Neuroscience Letters 393 (2006) 5155

TENS to the posterior aspect of the legs decreases postural sway during stance
Ruth Dickstein , Yocheved Laufer, Miri Katz
Department of Physical Therapy, Faculty of Social Welfare and Health Studies, University of Haifa, Mount Carmel, Haifa 31905, Israel Received 4 August 2005; received in revised form 13 September 2005; accepted 15 September 2005

Abstract The purpose of this study was to examine the effect of Transcutaneous Electrical Nerve Stimulation (TENS) applied to the posterior aspect of the legs, on postural sway during stance. Thirty healthy subjects were tested while standing on a force platform under four stimulation conditions: no TENS, bilateral TENS, and unilateral left and right TENS. Thirty-second long tests, employing detection threshold amplitudes, were performed in three blocks. In each block, the four conditions were applied both with and without vision in a random order. The results indicate that the application of TENS brought about a decrease in postural sway as expressed by average sway velocity, in addition to a decrease in the absolute values of maximal and minimal medio-lateral and anteriorposterior velocity. Thus, similar to sub-threshold random electrical noise, it appears that the application of low-amplitude TENS to the lower limbs decreases postural sway during stance. Considering the ease of TENS application and the high prevalence of postural disorders, the potential clinical signicance of this observation is to be determined by further studies. 2005 Elsevier Ireland Ltd. All rights reserved.
Keywords: TENS; Kinesthesis; Proprioception; Balance; Postural control; Somatosensory; Stance

Transcutaneous Electrical Nerve Stimulation (TENS) is an easily applied and well-tolerated clinical modality. Although stimulation at sub-motor threshold amplitude is primarily used for reducing pain (by depolarizing A sensory bers) [2], other effects are also well established: TENS at different amplitudes (below and above sensory or motor threshold level) has been shown to affect the excitability of the soleus H reex, pointing to its potential to change excitability of spinal internuncial and/or motor neurons. The reported nature of that effect is not unequivocal; although prevailing ndings indicate an inhibitory effect that is expressed in reduction in amplitude and delayed latency [13,19], fascilatory effect with an increase in H reex amplitude has also been reported [10]. The reason for the different ndings probably derives from the inherent variability of the H-reex amplitude in normal subjects as well from the use of different stimulation paradigms in different studies [7]. Nevertheless, the effect of TENS on the H reex points to a TENS-mediated depolarization of Ia bers, in addition to the
Corresponding author. Tel.: +972 4 8249065; mobile: 972 50 6407135; fax: +972 4 8288140. E-mail address: ruthd@research.haifa.ac.il (R. Dickstein). 0304-3940/$ see front matter 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2005.09.039

well-established depolarization of A (II) somatosensory bers. Other effects of TENS on improving spasticity and postural control have been investigated. The ameliorating effect of TENS on upper motor neuron spasticity such as in post-stroke hemiparesis [28,31] and in multiple sclerosis [1] is further explained by TENS-mediated inhibitory processes at the spinal level [17,28]. However, the effect of TENS on muscle tone of healthy subjects is not well known. The application of TENS to the neck muscles on the paretic side of patients with hemispatial neglect has been shown to improve postural control and spatial orientation [9,22,26,34]. Although the mechanism behind these improvements is not well understood, it is presumed that cutaneous and proprioceptive information provided by the stimulation is subjected to high-order modulation, which facilitates egocentric and spatial orientation [26]. It is noteworthy that similar to the effect of TENS, vibration of the neck muscles on the affected body side can alleviate the postural and spatial disorders associated with hemispatial neglect [18,20,30]. Interpretations of the effect of vibration were similarly based on the development and updating of space representation and on re-calibration of the egocentric coordinate system [18,30].

