ELSEVIER Gait and Posture 6 (1997) 210-217

Monaural and binaural galvanic vestibular stimulation in human dynamic balance function

Alexandra SCverac Cauquil a**, Philippe Bousquet b, Marie-Claude Costes Salon ‘, Philippe Dupui a, Paul Bessou a

a Centre de Recherche Cerveau et Cognition UMR 5549, Facultl de Mkdecine, 133 Route de Narbonne, 31062 Toulouse cedex, France b Service de Neurochirurgie, Hapital de Rangueil, I Avenue Jean Pouilh& 31403 Toulouse cedex 4, France

Accepted 13 November 1996

Abstract

Spontaneous dynamic balance reactions to galvanic binaural and monaural stimulation were investigated in lateral sway. Low-intensity currents were used to stimulate the vestibular apparatus of subjects, who were standing with their eyes closed on a rocking platform. Head and body base movements were measured in the lateral plane, simultaneously. In monaural as well as in binaural stimulation mode, the onset of the current induced a lateral biphasic stereotyped postural responses: firstly the pressure centre moved towards the cathode side then the whole body swayed towards the anode side. The cut-off of the current resulted in a similar pattern of movement but in the opposite direction. Two main features characterised the response obtained in monaural mode. First, the amplitude of the dynamic balance response was half the size of that recorded in binaural stimulation mode. Second, cathodal monaural stimulation on one side or anodal monaural stimulation on the opposite side elicited superimposable responses. The results demonstrate that in healthy subjects, postural response to binaural galvanic vestibular stimulation results from the linear sum of two equivalent stimulations: one from the cathodal excitation and the other from the anodal inhibition. The method could be used in clinical studies to detect vestibular asymmetries and dysfunction. 0 1997 Elsevier Science B.V.

Keywords: Vestibular system; Galvanic stimulation; Dynamic balance; Human

1. Introduction

Galvanic vestibular stimulation (GVS), though known since the last century [l], has not been widely used either in experimental or in clinical vestibular investigations, this is probably because the mechanisms of action of the electric current on the vestibular ap- paratus long remained questionable. There is evidence that the current has a peripheral action [2] and could act by modulating the tonic firing rate of vestibular afferent. In squirrel monkey, Goldberg et al. [3] have shown that externally applied cathodal current en-

*Corresponding author. Tel.: + 33 5621 72835; fax: + 33 5621 72809.

0966-6362/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SO966-6362(97)0001 1-8

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hances the vestibular nerve discharge whereas anodal current decreases it.

Early observations [4] described in humans the re- sponses to GVS according to the polarity of the stimu- lus. A postural response was observed for lower intensities (head and body tilt, at 1 mA), ocular re- sponses required higher intensities (nystagmus, at 3 mA). The postural response in humans has been usually recorded using a force-platform [5,6], electromyo- graphic activity of leg muscles [7- lo], or accelerometers placed at different sites of the body [9] of subjects standing still, usually on a stable base. In these condi- tions, the bipolar binaural galvanic stimulation of the vestibular apparatus has been shown to induce stereo- typed body sway response, directed along the binaural

Fig. I. (A) The stabilometer used to elicit and assess spontaneous dynamic balance function: platform with a curved base in contact with the ground through a line, the pivot (p.). When the platfotm tilts, a lever (1.) fixed to an extremity of the platform slides on the ground and rotates around its point of fixation. The rotation is assessed by an optic coder (o.c.). (B) The ataxiameter used to measure head linear displacement in the pivot plane. A string tightened between the head band (h.b.) fixed around the head and a pulley transmits head displacements to an optic coder (cc.) fixed to the shaft of the pulley. (C) Position of the subject on the platform to measure lateral body sway.

axis towards the ear bearing the anode [I 1,121. When the stimulus polarity is reversed, the GVS-produced balance reaction is inverted. Nevertheless, this does not indicate the part each side of the vestibular system is playing in the whole response.

The clinical interest of GVS has already been sug- gested and shown (e.g. [1,13-171. However, as the oculomotor response was mainly chosen as the response parameter, relatively strong intensities of stimulation were used ( > 1 mA). Moreover, the stimulations were often applied binaurally, which may be not ideal to assess unilateral vestibular function. Indeed Dix et al clinical observations [13,14] pointed out the interest of monaural GVS.

