Neuroscience Letters 561 (2014) 112–117
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Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Application of intermittent galvanic vestibular stimulation reveals age-related constraints in the multisensory reweighting of posture Diderik J.A. Eikema a , Vassilia Hatzitaki a,∗ , Dimitrios Tzovaras b , Charalambos Papaxanthis c,d a
Motor Control and Learning Laboratory, Department of Physical Education and Sport Science, Aristotle University of Thessaloniki, Greece Informatics and Telematics Institute, Centre for Research and Technology Hellas, 570 01 Thessaloniki, Greece c Université de Bourgogne, Unité de Formation et de Recherche en Sciences et Techniques des Activités Physiques et Sportives, F-21078 Dijon, France d Institut National de la Santé et de la Recherche Médicale (INSERM), U1093, Cognition, Action, and Plasticité Sensorimotrice, BP 27877, F-21078 Dijon, France b
h i g h l i g h t s • • • • •
Intermittent Galvanic Vestibular Stimulation (GVS) was applied during stance. Sensory reweighting was evoked by perturbing proprioception and vision. Intermittent GVS reduced excessive sway evoked by the multisensory perturbation. Intermittent GVS had no stabilizing effect in elderly’s sway. Intermittent GVS increases sensory reliance on the vestibular system.
a r t i c l e
i n f o
Article history: Received 22 July 2013 Received in revised form 28 November 2013 Accepted 21 December 2013 Keywords: Posture Aging Vision Proprioception Galvanic vestibular stimulation
a b s t r a c t In this study we examined the effects of intermittent short-duration Galvanic Vestibular Stimulation (GVS) during a multisensory perturbation of posture in young and elderly adults. Twelve young (24.91 ± 6.44 years) and eleven elderly (74.8 ± 6.42 years) participants stood upright under two task conditions: (a) quiet standing and (b) standing while receiving pseudo-randomly presented bipolar 2 s GVS pulses. In both conditions, sensory reweighting was evoked by visual surround oscillations (20 cm, 0.3 Hz) and Achilles tendon vibration (3 mm, 80 Hz), concurrently delivered during the middle 60 s of standing. Intermittent GVS decreased the excessive postural sway induced by the concurrent visual and proprioceptive perturbation in young but not in elderly participants. It is suggested that GVS increases sensory reliance on the vestibular system while elderly adults are less able to exploit this stimulation in order to reduce the destabilizing effect of the multisensory perturbation on their posture. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The vestibular system provides information on linear and angular head acceleration. This is combined with information from complementary sources such as vision and proprioception in order to establish an internal representation of the body’s position within the gravitational space [1]. The contribution of each sensory modality to this multisensory representation depends on the weight the Central Nervous System (CNS) assigns to each modality according to its perceived accuracy [2]. Vestibular cues are important in the
∗ Corresponding author at: Motor Control and Learning Laboratory, Department of Physical Education and Sport Science, Aristotle University of Thessaloniki, Thessaloniki 540 06, Greece. Tel.: +30 2310 992193; fax: +30 2310 992193. E-mail address: [email protected] (V. Hatzitaki). 0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2013.12.048
sensorial reweighting process because they reduce the effects of inaccurate vision and proprioception on the perception of postural vertical [3]. Advancing age impairs vestibular function due to loss of vestibular afferents [4]. As a result, elderly individuals display increased error and variability in the perception of the postural vertical, particularly in conditions of inaccurate vision and proprioception, which could result in an unstable posture and increased fall risk [5]. Short duration transmastoidal bipolar Galvanic Vestibular Stimulation (GVS) modulates the firing rate of vestibular afferents signaling head rotation through secondary neurons in the vestibular nuclei [6]. This results in the tonic reflex activation of the anti-gravity muscles eliciting a prolonged postural response in the medio-lateral direction when facing forward [7]. Existing evidence about the role of GVS in controlling posture under sensory perturbation conditions is conflicting. On one hand, postural responses to
D.J.A. Eikema et al. / Neuroscience Letters 561 (2014) 112–117
GVS increase in the absence of somatosensory or visual information [8,9] pointing to the increasing sensitivity of the vestibular system under conditions of sensory conflict. In this context, when GVS was applied synchronously or 500 ms prior to a backward platform translation the shift in the final equilibrium position was larger than the sum of the shifts for the galvanic stimulus and the platform translation alone [10]. On the contrary, stabilizing effects of GVS under sensory perturbations have also been reported. Application of bilateral, bipolar short duration GVS significantly reduced the antero-posterior sway velocity when standing on foam [11] and sway amplitude and latency in response to a simultaneous platform translation in the medio-lateral direction [12]. In this study, we were interested in the modulating after-effects of intermittent short-duration (2 s) GVS on body posture when vision and proprioception were concurrently disrupted in young and elderly adults. We perturbed vision by exposing participants to periodic Antero-Posterior (AP) visual field oscillations (20 cm, 0.3 Hz) and proprioception by bilateral application of continuous Achilles tendon vibration (3 mm, 80 Hz). The two perturbations were delivered simultaneously thereby increasing the system’s reliance on vestibular cues [13]. We hypothesized that intermittent GVS could reduce the destabilizing effects of the concurrent visual and proprioceptive perturbation on standing balance. We expected this effect to be less evident in elderly adults due to age associated vestibular degeneration. 2. Materials and methods 2.1. Participants Twelve young (5 males, 7 females; age 24.91 ± 6.44, mass 70.91 ± 13.93 kg) and eleven elderly (6 males, 5 females; age 74.8 ± 6.42, mass 78.44 ± 13.16 kg) adults participated in the study. Participants were free of neurological and musculoskeletal impairments and had normal or corrected to normal vision. Elderly participants were screened for cognitive dysfunction using the Mini Mental State Examination (MMSE). The MMSE cut-off score was set at 22. Participants were informed of the procedures and provided written consent. All experiments were performed with the approval of the local ethics committee on human research in accordance with the Declaration of Helsinki. 