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R. Dickstein et al. / Neuroscience Letters 393 (2006) 5155

The response of the postural control system to the application of TENS to the lower limbs is not yet well known. However, recent studies have shown that postural sway can be attenuated by the application of imperceptible white mechanical noise stimulation to the soles of the feet [29] as well as by the application of white electrical noise to the medial and lateral aspect of the knee of standing subjects [8]. These observations have been explained by the paradigm of stochastic resonance according to which a weak random stimulus can enhance the detection and transmission of a natural stimulus in biological systems [4]. More explicitly, it has been suggested that the subliminal stimuli at the sides of the knee joint activate joint proprioceptors causing a subsequent increase in knee position sense that facilitates stance stability [8]. In view of the hitherto evidence, the purpose of this study was to determine whether the application of electrical stimulation in the form of TENS to the posterior aspect of the legs affects the postural control and stance stability of healthy subjects. Participants were 30 healthy university student volunteers (10 men and 20 women) with a mean age of 25.4 years (ranging from 21 to 40). Five of them reported left leg dominance, as determined by the preferred kicking leg [25]. Prior to enrolment, each one of them completed a screening questionnaire to rule out symptoms of vertigo, ongoing balance problems, any known neuro-musculo-skeletal impairment, general malaise, consumption of alcohol or drugs in the 24 h before testing, and pregnancy. All accepted subjects signed an informed consent complying with the regulations of the Institutional Review Board. Postural control during stance was tested with the AMTI Balance Platform (AMTI, 176 Waltham Street, Watertown, MA 02472, USA) designed for measuring stance reaction forces and moments. Dedicated software (Accuswayplus ) controls data collection protocols, the continuous monitoring of the center of pressure (COP) and data storage and analysis. Prior to testing, adhesive TENS electrodes (5 cm2 ) were fastened to the skin overlying the left and right medial and lateral bellies of the gastrocnemius muscles. Testing was conducted with subjects standing with socks on the AMTI force plate and their upper extremities folded against the chest. A xed distance of 8 cm between the medial malleoli was kept with 10 between the feet. When assuming the testing position the rst time, the circumference of the feet of each subject was marked on the plate to assure the return to the same feet placement in each trial. Each subject underwent three blocks of testing, each consisting of a random sequence of eight trials. Each trial was composed of a unique combination of one of four stimulation modes [No TENS (NT), Bilateral TENS (BT), TENS Left (TL), and TENS Right (TR)] and one of two visual conditions [eyes open (EO), eyes closed (EC)]. The stimulation (bipolar balanced stimuli, pulse width 200 s, frequency of 100 Hz) was delivered by a dual-channel commercial TENS unit (Elpha battery 301 Moodie Drive, Suite 205 Ottawa, Ont. K2H 9C4, Canada). In conditions involving stimulation, TENS amplitude was adjusted before the start of measurements in increments of 0.01 mA and set at the sensory detection threshold of each subject.

The testing duration in each trial lasted for 30 s. A resting period of about 3 min was allowed between blocks but not between trials within a block. The data were saved on a PC computer and analyzed ofine. Postural sway was determined by the average sway velocity of the center of pressure during the testing period. In addition, in order to better appreciate the potential effects of TENS on extreme velocity values in both the anteriorposterior (AP) and medio-lateral (ML) directions, the maximal and minimal COP velocities in both dimensions were assessed. For each variable, the mean values of identical trials in the three blocks were used for analysis. Descriptive statistics and repeated-measures ANOVA were applied to compare between the effects of conditions of TENS (i.e., NT, BT, TL, and TR) and potential interaction with the effect of vision (i.e., EO and EC) with p-values equal to or less than 0.05 indicating statistical signicance. Preplanned contrasts were further applied to test the effects of NT against the pooled effect of the three TENS conditions. Given that the interaction between the effects of vision and TENS yielded non-signicant results (F = 2.4 (3, 27), p < 0.09 for average velocity), and considering the fact that the effect of vision on postural sway is well established, the following reported ndings address the pooled effects of TENS on postural sway in equivalent conditions of EO and EC. The application of TENS at threshold amplitudes (mean values of 3.6 (1.6) and 3.8 (1.4) mA for the left and the right leg, respectively) was associated with a signicant decrease in average sway velocity (F = 4.53 (3, 27), p < 0.01). Average sway velocity in the four conditions is presented in Fig. 1. Analysis of preplanned contrasts pointed to a signicant difference between the NT and the TENS conditions (F = 14.42 (1, 29), p < 0.0007). The mean decrease in sway velocity from NT condition to BT, TL, and TR was 0.032, 0.034, and 0.029 cm/s, respectively. Regarding maximal and minimal medio-lateral (ML, rightward = positive) and anteriorposterior (AP, anterior = positive) velocity, the ndings for the positive and negative directions consistently indicated a decrease/increase, respectively. Thus,