In the present work, we investigated the hypothesis that the body response to binaural GVS in humans results from the linear sum of two equivalent opposite actions, exerted on each vestibular apparatus: excita- tion on one side (cathodal stimulation) and inhibition on the other side (anodal stimulation). This could be of some interest in clinical assessment of unilateral vestibular function. For that, we compared the effect on balance of a bipolar monaural and a bipolar binau- ral stimulation of subjects facing straight ahead. Spon- taneous dynamic balance conditions were used to enhance the response since the effect of monaural GVS was expected half as large as the binaural one. Indeed, the responses to GVS are larger when the subjects stand on an unstable platform [lo]. In a previous study on motion sickness [ 1 S], standardised dynamic balance proved to be a sensitive and efficient means to detect the postural responses to GVS. The present study only deals with lateral sway since the subjects are facing straight ahead, anteroposterior body response to GVS only occurring when subjects rotate their head or trunk so as to align their binaural axis to the sagittal plane.

Part of the present data have been presented in a brief form [19,20].

2. Methods

2.1. Gulvanic vestibular stimulatiw

The stimulus was delivered by a DC stimulator driven by the microcomputer through two disposable electrodes (1 cm diameter) coated with conductive jelly and stuck on the skin. The stimulation device was a stimulator operating with 9-V batteries and driven by infrared command (thus unplugged in the mains power). The intensity of the current used was 0.4 mA, sufficient to induce a postural response [2X] but low enough to avoid any local cutaneous sensation and therefore awareness of the stimulation. The duration of the stimulation (7 s) was long enough to study and differentiate both phasic and tonic effects of the current application. Two different stimulation patterns were used, binaural and monaural. In the binaural mode the electrodes were situated over the mastoid bones, in the monaural mode one electrode was stuck on the fore- head and the other on the mastoid bone.

Spontaneous dynamic balance conditions were ob- tained by asking the subject to stand on a stabilometer [22] derived from Freeman platforms used to develop co-ordination of the calf muscles [23]. The stabilometer consisted of a square platform (50 x 50 cm) supported by a segment of a cylinder (radius 55 cm, 6 cm height when horizontal) laying on the ground (Fig. 1). The fixed characteristics of the stabilometer produce stan-

212 A. SPwrac Cuuquil er al. _I Gait and Posture 6 (1997) 210-217

Table 1

Cathode right Cathode left

R s PI P2 R s Pl P2

HMA (cm) 5.2 + 0.2 14.7 + 0.6 14.4 + 0.6 5.6 + 0.3 4.9 ) 0.2 14.3 + 0.5 13 +0.4 5.4 * 0.2 PMA (cm) 7.0 + 0.4 13.1 * 0.4 13.4 * 0.4 7.5 + 0.4 6.6 f 0.3 12.5 i. 0.3 12.5 + 0.3 6.9 + .0.3

Means (n = 30) and standard errors of the maximum amplitude of the head (HMA) and pivot (PMA) displacements, in lateral dynamic balance, measured before (R), during (S) and after (Pl and P2) binaural galvanic vestibular stimulation.

dardised conditions for subjects instability. The device reduces the area of support of a subject standing on it to a 50-cm line called the pivot. Because of the geome- try of the platform, at a given instant, the position of the pivot on the ground is the vertical projection of the centre of pressure of the subject on the platform. The measurement of the linear displacements of the pivot on the ground induced by a tilt of the platform was computed from the rotation of a lever, one extremity of which laid freely on the ground and slided with mini- mal friction according to the tilts of the platform. The lever rotation was assessed by an optical coder linked to a microcomputer fitted with a specific program (fre- quency sampling: 100 Hz; accuracy: 0.7 mm). The mechanical response time of the ‘subject-stabilometer’ system (mean weight 75 kg) had been calculated by recording the pivot deviation elicited by a twitch of the triceps surae muscle obtained by stimulating the poste- rior tibia1 nerve (ptn) in both anteroposterior and lat- eral sway. We subtracted the delay of the EMG response to this stimulation (approximately 8 ms, [24]) from the response delay measured on averaged graphs (n = SO), giving a 178-ms ( + 8.13) mechanical response time. Therefore latencies could be calculated by sub- tracting the mechanical delay of the recording system from the response delay measured on the graphs.