2.2. Apparatus and stimuli Visual stimuli were provided by a stereoscopic projection screen (Barco Baron 908, Barco N.V., Kuurne, Belgium, width 128 cm, height 102 cm), viewed through active shutter goggles (Chrystal Eyes 3, Stereographics, 105 Hz). The screen was located 200 cm in front of the participant, allowing for a horizontal viewing angle of 38◦ . The visual stimulus consisted of a 3D horizontal and vertical alternating light and dark gray bar pattern (Fig. 1a). This was a stimulus of contractive-expansive nature mimicking actual optic flow. During the perturbation phase the virtual surround oscillated (frequency: 0.3 Hz, amplitude: 20 cm), following a sinusoidal pattern along the AP axis. The surroundings were darkened to ensure the contribution of peripheral vision was limited. The proprioceptive perturbation of bilateral Achilles Tendon vibration (80 Hz, 3 mm amplitude) was delivered by a pair of cylindrical mechanical vibrators (VB115, Technoconcept, Mane, France). GVS waveforms were generated by a data-acquisition board (NI PCI-6221, National Instruments, Austin, USA) and delivered by a Model 2200 constant current isolator (A-M Systems, Carlsborg, USA). The current followed a sinusoidal waveform of a single cycle (cycle duration: 2 s, frequency: 0.5 Hz, amplitude: ±0.5 mA to 3 mA, Fig. 1b). The stimulus was bilaterally applied to the
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mastoid processes through conduction gel-coated 2 cm × 3 cm Stimex electrodes (Pierenkemper, Wetzlar, Germany). Postural sway was assessed with a force platform (Balance Plate 6501, Bertec Corporation, Columbus, USA, 100 Hz) recording Center of Pressure (CoP) displacement in the AP and Medio-Lateral (ML) directions and a six DoF electromagnetic tracker (Nest of Birds, Ascension Inc, Burlington, USA, 100 Hz) attached to the C7 vertebra that recorded upper trunk pitch rotation. 2.3. Task and procedure Prior to the experiment participants were familiarized with the vestibular and proprioceptive stimuli. GVS was applied using a bipolar binaural configuration with the anodal electrode attached on the left and the cathodal electrode on the right mastoid. Soft pads with an additional layer of electrode gel were placed over the electrodes and were held in place by an elastic band that did not constrain head movement. This process ensured the minimization of skin irritation at the electrode site during the delivery of the galvanic current. The stimulus intensity was individually adjusted through a process by which repeated stimulations of progressively increasing amplitude (in steps of 0.15 mA) were applied until a criterion threshold was reached [14]. This was defined as the stimulus amplitude at which a consistent bipolar ML CoP response was observed (Fig. 1c). This procedure ensured that the GVS amplitude evoked a similar postural response across all participants. As a result, the GVS amplitude was set at 1.65 ± 0.58 mA and 1.58 ± 0.52 mA for the young and older group, respectively. A t-test on the stimulus amplitudes indicated these were not significantly different between groups. Participants were asked to verbally report the experience of any unpleasant sensations during the familiarization and experimentation phase or after the experiment. The second part of the familiarization phase consisted of exposure to Achilles tendon vibration for 15 s in order to acquaint the participant with the vibratory stimulus [15]. During the experiment participants stood on the force platform in a relaxed position (eyes open, inter-malleolar distance: 10 cm, arms freely hanging by the sides). Standing period was split into three 60 s phases (Fig. 2): (a) the pre-perturbation phase with accurate visual and proprioceptive input, (b) the perturbation phase in which the visual surround oscillated in the AP direction and bilateral Achilles tendon vibration was concurrently applied and (c) the post-perturbation phase in which accurate vision and proprioception were re-inserted. The two perturbations, visual and proprioceptive, were also delivered separately in two additional 60 s phases. Postural responses to the isolated perturbations are shown in two figures submitted as supplementary material to this article. Participants performed two postural tasks in a randomized order: a Quiet Stance (QS) task and a GVS task. During the GVS task, a total of 15 GVS stimuli (each lasting 2 s) were delivered at quasi-random times, 5 within each 60 s phase. Specifically, one GVS stimulus was delivered randomly between the 4th and 8th of each 12 s time interval. 2.4. Data and statistical analysis Kinetic and kinematic data were processed using customized MatLab software (Mathworks Inc, Natick, USA). The CoP displacement and C7 pitch rotation signals were low-pass filtered with a 4th order zero-lag Butterworth filter (5 Hz cut-off) and then segmented into five 12 s time intervals (T1–T5) in order to quantify adaptation within each phase. Postural sway variability was quantified by calculating the Root Mean Square (RMS) of the CoP displacement and C7 rotation across each time interval. In the GVS trials, the RMS was calculated over the time interval consisting of the 4 s before the delivery of the GVS pulse, ending at stimulus onset (Fig. 1c). In order
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Fig. 1. (a) An illustration of the visual surround (i.e. virtual room) used in both stance tasks. The virtual room consisted of an alternating light and dark gray bar pattern to optimally stimulate the visual system, (b) a 2 s bipolar sinusoidal GVS current (gray line) delivered at a quasi-random onset time in each 12 s window, (c) representative Center of Pressure (CoP) time series in the mediolateral (ML) direction during a single 12 s interval of the galvanic vestibular stimulation (GVS) task (black line). GVS was followed by Stabilization Time (ST), during which the participant regained equilibrium sway. The 4 s stance period prior to the GVS event was selected to calculate the Root Mean Square of the CoP displacement.
to ensure that the participant returned to a stable postural equilibrium prior to the 4 s period that was used to calculate the RMS, stabilization time was computed. Stabilization time was defined as the time in seconds for which the RMS pre-GVS was greater than the RMS post-GVS. Stabilization time was calculated using an AutoRegressive Moving Average model in which the expression (1 s pre-avoidance RMS) ≥ (1 s post-avoidance RMS) was recursively evaluated.