Fig. 1. Mean (+S.E.M.) average COP sway velocity under the four stimulation conditions.

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Fig. 2. Absolute values of mean (+S.E.M.) maximal (upper trace) and minimal (bottom trace) medio-lateral COP sway velocity under the four TENS conditions.

with TENS, the absolute values of both ML and AP velocity values decreased and came closer to the central zero value: the mean values of the maximal ML velocity are depicted in Fig. 2 (upper trace). The difference between the NT and the three TENS conditions pointed to a trend toward signicant decrease in maximal ML velocity due to the application of TENS (F = 3.59 (1, 29), p < 0.07). The ndings for the minimal ML velocity (Fig. 2, lower trace) indicated an overall effect of TENS (F = 4.87 (3, 27), p < 0.008) with the minimal velocity in the No TENS condition being signicantly more negative (higher absolute value) than the three TENS conditions (F = 5.30 (1, 29), p < 0.03). Regarding the maximal AP velocity (Fig. 3, lower trace) in comparison to the NT condition, TENS application in the three conditions caused a signicant decrease in its value (F = 4.94 (1, 29), p < 0.03). The ndings for the minimal AP velocity (Fig. 3, upper trace) pointed to a trend toward signicant decrease (F = 2.63 (3, 27), p < 0.07), which was characterized by a decrease in its absolute value, that is, a decrease in posterior directed velocity in each one of the TENS conditions. A trend for a superior effect of the left as opposed to the right application of TENS in decreasing sway was observed (see Figs. 13), yet that effect was not statistically signicant at the 0.05 level. The main outcome of this work is that the application of TENS at threshold amplitudes to the posterior aspect of the calves reduces postural sway during stance. The size of the effect of TENS on average sway velocity (decrease of 5%) is comparable to that reported by Gravelle et al. [8] (decrease of 3.1%) who tested postural sway during one-legged stance with

Fig. 3. Absolute values of mean (+S.E.M.) maximal (lower trace) and minimal (upper trace) anteriorposterior COP sway velocity under the four TENS conditions.