Head position, as well as support surface position, was recorded to analyse a global body response. An ataxiameter [25,26] was used to measure the head movements in the same plane as that of the pivot movements (Fig. 1B). A string was tightened between the head and a pulley by a small weight (20 g), the axis of the pulley supported an optical coder, linked to the microcomputer, that sampled head displacements at IOO-Hz and provided recordings with an accuracy of 0.2 mm.

Lateral sway was explored by making the subject stand on the platform with his frontal plane normal to the plane of translation of the pivot, which oscillated right-left (Fig. IC). The ataxiagrams and the stabilo- grams plot the amplitude (cm) of head and pivot dis- placements, respectively, against time. In this work, maximum amplitude (cm) of the head displacement (HMA) and maximum amplitude of the pivot displace- ment (PMA) during each recording period (7 s) were

the parameters used to assess and quantify dynamic balance skill.

2.3. Experimental protocol

With local ethics committee approval, the experi- ments were carried out on 30 healthy volunteers, 15 men and 15 women (age ranging from 29 to 46; mean height: 169.6 + 8 cm; mean weight: 64.3 + 7 kg), who gave their informed consent prior to their inclusion in the study. The subjects stood on the stabilometer, the head facing forwards with eyes closed. Each test con- sisted of the repetition of four contiguous sequences, each subdivided into four periods of 7 s: the reference period (R), the stimulation period (S), the 1st post-stim- ulation period (Pl) and the 2nd post-stimulation period 059.

For the binaural mode, the two stimulus polarities (cathode on the right and cathode on the left ear) were studied. For the monaural mode, four stimulation pat- terns were investigated: cathode on the right and cathode on the left ear with anode on the forehead, anode on the right and anode on the left ear with cathode on the forehead.

The trials were pseudo-randomly distributed to avoid any order effect.

2.4. Statistical analysis

The effects of GVS on dynamic balance parameters were statistically tested by an ANOVA with repeated measures with 3 factors: one factor ‘Stimulation’ with four levels (R, S, Pl and P2), one factor ‘Repetition’ with four levels corresponding to the four contiguous sequences and one factor ‘Cathode Side’ with two levels (cathode on the right, cathode on the left). For the monaural tests, the factor ‘Cathode Position’ with two levels (cathode on the forehead, cathode on the mas- toid) was also examined. Post-hoc testing was per- formed with the method of contrasts and Sheffe’s test (numerical results are given as means + SEM in text and Tables 1 and 2).

Continuous movements of the platform characteris- ing the dynamic balance constitute a background noise that, although valuable to reveal the response to GVS,

interferes with a precise determination and measure of the delays and amplitudes of the responses. It is possi- ble to cope with this by averaging recordings synchro- nised from the onset of the stimulation. Records could be averaged within subjects to obtain more accurate response patterns of each of them. The individual re- sponse patterns were then averaged between subjects to obtain the response of the whole population sample. We also displayed the average plus or minus the stan- dard deviation as an indication of the variability.

3. Results

.:. I. Binnlrurd ,.&nnic wstihlar stimulrtiorl

Binaural galvanic stimulation induced stereotyped spontaneous dynamic lateral balance reactions in the 30 subjects. The results presented below concern trials performed with the cathode on the right mastoid and the anode on the left mastoid. With the opposite polar- ity (cathode on the left side) the shape of the ataxia- gram and the stabilogram recorded was symmetrical.

The single recordings from one subject (Fig. 2A) as well as the average recordings from the 30 subjects undergoing a GVS test (Fig. 2B) show that stereotyped lateral biphasic balance reactions occurred during both the stimulation and the post-stimulation periods.

The earliest balance change induced by the galvanic stimulus was a movement of the pivot towards the cathode side, the head remaining stable. The pivot

rat-k ?