Postural sway variability (RMS of CoP displacement and C7 rotation) was compared between tasks (QS, GVS), groups (Young, Old), across phases (pre-perturbation, perturbation, postperturbation) and the time intervals (T1–T5) by employing a 2(Task) × 2(Group) × 3 (Phase) × 5(Time Interval) Repeated Measures ANOVA model. In cases where the statistical output revealed a violation of the sphericity assumption, the Greenhouse-Geisser correction has been applied in the analyses of the respective factors
Fig. 2. Representative Center of Pressure (CoP) time series in the anteroposterior (AP) direction of a young (black line) and an older (gray line) participant during the pre-perturbation, perturbation and post-perturbation phases of a the quiet stance (a) and the GVS (b) trial.
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Fig. 3. Root Mean Square of Center of Pressure displacement (RMS dCoP) for the young (a) and old (b) group across the five time intervals (T1–T5) of the pre-perturbation, perturbation and post-perturbation phases. Group mean ± SE values are plotted for the Quiet Stance (QS, circles) and Galvanic Vestibular Stimulation (GVS, squares) task. Asterisks (*) indicate significant differences between the two tasks at p < 0.05.
and interactions. Significant interaction effects were further analyzed using post hoc paired samples t-tests between the respective factor levels. Bonferroni–Holm adjustments were applied to correct for multiple comparisons.
3. Results Representative CoP displacement traces in the AP direction for one young and one old participant during performance of the QS and GVS task are plotted in Fig. 2. Administration of Achilles tendon vibration and concurrent exposure to visual field oscillations resulted in a backward CoP displacement in both age groups (Fig. 2a). Although this backward shift was greater for the old participant in the QS task, this age difference was not evident in the GVS task (Fig. 2b). Overall, CoP displacement variability was significantly greater in the Old compared to the Young group (F(1, 21) = 5.14, p < 0.05) and also greater as a result of the concurrent visual and proprioceptive perturbation (F(1.51, 31.61) = 53.26, p < 0.001; Fig. 3). Contrast effects revealed that, compared to the pre-perturbation phase, the RMS of CoP significantly increased during the perturbation phase (F(1, 21) = 98.16, p < 0.001) and remained increased in the postperturbation phase (F(1, 21) = 117.29, p < 0.001). Intermittent GVS decreased the excessive CoP displacement induced by the concurrent visual and proprioceptive disturbance during the perturbation phase (F(1.43, 29.93) = 8.35, p < 0.01). Specifically, the RMS of CoP was significantly smaller in the GVS compared to the QS task during the perturbation phase (F(1, 21) = 13.82, p < 0.01) whereas the difference in sway variability between the two tasks was not significant in the pre- and postperturbation phases (Fig. 3). Interestingly, a significant Task by Group interaction (F(1, 21) = 4.35, p < 0.05) further revealed that the stabilizing effect of GVS on the excessive sway induced by the multisensory perturbation was age specific. Post hoc pair wise comparisons indicated that during the perturbation phase, the RMS of CoP was significantly smaller in the GVS than the QS task at T1 (t(11) = 2.91, p < 0.05), T2 (t(11) = 2.29, p < 0.05), T3 (t(11) = 3.46, p < 0.01) and T5 (t(11) = 2.46, p < 0.05) for the young group participants only (Fig. 3a). A significant difference between the two tasks was also noted in the 3rd (t(11) = 2.5, p < 0.05) and 5th (t(11) = 3.72),
p < 0.01) time interval of the post-perturbation phase. For the Old group on the other hand, there was no significant difference between the two tasks for any of the perturbation intervals (Fig. 3b) suggesting the elderly participants were not able to exploit the GVS stimulation in order to reduce the destabilizing effect of the perturbation. CoP displacement variability decreased across the successive time intervals of each phase in both tasks (F(1.78, 37.36) = 84.52, p < 0.001). This decrease was dependent on the phase of the task (F(2.16, 45.28) = 37.93, p < 0.001). Particularly, there was a significant decrease in RMS of CoP between T1 and T2 during the perturbation phase (F(1, 21) = 5.82, p < 0.05) and also a decrease between T1–T2 (F(1, 21) = 83.26, p < 0.001) and T2–T3 (F(1, 21) = 7.27, p < 0.05) when accurate information was re-inserted in the post-perturbation phase. Interestingly, a greater decrease between T1 and T2 was noted in the GVS compared to the QS task (F(2.79, 58.67) = 7.24, p < 0.001) particularly for the Old group in which the re-insertion of accurate input had a greater destabilizing effect on RMS of CoP (t(10) = 2.98, p < 0.05, Fig. 3b). Analysis of the C7 pitch rotation RMS data revealed similar results (Fig. 4). Specifically, a significant main effect of Task on the RMS of C7 rotation (F(1, 16) = 21.5, p < 0.001) confirmed that there was less upper trunk variability in the GVS compared to the QS task. This effect was specific to the Young group during the perturbation phase as shown by a significant Task × Group × Phase interaction (F(2, 32) = 7.59, p < 0.01). By contrast, GVS had no effect on elderly’s upper trunk sway in none of the three task phases.