the application of white sub-threshold electrical noise stimulation. Since TENS is not a random stimulation, sway attenuation in the current study cannot be explained by stochastic resonance, which pertains specically to white noise stimuli [4,29]. Thus, if a common mechanism underlies the effects of both random noise stimuli and of TENS on postural sway, a more comprehensive hypothesis has to be formulated. Alternatively, it can be argued that stimulus dependent decrease in sway can be caused by different mechanisms depending on the type of electrical stimulation. The clinical signicance of the demonstrated effect is to be determined in future studies in which patients with impaired postural control are included. In addition, the question if TENS effect lasted beyond the stimulation period has not been addressed in the current work and awaits further research. One encouraging study of a subject with chronic post-stroke hemiparesis and decient somatosensory sensation, who was treated with TENS to the sole and lower calf of the affected leg, demonstrated gradual and substantial long-lasting functional improvement in the performance of gait and balance tasks [33]. However, as this is a case report, further conrmation of the results is required. Two complimentary interpretations can shed light on the observed decrease in postural sway attributable to TENS. The most straightforward explanation is the enhancement of somatosensory information from the legs. Accordingly, the addition of TENS sensory stimulation enhances the natural somatosensory inow from the lower limbs, which is relevant for the maintenance and regulation of orthograde posture. The contribution of proprioceptive information from the lower legs, especially from structures near the ankle joint, to upright stance is well substantiated [11,1416,21,27,35]. While both neck vibration and TENS stimulate somatosensory receptors that contribute to perception of verticality and postural orientation in subjects with hemispatial neglect [22,26], the current results indicate opposing effects of their application to the calves in healthy subjects. Thus, while vibration is associated with increase in AP sway [6,36], low-amplitude TENS was found to have a contradictory effect. Inherent differences between these mechanical and electrical stimulus modalities, the specic application of TENS at the sensory detection threshold as well as differential effects on corticomotor excitability may underlie these different effects. Nevertheless, whereas in prior studies vibration was commonly applied to stimulate proprioceptive lower limb afferents [5,6,36], the current ndings imply that we may be able to use TENS for the same purpose. The results broaden the scope of the established effects of TENS and vibration at the neck region in subjects with hemi-neglect, by showing that upright whole body postural control is also affected by TENS to the lower extremities. Obviously, the effects of stimulus parameters, stimulation sites, and comparison with the effects of vibratory stimuli are yet to be determined. Studies using Trans-Cranial Magnetic Stimulation (TMS) have provided evidence that the application of TENS at different body sites, both below as well as above motor threshold amplitudes signicantly affects cortico-motor excitability. Therefore,