,4node on forehead/ Cathode on forehead/ Cathode on mastoid Anode on mastoid

Right Left Right Left _.-. ._.~.~.. -..- ~..-..~--.-._. .-___- ~.- HMA (cm) 5.2 _t 0.2 5.4 * 0.’ 5.0 + 0.2 5.1 2 0.2

R HMA (cm) _ ‘I.2 + 0.4 9.2 rt 0.4 8.9 + 0.3 8.4 + 0.3

s HMA (cm) 4.2 & 0.4 8.S _t 0.4 9.2 + 0.3 8.5 * 0.3

Pi HM.4 (cm) i j co.3 _. 5.5 .* 0.3 5.2 2 0.2 5.0 + 0.2

P:! PMA (cm) 6.4 -i-r 0.3 6.5 f. 0.3 6.3 i 0.2 6.3 i 0.3

R PMA (ml) s 9.1 yo.4 4.2 f 0.3 8.6 & 0.3 8.6 ) 0.3 PMA (cm) Y I ~. !I.4 s.s y cl.3 8.9 + 0.3 8.9 & 0.3

PI PM4. (cm) 6 8 c 0 3 6.4 I: 0.3 6.2 r 0.2 6.0 + 0.2

P2 --__~ ~---

Means (n = 30) and standard errors of the maximum amplitude of the head (HMA) and pivot (PMA) displacements, in lateral dynamic balance, measured before (R). during (S) and after (Pl and P2) monaural galvanic vestibular stimulation,

displacement began 280 f 47 ms after the onset of the stimulus. Therefore the response Latency could be esti- mated at 102 ms (see method). The maximum right- wards displacement (1.88 + 0.24 cm) was reached at 610 + 20 ms. This indicates the development of a verti- cal force on the stabilometer causmg a tilt of the platform (right side down, left side up). ‘The second part of the response was an ensuing large movement of the body (detected at both the head and support base level) in the opposite direction, i.e. towards the anode side. The total displacement of the pivot was 10.67 2 0.65 cm and that of the head 12.6 15 I. Ih cm. During the remainder of the stimulation time the pivot and the head positions were different from the baseline al- though they tended to return slightly towards it. At the end of the stimulation, the pivot and the head were respectively 3.8 cm and 5.4 cm Ectt :,I their position before stimulation.

During the post-stimulation period. the stabilogram and the ataxiagram. instead of progress&cl!, returning towards their baseline. showed shapes iooking like those of the initial part of the S period but in the opposite direction. After a 275 2 I I .3-m delay i.c. at 97 ms latency (see method) the pivot underwent a displacement of I .86 i 0.13 cm leftwards (anode side) whereas the head remained in the satnc position. Then the pivot and the head underwent an 10.9 2:: 0.65 cm and a 11.18 i 0.85cm displacement rightwards, respec- tively. Later on, they returned towards the position they occupied before the stimulation, without recover- ing it completely at the end of the records.

The stereotyped balance reactions <:niailcd statisti- cally significant changes of the amplitude ol‘ the head and pivot displacements. Table 1 contains the mean values measured during the four periods of the lirst sequence of stimulation. A strong effect “Sttmulation’ was found for HMA (F= 215.67: P <. C).OOl) and PMA (F- 240.78; P = 0.001). The factor ‘C’athode Side’ did influence neither HMA (F= 2.31, P :=: !). 14) nor PM.4 (F- 3.45, P = 0.128 ). The effect ‘Repetition’ did not influence signihcantlv any dynamic balance parameters (HMA: F= 1.99, P=O.351; PMA: r”:=r).664. P.= 0.576). evidencing neither habituation nor sensitisation to the electrical stimulus.

The upper part of Fig. 3 represents the average recordings from the 30 subjects in two different condi- tions of monaural GVS. In Fig. 3.4 the cathode was on the right mastoid and the anode on lhc forehead, in Fig. 3B the cathode was on the forehead and the anode on the left mastoid. Three points arise: (i) monaural GVS induced stereotyped lateral dynamic balance reac- tions. with a similar time course to that induced by binaural GVS. The amplitudes of the iirst. part of the

214 A. Sherac Cauquil et al. /Gait and Posture 6 (1997) 210-217

Amplitude (cm)

Fig. 2. Curves recorded during binaural galvanic stimulation, cathode on the right mastoid and anode on the left mastoid (S: period of stimulation). (A) Single ataxiagram (upper curve) and stabilogram (lower curve) of subject no. 16. (B) Average (n = 30) ataxiagram and stabilogram; dotted lines: minus standard deviation of the average ataxiagram and plus standard deviation of the average stabilogram. The two bottom windows contain expanded zones of the average curves, within the limits indicated by the frame.