4. Discussion In young participants, application of intermittent GVS reduced the excessive postural sway evoked by the concurrent visual and proprioceptive perturbation suggesting improved postural control possibly through a facilitation of the underlying sensorial reweighting. This finding is in concert with previous evidence showing a stabilizing effect of short-duration GVS in conditions of perturbed proprioception [11,12]. In the present study however, the stabilizing effect of GVS was noted after the offset of the postural response to the GVS pulse and in anticipation of the next pulse. Using stabilization time as a measure of the latency of the evoked postural
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Fig. 4. Root Mean Square of upper trunk pitch rotation (RMS C7)) for the young (a) and old (b) group across the five time intervals (T1–T5) of the pre-perturbation, perturbation and post-perturbation phases. Group mean ± SE values are plotted for the Quiet Stance (QS, circles) and Galvanic Vestibular Stimulation (GVS, squares) task. Asterisks (*) indicate significant differences between the two tasks at p < 0.05.
response, we ensured that participants returned to their baseline sway levels prior to the 4 s time window that was selected for calculating sway variability. In addition, whereas GVS evoked a postural response in the ML direction, it stabilized the sway induced by the multiple perturbations in the AP direction. This observation together with the long latency between the application of the GVS pulse and its stabilizing effect eliminates the possibility of a vestibular reflex pathway [16] as a plausible interpretation of the observed stabilizing effect. An alternative hypothesis that could explain this novel finding is that intermittent GVS increased the sensory reliance on the vestibular system. It is speculated that anticipation of short duration random GVS pulses could reduce the destabilizing effect of the concurrent tendon vibration and visual surround motion through opposite gain changes in the vestibular and proprioceptive-visual weights that can be set in either a feed-forward [17] or feedback manner [18]. Since GVS is not a self generated vestibular stimulus but signals an “artificial” head rotation, the CNS may detect that something odd is happening and increases the reliance or sensitivity of the vestibular system in sensing verticality. This speculation is supported by evidence showing an increased sensitivity of the postural control system to vestibular stimulation when somatosensory and proprioceptive information is disrupted [8,9]. A similar reweighting effect was elicited by the anticipation of visual collision avoidance events which had a stabilizing effect on the sway variability evoked by tendon vibration [19]. This was attributed to an increase in the visual weight evoked by visual anticipation which facilitated the shift from proprioceptive to visual dominance for controlling posture. In elderly participants, intermittent vestibular stimulation was not effective in reducing the destabilizing effect of the concurrently perturbed vision and proprioception on their posture. The aging vestibular system maintains its sensitivity to galvanic stimulation although the amplitude and latency of the Vestibular Evoked Myogenic Potentials evoked by GVS are reduced [20]. In the present study, all elderly participants had a consistent postural response to the GVS pulse confirming that they maintain their sensitivity to vestibular stimulation. It is argued however that the ability to exploit vestibular stimulation in order to reduce the destabilizing effect of the multisensory perturbation may be limited in aging due to vestibular degeneration. The greater postural disturbance evoked by the concurrent visual and proprioceptive perturbation
when compared to young controls suggests the possibility of an age related vestibular dysfunction in our older group participants. Vestibular dysfunction impairs the ability to suppress inaccurate cues for establishing verticality when vision and proprioception are concurrently perturbed resulting in increased visual bias in the perception of postural vertical [21,22]. Because elderly adults do not optimally use vestibular resources to regulate the effects of the multisensory perturbation they may not be able to exploit vestibular stimulation to increase sensory reliance on vestibular cues. This also suggests a less flexible sensorial reweighting process or even a lack of adaptability in the aging CNS. Intermittent vestibular stimulation facilitated the adaptation to the re-insertion of accurate sensory input. This was evident in the young CoP sway profiles but also in elderly upper trunk sway profile although the latter effect was not significant (Fig. 4b). Sway variability in the post-perturbation phase was higher than that in the pre-perturbation phase probably due to an after effect of the perturbation. Reinsertion of accurate visual and proprioceptive information resulted in an initial destabilization due to the time needed for the central integration of the newly inserted information [23,24]. The fact that sway variability was lower during GVS than the QS task in the post perturbation phase suggests that intermittent GVS may enable a more effective central integration of the newly inserted information after the offset of the perturbation. In conclusion, the current study has shown that intermittent GVS decreases the postural instability evoked by a simultaneous visual and proprioceptive perturbation. Elderly adults are less capable of exploiting vestibular stimulation to reduce the destabilizing effect of the multisensory perturbation. Further investigation of the effects of vestibular stimulation on the sensory reweighting of posture could lead to the development of novel balance prostheses tools and methods of balance rehabilitation. Acknowledgements The research leading to these results has received funding from the European Community’s Seventh Framework Program FP7/2007–2013 under grant agreement number 214728-2. We would like to acknowledge the Informatics and Telematics Institute of the Center for Research and Technology Hellas (CERTH) for providing technical assistance in the development of the virtual environment.