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R. Dickstein et al. / Neuroscience Letters 393 (2006) 5155 [12] M. Heroux, F. Tremblay, L. Tremblay, M. Boisvenue, M. Carriere, J. Houston, Differential effect of peropheral electrical stimulation and vibratory stimulation on corticomotor excitability in lower limb muscles, Physiother. Can. 55 (2003) 153159. [13] K. Hiraoka, Neural mechanisms underlying the effect of transcutaneous electrical nerve stimulation in humans, Electromyogr. Clin. Neurophys. 42 (2002) 359366. [14] F. Hlavacka, T. Mergner, M. Krizkova, Control of the body vertical by vestibular and proprioceptive inputs, Brain Res. Bull. 40 (1996) 431434. [15] F.B. Horak, F. Hlavacka, Somatosensory loss increases vestibulospinal sensitivity, J. Neurophys. 86 (2001) 575585. [16] F.B. Horak, J.M. Macpherson, Postural orientation and equilibrium, in: J. Shepard, L. Rowell (Eds.), Handbook of Physiology, Oxford University Press, New York, 1996, pp. 255292. [17] C.W. Hui-Chan, M.F. Levin, Stretch reex latencies in spastic hemiparetic subjects are prolonged after transcutaneous electrical nerve stimulation, Can. J. Neurol. Sci. 20 (1993) 97106. [18] L. Johannsen, H. Ackermann, H.O. Karnath, Lasting amelioration of spatial neglect by treatment with neck muscle vibration even without concurrent training, J. Rehabil. Med. 35 (2003) 249253. [19] M.R. Joodaki, G.R. Olyaei, H. Bagheri, The effects of electrical nerve stimulation of the lower extremity on H-reex and F-wave parameters, Electromyogr. Clin. Neurophysiol. 41 (2001) 2328. [20] H.O. Karnath, K. Christ, W. Hartje, Decrease of contralateral neglect by neck muscle vibration and spatial orientation of trunk midline, Brain 116 (1993) 383396. [21] A. Kavounoudias, R. Roll, J.P. Roll, Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation, J. Physiol. 1 (2001) 869878. [22] C. Lafosse, E. Kerckhofs, M. Troch, E. Vandenbussche, Upper limb exteroceptive somatosensory and proprioceptive sensory afferent modulation of hemispatial neglect, J. Clin. Exp. Neuropsychol. 25 (2003) 308323. [23] T. Mima, T. Oga, J. Rothwell, T. Satow, J. Yamamoto, K. Toma, H. Fukuyama, H. Shibasaki, T. Nagamine, Short-term high-frequency transcutaneous electrical nerve stimulation decreases human motor cortex excitability, Neurosci. Lett. 355 (2004) 8588. [24] E. Naito, P.E. Roland, C. Grefkes, H.J. Choi, S. Eickhoff, S.Z. Geyer, Karl, H.H. Ehrsson, Dominance of the right hemisphere and role of area 2 in human kinaesthesia, J. Neurophysiol. 93 (2005) 10201034. [25] P.E. Niemuth, R.J. Johnson, M.J. Myers, T.J. Thieman, Hip muscle weakness and overuse injuries in recreational runners, Clin. J. Sport Med. 15 (2005) 1421. [26] D.A. Perennou, C. Leblond, B. Amblard, J.P. Micallef, C. Herisson, J.Y. Pelissier, Transcutaneous electric nerve stimulation reduces neglectrelated postural instability after stroke, Arch. Phys. Med. Rehabil. 82 (2001) 440448. [27] K.E. Popov, G.V. Kozhina, B.N. Smetanin, V.Y. Shlikov, Postural responses to combined vestibular and hip proprioceptive stimulation in man, Eur. J. Neurosci. 11 (1999) 33073311. [28] K.P. Potisk, M. Gregoric, L. Vodovnik, Effects of transcutaneous electrical nerve stimulation (TENS) on spasticity in patients with hemiplegia, Scand. J. Rehabil. Med. 27 (1995) 169174. [29] A. Priplata, J. Niemi, M. Salen, J. Harry, L.A. Lipsitz, J.J. Collins, Noise-enhanced human balance control, Phys. Rev. Lett. 89 (2002) 238101. [30] I. Schindler, G. Kerkhoff, H.O. Karnath, I. Keller, G. Goldenberg, Neck muscle vibration induces lasting recovery in spatial neglect, J. Neurol. Neurosurg. Psychiatry 73 (2002) 412419. [31] Y. Tekeoglu, B. Adak, T. Goksoy, Effect of transcutaneous electrical nerve stimulation (TENS) on Barthel Activities of Daily Living (ADL) index score following stroke, Clin. Rehabil. 12 (1998) 277280. [32] M. Tinazzi, S. Zarattini, M. Valeriani, S. Romito, S. Farina, G. Moretto, N. Smania, A. Fiaschi, G. Abbruzzese, Long-lasting modulation of human motor cortex following prolonged transcutaneous electrical nerve stimulation (TENS) of forearm muscles: evidence of reciprocal inhibition and facilitation, Exp. Brain Res. 161 (2005) 457464.

it appears that TENS may intervene in the modulation of highorder (cortical) motor responses including postural ones. Despite the fact that in most of these studies TENS was applied for at least 20 min and its effects were measured after the stimulation period [12,23,32], the minimal time period for TENS-induced motor effects has not been established. In the current work, as well in the study of Gravelle et al. [8] who applied white random electrical noise stimulation at sub-threshold amplitudes, time periods of less than a minute sufced to induce a postural response. Recent observations that weak imperceptible sensory stimuli can fully escape conscious perception and yet evoke EEG responses [3] support the notion of high-order effects of TENS. The observed side differences alluding to a more enhanced effect of left than of right side TENS are strengthened by recent suggestions that human kinesthesia is associated with a network of brain areas which include the right fronto-parietal areas, as well as by evidence for a right hemisphere dominance over perception of limb movement [24]. In conclusion, the ndings of the current study indicate that the application of TENS to the posterior aspects of the calves causes a decrease in postural sway during stance. The potential clinical signicance of such an effect calls for further elaboration of these ndings, especially considering the availability and simplicity of TENS application. References
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