reaction, occurring at 276 + 11.3 ms, i.e. at a 9%ms latency, were equal (0.77 + 0.21 cm for cathode on the right; 0.9 + 0.13 cm for cathode on the forehead). The following large movements of the pivot and the head in the opposite direction were also of similar amplitude in both the monaural conditions: 5.76 + 0.37 cm and 5.35 + 0.33 cm for the pivot and 6.24 + 0.57 cm and 6.08 f 0.38 cm for the head; (ii) anodal stimulation of one side induced body sway superimposable on that induced by cathodal stimulation of the opposite vestibular apparatus and (iii) the amplitude of the responses recorded in monaural were half the size of the response obtained in binaural mode. When tti sum of average recordings of Fig. 3A and Fig. 3B is plotted as in Fig. 3C, the curves are totally superimposable to those obtained by binaural GVS (superimposed thick curve).

In monaural as in binaural GVS, the cut-off of the stimulation also induced stereotyped responses. The reversal of the stimulus polarity in monaural GVS inverted the direction of the response (not illustrated).

Table 2 contains the mean values of dynamic balance parameters measured during monaural GVS. The in- crease of the maximum amplitude of the head and pivot displacements is half as high as during binaural GVS but nevertheless, monaural GVS induced a significant increase of the parameters during S and Pl (P < 0.001, HMA: F = 164.4; PMA: F = 156.4). The balance parameters were not influenced by either the cathode side (right or left; HMA: F = 1.36, P = 0.253; PMA: F = 0.088, P = 0.769) or the cathode position (forehead or mastoid; HMA: F= 1.33, P = 0.257; PMA: F= 2.33,

P = 0.137).

4. Discussion

Previous works have shown that the motor responses to a galvanic stimulus are well organised and stereo- typed. The present study demonstrates that a large, reproducible, stereotyped response can also be obtained in spontaneous dynamic balance conditions, using a

A. SPverac Cauyuil et al. ./Gait and Posturr 6 (1997) -710 -217 315

A

Amplitude (cm) lo-

left

-1o right

B

Amplitude (cm) 10 -

left

z$&

Fig. 3. (A. B) Average (n = 30) curves recorded during monaural galvanic vestibular stimulation. (A) Cathode on the right mastoid and anode OII the forehead. (B) Cathode on the forehead and anode on the left mastoid. KY) Thin curves: sum of A and B recordings. Thick curves: for comparison. average recordings obtained in binaural mode (see Fig. 2).

low-intensity galvanic current. The responses to GVS were assessed by recording the movements of the body base (the pivot of the stabilometer) and the head in the same plane. Compared to EMG recording methods, the drawback of the approach used in the present work for studying balance is the introduction of a mechanical delay in the appearance of responses but, on the other hand, the advantage is to obtain a whole and not a partial response of the body muscles involved in the postural reaction. The responses of the different body segments were not investigated in this study, the results of the vestibular evoked postural adjustments were studied only at the head and the support area levels. The balance strategy could therefore only be inferred from the position of the two body extremities. Never- theless, this approach allowed the investigation of our hypothesis and provided the opportunity to discuss further the action of the galvanic stimulus on the vestibular apparatus.

4.1. Cathodal and anodal effects of’ the srimulatirm revealed by the monaural mode

When the vestibular system is functionally well bal- anced, as assumed for the subjects tested in this work, a monaural GVS with the anode on the right side induces the same postural sway as that induced by monaural GVS with the cathode on the left side. We can consider that in humans (as shown in the squirrel monkey by Goldberg et al. [3]), the cathode induces a vestibular excitation and the anode a depression of the same absolute amplitude. The very dose responses ob- tained in both monaural stimulations suggest that in healthy subjects the excitation on one side induces the same postural reaction as the inhibition of the same amplitude on the other side. Monaural GVS appears to act unilaterally on the vestibular apparatus. The present work suggests that in binaural GVS, two separate but simultaneous and equivalent actions on both right and