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Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.neulet. 2013.12.048. References [1] H.O. Karnath, M. Dieterich, Spatial neglect – a vestibular disorder? Brain 129 (2006) 293–305. [2] R.J. Peterka, Sensorimotor integration in human postural control, J. Neurophysiol. 88 (2002) 1097–1118. [3] A.M. Bronstein, L. Yardley, A.P. Moore, L. Cleeves, Visually and posturally mediated tilt illusion in Parkinson’s disease and in labyrinthine defective subjects, Neurology 47 (1996) 651–656. [4] G. Barbieri, A.S. Gissot, D. Perennou, Ageing of the postural vertical, Age (Dordr) 32 (2010) 51–60. [5] J.C. Menant, R.J. St George, R.C. Fitzpatrick, S.R. Lord, Perception of the postural vertical and falls in older people, Gerontology 58 (2012) 497–503. [6] R.C. Fitzpatrick, B.L. Day, Probing the human vestibular system with galvanic stimulation, J. Appl. Physiol. 96 (2004) 2301–2316. [7] I. Cathers, B.L. Day, R.C. Fitzpatrick, Otolith and canal reflexes in human standing, J. Physiol. 563 (2005) 229–234. [8] B.L. Day, M. Guerraz, J. Cole, Sensory interactions for human balance control revealed by galvanic vestibular stimulation, Adv. Exp. Med. Biol. 508 (2002) 129–137. [9] B.L. Day, J. Cole, Vestibular-evoked postural responses in the absence of somatosensory information, Brain 125 (2002) 2081–2088. [10] F. Hlavacka, C.L. Shupert, F.B. Horak, The timing of galvanic vestibular stimulation affects responses to platform translation, Brain Res. 821 (1999) 8–16. [11] M. Krizkova, F. Hlavacka, Binaural monopolar galvanic vestibular stimulation reduces body sway during human stance, Physiol. Res. 43 (1994) 187–192.
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Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Application of intermittent galvanic vestibular stimulation reveals age-related constraints in the multisensory reweighting of posture Diderik J.A. Eikema a , Vassilia Hatzitaki a,∗ , Dimitrios Tzovaras b , Charalambos Papaxanthis c,d a
Motor Control and Learning Laboratory, Department of Physical Education and Sport Science, Aristotle University of Thessaloniki, Greece Informatics and Telematics Institute, Centre for Research and Technology Hellas, 570 01 Thessaloniki, Greece c Université de Bourgogne, Unité de Formation et de Recherche en Sciences et Techniques des Activités Physiques et Sportives, F-21078 Dijon, France d Institut National de la Santé et de la Recherche Médicale (INSERM), U1093, Cognition, Action, and Plasticité Sensorimotrice, BP 27877, F-21078 Dijon, France b
h i g h l i g h t s • • • • •
Intermittent Galvanic Vestibular Stimulation (GVS) was applied during stance. Sensory reweighting was evoked by perturbing proprioception and vision. Intermittent GVS reduced excessive sway evoked by the multisensory perturbation. Intermittent GVS had no stabilizing effect in elderly’s sway. Intermittent GVS increases sensory reliance on the vestibular system.
a r t i c l e
i n f o
Article history: Received 22 July 2013 Received in revised form 28 November 2013 Accepted 21 December 2013 Keywords: Posture Aging Vision Proprioception Galvanic vestibular stimulation
a b s t r a c t In this study we examined the effects of intermittent short-duration Galvanic Vestibular Stimulation (GVS) during a multisensory perturbation of posture in young and elderly adults. Twelve young (24.91 ± 6.44 years) and eleven elderly (74.8 ± 6.42 years) participants stood upright under two task conditions: (a) quiet standing and (b) standing while receiving pseudo-randomly presented bipolar 2 s GVS pulses. In both conditions, sensory reweighting was evoked by visual surround oscillations (20 cm, 0.3 Hz) and Achilles tendon vibration (3 mm, 80 Hz), concurrently delivered during the middle 60 s of standing. Intermittent GVS decreased the excessive postural sway induced by the concurrent visual and proprioceptive perturbation in young but not in elderly participants. It is suggested that GVS increases sensory reliance on the vestibular system while elderly adults are less able to exploit this stimulation in order to reduce the destabilizing effect of the multisensory perturbation on their posture. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The vestibular system provides information on linear and angular head acceleration. This is combined with information from complementary sources such as vision and proprioception in order to establish an internal representation of the body’s position within the gravitational space [1]. The contribution of each sensory modality to this multisensory representation depends on the weight the Central Nervous System (CNS) assigns to each modality according to its perceived accuracy [2]. Vestibular cues are important in the
∗ Corresponding author at: Motor Control and Learning Laboratory, Department of Physical Education and Sport Science, Aristotle University of Thessaloniki, Thessaloniki 540 06, Greece. Tel.: +30 2310 992193; fax: +30 2310 992193. E-mail address: [email protected] (V. Hatzitaki). 0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2013.12.048
sensorial reweighting process because they reduce the effects of inaccurate vision and proprioception on the perception of postural vertical [3]. Advancing age impairs vestibular function due to loss of vestibular afferents [4]. As a result, elderly individuals display increased error and variability in the perception of the postural vertical, particularly in conditions of inaccurate vision and proprioception, which could result in an unstable posture and increased fall risk [5]. Short duration transmastoidal bipolar Galvanic Vestibular Stimulation (GVS) modulates the firing rate of vestibular afferents signaling head rotation through secondary neurons in the vestibular nuclei [6]. This results in the tonic reflex activation of the anti-gravity muscles eliciting a prolonged postural response in the medio-lateral direction when facing forward [7]. Existing evidence about the role of GVS in controlling posture under sensory perturbation conditions is conflicting. On one hand, postural responses to
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GVS increase in the absence of somatosensory or visual information [8,9] pointing to the increasing sensitivity of the vestibular system under conditions of sensory conflict. In this context, when GVS was applied synchronously or 500 ms prior to a backward platform translation the shift in the final equilibrium position was larger than the sum of the shifts for the galvanic stimulus and the platform translation alone [10]. On the contrary, stabilizing effects of GVS under sensory perturbations have also been reported. Application of bilateral, bipolar short duration GVS significantly reduced the antero-posterior sway velocity when standing on foam [11] and sway amplitude and latency in response to a simultaneous platform translation in the medio-lateral direction [12]. In this study, we were interested in the modulating after-effects of intermittent short-duration (2 s) GVS on body posture when vision and proprioception were concurrently disrupted in young and elderly adults. We perturbed vision by exposing participants to periodic Antero-Posterior (AP) visual field oscillations (20 cm, 0.3 Hz) and proprioception by bilateral application of continuous Achilles tendon vibration (3 mm, 80 Hz). The two perturbations were delivered simultaneously thereby increasing the system’s reliance on vestibular cues [13]. We hypothesized that intermittent GVS could reduce the destabilizing effects of the concurrent visual and proprioceptive perturbation on standing balance. We expected this effect to be less evident in elderly adults due to age associated vestibular degeneration. 