MS in all the muscles except RF (shoulder flexion) and in RF, RA, BF and ES muscles (shoulder extension). Mixed design 2-way MANOVA (group × direction) was applied to all the six muscles, where group (MS and HC) and direction (flexion and extension) had 2 levels. The MANOVA results revealed a significant effect of group × direction interaction [Wilks’ Lambda = .37, F(6,15) = 4.3, p < .05] and a main effect of direction [Wilks’ Lambda = .03, F(6,15) = 80.5, p < .001], with no significant effect of group. In the subsequent univariate analyses of the interaction, SOL (F(1,20) = 6.7, p < .05) and RF (F(1,20) = 11.6, p < .01) showed a significant contrast pattern between MS and controls. For example, control subjects used activation and inhibition of SOL in flexion and extension movement respectively, while the individuals with MS used activation of SOL in both the tasks. The individuals with MS and the control subjects demonstrated similar directional specific changes in the center of pressure. In addition, comparable anticipatory COP displacements (A-COP) were seen in both the groups in each of the movements (Fig. 3). However, the individuals with MS showed larger COP peak displacement (C-COP) in both the tasks as compared to the healthy controls. A 3-way mixed design ANOVA (group × direction × displacement), with group (2 levels: MS and HC), direction (2 levels: flexion and extension) and displacement (A-COP and C-COP) revealed a significant main effect of group (F(1,20) = 4.4, p < .05), main effect of direction (F(1,20) = 156.1, p < .001), and significant interaction direction × displacement (F(1,20) = 68.3, p < .001). All subjects in the MS group except one could perform the LOS test. To compare the two groups, a two-tailed independent t-test was applied for the composite score of each of the four outcome measures of the LOS. As compared to healthy controls, individuals with MS showed significantly reduced endpoint excursion (the mean and standard deviation for healthy controls were 75.18 ± 12.61% of maximum LOS and for individuals with MS were 57.8 ± 16.43% of maximum LOS, p = .01), significantly
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Fig. 1. EMG traces for a representative subjects (average of five trials) obtained from the rectus abdominis (RA) and erector spinae (ES) muscles during the performance of flexion and extension movements. The vertical line (T0 ) represents the onset of the perturbation and the point of alignment. Time scales are in milliseconds and EMG scales are in arbitrary units. EMG traces for ES are shown inverted for ease of comparison and their scales are on the right. MS- individual with MS, HC- healthy control.
reduced maximum excursion (for healthy controls: 89.63 ± 8.59% of maximum LOS and for individuals with MS: 76 ± 15.69% of maximum LOS, p = .02), and significant impairments of movement directional control (for healthy controls: 77.45 ± 5.37% and for
individuals with MS: 68.2 ± 9.7%, p = .01). Individuals with MS also demonstrated somewhat reduced movement reaction times and movement velocity as compared to healthy controls; however these values did not reach statistical significance. Thus, the overall
Fig. 2. Mean values and standard error bars of integrals for APAs (−100 to +50 ms in relation to T0 ) are shown for all the muscles in the flexion and extension movements.
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These results, the first to document the organization of APAs in individuals with MS, should be further studied to delineate the effect of different forms of MS on generation of APAs and to provide a background for development of rehabilitation strategies focused on balance restoration in individuals with MS. Acknowledgements
Fig. 3. Mean values and standard errors of the anticipatory displacement of the center of pressure (A-COP) at the time of perturbation (T0 ) and the peak of center of pressure displacement (C-COP) are shown for the flexion and extension movements. COPAP magnitudes are in mm and negative values correspond to displacements of the COPAP backwards. COP displacement for arm extension is inverted for better representation. *Significant main effect between MS and control subjects.
LOS test results suggest that balance control in individuals with MS was affected as compared to healthy control subjects. The results of the current study supported all three hypotheses. Subjects in both the groups were able to perform the experimental tasks (shoulder flexion and extension) and utilize APAs to control body posture. In general, individuals with MS demonstrated lesser directional-specific activation of muscles and smaller magnitudes of anticipatory muscle activation as compared to the control subjects. As a consequence, a larger displacement of the COP was produced during the balance restoration phase (after T0 ). It is known that large COP displacements are associated with decreased body stability and are reported to be observed in the elderly [18] and in individuals with neurological disorders [22]. As such, it is reasonable to believe that the increased displacement of COP seen in individuals with MS could exemplify their increased instability while restoring balance after the body perturbation. The increased COP displacement seen in individuals with MS could be the result of one of three factors. First, is the reduced ability of individuals with MS to utilize APAs for balance control; indeed individuals with MS in the current study utilized lesser APAs (integrals) as compared to the control subjects that resulted in larger displacements of the COP in both the tasks. Second, is the diminished ability to maintain body position commonly observed in individuals with MS: it was reported that individuals with MS experience more difficulty while standing with a reduced base of support [8]. Additionally, the outcome of our LOS test suggests that the ability of individuals with MS to voluntarily move their center of gravity to their stability limits is diminished, indicating weak balance control. Finally, the ability to use directional-specific patterns of activation of muscles was affected in individuals with MS as confirmed by the observed patterns of activation of SOL and RF. Thus, the impairments of balance control in MS described in the present study taken together with the diminished performance on the clinical tests of balance [7,27] could explain why individuals with MS showed lesser ability to generate both anticipatory and directional-specific patterns of activation of muscles. We would particularly like to point out that the individuals with MS tested in the current study were only mildly involved (averaged EDSS score 2.3 ± 0.9) with minimal motor impairment, and were able to live a professionally active life. Nevertheless, they showed an impaired balance control when compared to the healthy subjects.
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