216 A. Stverac Cauquil et al. /Gait and Posture 6 (1997) 210-217

left vestibular apparatus add linearly. The postural responses induced by GVS with binaural electrodes indicates indirectly the sensory weight of the inter- vestibular imbalance within the multisensory motor control of the equilibrium. The part each side of the vestibular apparatus plays in this imbalance could only be determined by using successive monaural stimulation on each side. This presents a substantial interest for the clinical assessment of the separate function of the right and left vestibular system. This work supplies sufficient control data for undertaking now a clinical data collec- tion to confirm these results and validate the method as a clinical tool. Indeed, the diagnostic value of GVS has been reported. Monaural GVS has already been used to discriminate patients intoxicated with streptomycin [ 131 and patients affected with vestibular neuronitis [14] from normals. In these studies the body response was not quantified but mentioned as present or absent. Pfaltz and Richter [15] emphasised GVS usefulness in differentiating between a lesion of the sensory organ and a lesion of the peripheral nerve. Responses to GVS have been also found different in central vestibular lesions [ 16,271. Later clinical investigations renewed GVS usefulness in differentiating between a labyrinthine and retrolabyrinthine lesion [28]. However, these studies assessed GVS effect with nystagmography and used binaural GVS at a stronger stimulus intensity than the one used here. Our method could present a way to study unilateral vestibular function with very low and accurate stimulations and therefore to detect vestibular asymmetry.

tion: (i) firing rates change abruptly at the onset and the termination of the current step, (ii) change in the cur- rent flow direction changes the direction of the firing rate variation at the beginning and at the end of the current step, (iii) adaptation during perstimulation re- sponses occurs with either excitatory or inhibitory cur- rents.

4.3. Selective sensitivity of the labyrinth to galvanic stimulation

4.2. Effect of the current variation

Further studies remain necessary to elucidate the site of action of GVS. With the low intensity current used in our experiments, the specificity of the galvanic vestibular stimulation is shown by the fact that during the stimulation, subjects did not experience any audi- tory sensation, indicating that the galvanic stimulation did not involve cochlear sensory receptors. There is evidence that cochlear and ampullar systems can be stimulated by galvanic current with a stronger current intensity: an anteroposterior sway and a head or trunk rotation, and also nystagmus have been related by several authors as a result of 1 to 2 mA stimulation [5,29,30]. Acouphenes were felt by subjects during higher intensity stimulations [4]. This suggests that the electrical excitability threshold of the macular system is lower than those of the ampulla and the cochlea. The galvanic vestibular stimulation with low current inten- sity could be a means to study the postural response to a purely otolithic disturbance. Three dimensional eye movement recordings and psychophysical experiments (e.g. perceived verticality) would bring further argu- ment to discuss this hypothesis.

Balance responses occurring at the beginning and at the end of the galvanic current pulse have a similar shape in amplitude and duration but are opposite in direction. This feature, already stated in binaural GVS [2], has never been thoroughly discussed in previous studies dealing with the effect of electrical vestibular stimulation on static balance, although Nashner and Wolfson [7] reported similar results on EMG responses to electrical vestibular stimulation. The mirror symme- try of the two responses is made conspicuous here by the spontaneous dynamic balance conditions and by using long enough current pulses of stimulation. Such a result suggests a vestibular sensitivity to both phasic stimulations of opposite directions constituted by the onset and the cut-off of the current. In our experimen- tal conditions, the vestibular apparatus appears less sensitive to constant current flow.

The results presented here, although insufficient to explain the mechanisms of action of the GVS, put forward the usefulness of this method as a means to selectively study the vestibular function. GVS as used in this experiment was shown to stimulate efficiently the vestibular apparatus, inducing large, stereotyped dy- namic balance responses. Separate stimulation of the right or left vestibular system showed that excitation on one side is equivalent to inhibition on the other side and that the effects of both cathodal and anodal stimuli add linearly in binaural stimulation. This aspect could be useful for vestibular asymmetry investigation, by comparing dynamic balance responses evoked by uni- lateral stimulation of the vestibular apparatus.

Acknowledgements

The time course of the responses recorded in the This work was supported by grants from CNES present experiments are supported by those obtained by (Centre National d’Etudes Spatiales) and Fondation Goldberg et al. [3] who studied the responses of pour la Recherche Medicale. The authors wish to thank vestibular nerve afferents of the squirrel monkey to Dr B.L. Day for his helpful comments on the externally applied galvanic current pulses of 5 s dura- manuscript, MS K. Cullum for the English correction

A. SPverac Cauyuil et al. ,, Guir und Posrure 6 (1497) 2/O-_‘I 7 217

and J. Lamaison for building the software used in this study.

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