2. Materials and methods 2.1. Participants Twelve young (5 males, 7 females; age 24.91 ± 6.44, mass 70.91 ± 13.93 kg) and eleven elderly (6 males, 5 females; age 74.8 ± 6.42, mass 78.44 ± 13.16 kg) adults participated in the study. Participants were free of neurological and musculoskeletal impairments and had normal or corrected to normal vision. Elderly participants were screened for cognitive dysfunction using the Mini Mental State Examination (MMSE). The MMSE cut-off score was set at 22. Participants were informed of the procedures and provided written consent. All experiments were performed with the approval of the local ethics committee on human research in accordance with the Declaration of Helsinki. 2.2. Apparatus and stimuli Visual stimuli were provided by a stereoscopic projection screen (Barco Baron 908, Barco N.V., Kuurne, Belgium, width 128 cm, height 102 cm), viewed through active shutter goggles (Chrystal Eyes 3, Stereographics, 105 Hz). The screen was located 200 cm in front of the participant, allowing for a horizontal viewing angle of 38◦ . The visual stimulus consisted of a 3D horizontal and vertical alternating light and dark gray bar pattern (Fig. 1a). This was a stimulus of contractive-expansive nature mimicking actual optic flow. During the perturbation phase the virtual surround oscillated (frequency: 0.3 Hz, amplitude: 20 cm), following a sinusoidal pattern along the AP axis. The surroundings were darkened to ensure the contribution of peripheral vision was limited. The proprioceptive perturbation of bilateral Achilles Tendon vibration (80 Hz, 3 mm amplitude) was delivered by a pair of cylindrical mechanical vibrators (VB115, Technoconcept, Mane, France). GVS waveforms were generated by a data-acquisition board (NI PCI-6221, National Instruments, Austin, USA) and delivered by a Model 2200 constant current isolator (A-M Systems, Carlsborg, USA). The current followed a sinusoidal waveform of a single cycle (cycle duration: 2 s, frequency: 0.5 Hz, amplitude: ±0.5 mA to 3 mA, Fig. 1b). The stimulus was bilaterally applied to the
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mastoid processes through conduction gel-coated 2 cm × 3 cm Stimex electrodes (Pierenkemper, Wetzlar, Germany). Postural sway was assessed with a force platform (Balance Plate 6501, Bertec Corporation, Columbus, USA, 100 Hz) recording Center of Pressure (CoP) displacement in the AP and Medio-Lateral (ML) directions and a six DoF electromagnetic tracker (Nest of Birds, Ascension Inc, Burlington, USA, 100 Hz) attached to the C7 vertebra that recorded upper trunk pitch rotation. 2.3. Task and procedure Prior to the experiment participants were familiarized with the vestibular and proprioceptive stimuli. GVS was applied using a bipolar binaural configuration with the anodal electrode attached on the left and the cathodal electrode on the right mastoid. Soft pads with an additional layer of electrode gel were placed over the electrodes and were held in place by an elastic band that did not constrain head movement. This process ensured the minimization of skin irritation at the electrode site during the delivery of the galvanic current. The stimulus intensity was individually adjusted through a process by which repeated stimulations of progressively increasing amplitude (in steps of 0.15 mA) were applied until a criterion threshold was reached [14]. This was defined as the stimulus amplitude at which a consistent bipolar ML CoP response was observed (Fig. 1c). This procedure ensured that the GVS amplitude evoked a similar postural response across all participants. As a result, the GVS amplitude was set at 1.65 ± 0.58 mA and 1.58 ± 0.52 mA for the young and older group, respectively. A t-test on the stimulus amplitudes indicated these were not significantly different between groups. Participants were asked to verbally report the experience of any unpleasant sensations during the familiarization and experimentation phase or after the experiment. The second part of the familiarization phase consisted of exposure to Achilles tendon vibration for 15 s in order to acquaint the participant with the vibratory stimulus [15]. During the experiment participants stood on the force platform in a relaxed position (eyes open, inter-malleolar distance: 10 cm, arms freely hanging by the sides). Standing period was split into three 60 s phases (Fig. 2): (a) the pre-perturbation phase with accurate visual and proprioceptive input, (b) the perturbation phase in which the visual surround oscillated in the AP direction and bilateral Achilles tendon vibration was concurrently applied and (c) the post-perturbation phase in which accurate vision and proprioception were re-inserted. The two perturbations, visual and proprioceptive, were also delivered separately in two additional 60 s phases. Postural responses to the isolated perturbations are shown in two figures submitted as supplementary material to this article. Participants performed two postural tasks in a randomized order: a Quiet Stance (QS) task and a GVS task. During the GVS task, a total of 15 GVS stimuli (each lasting 2 s) were delivered at quasi-random times, 5 within each 60 s phase. Specifically, one GVS stimulus was delivered randomly between the 4th and 8th of each 12 s time interval. 2.4. Data and statistical analysis Kinetic and kinematic data were processed using customized MatLab software (Mathworks Inc, Natick, USA). The CoP displacement and C7 pitch rotation signals were low-pass filtered with a 4th order zero-lag Butterworth filter (5 Hz cut-off) and then segmented into five 12 s time intervals (T1–T5) in order to quantify adaptation within each phase. Postural sway variability was quantified by calculating the Root Mean Square (RMS) of the CoP displacement and C7 rotation across each time interval. In the GVS trials, the RMS was calculated over the time interval consisting of the 4 s before the delivery of the GVS pulse, ending at stimulus onset (Fig. 1c). In order
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Fig. 1. (a) An illustration of the visual surround (i.e. virtual room) used in both stance tasks. The virtual room consisted of an alternating light and dark gray bar pattern to optimally stimulate the visual system, (b) a 2 s bipolar sinusoidal GVS current (gray line) delivered at a quasi-random onset time in each 12 s window, (c) representative Center of Pressure (CoP) time series in the mediolateral (ML) direction during a single 12 s interval of the galvanic vestibular stimulation (GVS) task (black line). GVS was followed by Stabilization Time (ST), during which the participant regained equilibrium sway. The 4 s stance period prior to the GVS event was selected to calculate the Root Mean Square of the CoP displacement.
to ensure that the participant returned to a stable postural equilibrium prior to the 4 s period that was used to calculate the RMS, stabilization time was computed. Stabilization time was defined as the time in seconds for which the RMS pre-GVS was greater than the RMS post-GVS. Stabilization time was calculated using an AutoRegressive Moving Average model in which the expression (1 s pre-avoidance RMS) ≥ (1 s post-avoidance RMS) was recursively evaluated.
Postural sway variability (RMS of CoP displacement and C7 rotation) was compared between tasks (QS, GVS), groups (Young, Old), across phases (pre-perturbation, perturbation, postperturbation) and the time intervals (T1–T5) by employing a 2(Task) × 2(Group) × 3 (Phase) × 5(Time Interval) Repeated Measures ANOVA model. In cases where the statistical output revealed a violation of the sphericity assumption, the Greenhouse-Geisser correction has been applied in the analyses of the respective factors
Fig. 2. Representative Center of Pressure (CoP) time series in the anteroposterior (AP) direction of a young (black line) and an older (gray line) participant during the pre-perturbation, perturbation and post-perturbation phases of a the quiet stance (a) and the GVS (b) trial.
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Fig. 3. Root Mean Square of Center of Pressure displacement (RMS dCoP) for the young (a) and old (b) group across the five time intervals (T1–T5) of the pre-perturbation, perturbation and post-perturbation phases. Group mean ± SE values are plotted for the Quiet Stance (QS, circles) and Galvanic Vestibular Stimulation (GVS, squares) task. Asterisks (*) indicate significant differences between the two tasks at p < 0.05.
and interactions. Significant interaction effects were further analyzed using post hoc paired samples t-tests between the respective factor levels. Bonferroni–Holm adjustments were applied to correct for multiple comparisons.
3. Results Representative CoP displacement traces in the AP direction for one young and one old participant during performance of the QS and GVS task are plotted in Fig. 2. Administration of Achilles tendon vibration and concurrent exposure to visual field oscillations resulted in a backward CoP displacement in both age groups (Fig. 2a). Although this backward shift was greater for the old participant in the QS task, this age difference was not evident in the GVS task (Fig. 2b). Overall, CoP displacement variability was significantly greater in the Old compared to the Young group (F(1, 21) = 5.14, p < 0.05) and also greater as a result of the concurrent visual and proprioceptive perturbation (F(1.51, 31.61) = 53.26, p < 0.001; Fig. 3). Contrast effects revealed that, compared to the pre-perturbation phase, the RMS of CoP significantly increased during the perturbation phase (F(1, 21) = 98.16, p < 0.001) and remained increased in the postperturbation phase (F(1, 21) = 117.29, p < 0.001). Intermittent GVS decreased the excessive CoP displacement induced by the concurrent visual and proprioceptive disturbance during the perturbation phase (F(1.43, 29.93) = 8.35, p < 0.01). Specifically, the RMS of CoP was significantly smaller in the GVS compared to the QS task during the perturbation phase (F(1, 21) = 13.82, p < 0.01) whereas the difference in sway variability between the two tasks was not significant in the pre- and postperturbation phases (Fig. 3). Interestingly, a significant Task by Group interaction (F(1, 21) = 4.35, p < 0.05) further revealed that the stabilizing effect of GVS on the excessive sway induced by the multisensory perturbation was age specific. Post hoc pair wise comparisons indicated that during the perturbation phase, the RMS of CoP was significantly smaller in the GVS than the QS task at T1 (t(11) = 2.91, p < 0.05), T2 (t(11) = 2.29, p < 0.05), T3 (t(11) = 3.46, p < 0.01) and T5 (t(11) = 2.46, p < 0.05) for the young group participants only (Fig. 3a). A significant difference between the two tasks was also noted in the 3rd (t(11) = 2.5, p < 0.05) and 5th (t(11) = 3.72),
p < 0.01) time interval of the post-perturbation phase. For the Old group on the other hand, there was no significant difference between the two tasks for any of the perturbation intervals (Fig. 3b) suggesting the elderly participants were not able to exploit the GVS stimulation in order to reduce the destabilizing effect of the perturbation. CoP displacement variability decreased across the successive time intervals of each phase in both tasks (F(1.78, 37.36) = 84.52, p < 0.001). This decrease was dependent on the phase of the task (F(2.16, 45.28) = 37.93, p < 0.001). Particularly, there was a significant decrease in RMS of CoP between T1 and T2 during the perturbation phase (F(1, 21) = 5.82, p < 0.05) and also a decrease between T1–T2 (F(1, 21) = 83.26, p < 0.001) and T2–T3 (F(1, 21) = 7.27, p < 0.05) when accurate information was re-inserted in the post-perturbation phase. Interestingly, a greater decrease between T1 and T2 was noted in the GVS compared to the QS task (F(2.79, 58.67) = 7.24, p < 0.001) particularly for the Old group in which the re-insertion of accurate input had a greater destabilizing effect on RMS of CoP (t(10) = 2.98, p < 0.05, Fig. 3b). Analysis of the C7 pitch rotation RMS data revealed similar results (Fig. 4). Specifically, a significant main effect of Task on the RMS of C7 rotation (F(1, 16) = 21.5, p < 0.001) confirmed that there was less upper trunk variability in the GVS compared to the QS task. This effect was specific to the Young group during the perturbation phase as shown by a significant Task × Group × Phase interaction (F(2, 32) = 7.59, p < 0.01). By contrast, GVS had no effect on elderly’s upper trunk sway in none of the three task phases.
4. Discussion In young participants, application of intermittent GVS reduced the excessive postural sway evoked by the concurrent visual and proprioceptive perturbation suggesting improved postural control possibly through a facilitation of the underlying sensorial reweighting. This finding is in concert with previous evidence showing a stabilizing effect of short-duration GVS in conditions of perturbed proprioception [11,12]. In the present study however, the stabilizing effect of GVS was noted after the offset of the postural response to the GVS pulse and in anticipation of the next pulse. Using stabilization time as a measure of the latency of the evoked postural
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Fig. 4. Root Mean Square of upper trunk pitch rotation (RMS C7)) for the young (a) and old (b) group across the five time intervals (T1–T5) of the pre-perturbation, perturbation and post-perturbation phases. Group mean ± SE values are plotted for the Quiet Stance (QS, circles) and Galvanic Vestibular Stimulation (GVS, squares) task. Asterisks (*) indicate significant differences between the two tasks at p < 0.05.
response, we ensured that participants returned to their baseline sway levels prior to the 4 s time window that was selected for calculating sway variability. In addition, whereas GVS evoked a postural response in the ML direction, it stabilized the sway induced by the multiple perturbations in the AP direction. This observation together with the long latency between the application of the GVS pulse and its stabilizing effect eliminates the possibility of a vestibular reflex pathway [16] as a plausible interpretation of the observed stabilizing effect. An alternative hypothesis that could explain this novel finding is that intermittent GVS increased the sensory reliance on the vestibular system. It is speculated that anticipation of short duration random GVS pulses could reduce the destabilizing effect of the concurrent tendon vibration and visual surround motion through opposite gain changes in the vestibular and proprioceptive-visual weights that can be set in either a feed-forward [17] or feedback manner [18]. Since GVS is not a self generated vestibular stimulus but signals an “artificial” head rotation, the CNS may detect that something odd is happening and increases the reliance or sensitivity of the vestibular system in sensing verticality. This speculation is supported by evidence showing an increased sensitivity of the postural control system to vestibular stimulation when somatosensory and proprioceptive information is disrupted [8,9]. A similar reweighting effect was elicited by the anticipation of visual collision avoidance events which had a stabilizing effect on the sway variability evoked by tendon vibration [19]. This was attributed to an increase in the visual weight evoked by visual anticipation which facilitated the shift from proprioceptive to visual dominance for controlling posture. In elderly participants, intermittent vestibular stimulation was not effective in reducing the destabilizing effect of the concurrently perturbed vision and proprioception on their posture. The aging vestibular system maintains its sensitivity to galvanic stimulation although the amplitude and latency of the Vestibular Evoked Myogenic Potentials evoked by GVS are reduced [20]. In the present study, all elderly participants had a consistent postural response to the GVS pulse confirming that they maintain their sensitivity to vestibular stimulation. It is argued however that the ability to exploit vestibular stimulation in order to reduce the destabilizing effect of the multisensory perturbation may be limited in aging due to vestibular degeneration. The greater postural disturbance evoked by the concurrent visual and proprioceptive perturbation
when compared to young controls suggests the possibility of an age related vestibular dysfunction in our older group participants. Vestibular dysfunction impairs the ability to suppress inaccurate cues for establishing verticality when vision and proprioception are concurrently perturbed resulting in increased visual bias in the perception of postural vertical [21,22]. Because elderly adults do not optimally use vestibular resources to regulate the effects of the multisensory perturbation they may not be able to exploit vestibular stimulation to increase sensory reliance on vestibular cues. This also suggests a less flexible sensorial reweighting process or even a lack of adaptability in the aging CNS. Intermittent vestibular stimulation facilitated the adaptation to the re-insertion of accurate sensory input. This was evident in the young CoP sway profiles but also in elderly upper trunk sway profile although the latter effect was not significant (Fig. 4b). Sway variability in the post-perturbation phase was higher than that in the pre-perturbation phase probably due to an after effect of the perturbation. Reinsertion of accurate visual and proprioceptive information resulted in an initial destabilization due to the time needed for the central integration of the newly inserted information [23,24]. The fact that sway variability was lower during GVS than the QS task in the post perturbation phase suggests that intermittent GVS may enable a more effective central integration of the newly inserted information after the offset of the perturbation. In conclusion, the current study has shown that intermittent GVS decreases the postural instability evoked by a simultaneous visual and proprioceptive perturbation. Elderly adults are less capable of exploiting vestibular stimulation to reduce the destabilizing effect of the multisensory perturbation. Further investigation of the effects of vestibular stimulation on the sensory reweighting of posture could lead to the development of novel balance prostheses tools and methods of balance rehabilitation. Acknowledgements The research leading to these results has received funding from the European Community’s Seventh Framework Program FP7/2007–2013 under grant agreement number 214728-2. We would like to acknowledge the Informatics and Telematics Institute of the Center for Research and Technology Hellas (CERTH) for providing technical assistance in the development of the virtual environment.
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