Stochastic resonance stimulation improves balance in children with cerebral palsy: a case control study

Anastasia Zarkou, Samuel C K Lee, Laura A Prosser, Sungjae Hwang, John Jeka, Anastasia Zarkou, Samuel C K Lee, Laura A Prosser, Sungjae Hwang, John Jeka

Abstract

Background: Stochastic Resonance (SR) Stimulation has been used to enhance balance in populations with sensory deficits by improving the detection and transmission of afferent information. Despite the potential promise of SR in improving postural control, its use in individuals with cerebral palsy (CP) is novel. The objective of this study was to investigate the immediate effects of electrical SR stimulation when applied in the ankle muscles and ligaments on postural stability in children with CP and their typically developing (TD) peers.

Methods: Ten children with spastic diplegia (GMFCS level I- III) and ten age-matched TD children participated in this study. For each participant the SR sensory threshold was determined. Then, five different SR intensity levels (no stimulation, 25, 50, 75, and 90% of sensory threshold) were used to identify the optimal SR intensity for each subject. The optimal SR and no stimulation condition were tested while children stood on top of 2 force plates with their eyes open and closed. To assess balance, the center of pressure velocity (COPV) in anteroposterior (A/P) and medial-lateral (M/L) direction, 95% COP confidence ellipse area (COPA), and A/P and M/L root mean square (RMS) measures were computed and compared.

Results: For the CP group, SR significantly decreased COPV in A/P direction, and COPA measures compared to the no stimulation condition for the eyes open condition. In the eyes closed condition, SR significantly decreased COPV only in M/L direction. Children with CP demonstrated greater reduction in all the COP measures but the RMS in M/L direction during the eyes open condition compared to their TD peers. The only significant difference between groups in the eyes closed condition was in the COPV in M/L direction.

Conclusions: SR electrical stimulation may be an effective stimulation approach for decreasing postural sway and has the potential to be used as a therapeutic tool to improve balance. Applying subject-specific SR stimulation intensities is recommended to maximize balance improvements. Overall, balance rehabilitation interventions in CP might be more effective if sensory facilitation methods, like SR, are utilized by the clinicians.

Trial registration: ClinicalTrials.gov identifier NCT02456376; 28 May 2015 (Retrospectively registered); https://ichgcp.net/clinical-trials-registry/NCT02456376 .

Keywords: Afferent stimulation; Balance; Cerebral palsy; Postural control; Somatosensation; Stochastic resonance stimulation.

Conflict of interest statement

Ethics approval and consent to participate

Parents or legal guardians signed informed consents and participants under 18 years of age signed informed assent documents prior to participation. Eighteen-year-old subjects signed their own informed consent. The study was approved by the Western IRB and the Temple University IRB for Shriners Hospital for Children, Philadelphia, and the University of Delaware IRB.

Consent for publication

Not Applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Schematic illustration of the SR Stimulation System. Our system consisted of a computer and 4 stimulators. The SR signal was generated by a custom LabView control program to trigger the stimulators that subsequently delivered electrical SR stimulation in the muscles and ligaments of the ankle joints
Fig. 2
Fig. 2
Center of Pressure measures during upright quiet stance in children with cerebral palsy with their eyes open and closed. White bars represent the control-no stimulation-condition and the black bars the optimal SR stimulation condition. Error bars represent standard errors, * p < 0.05, ** p < 0.01
Fig. 3
Fig. 3
(a) SR sensory threshold and SR optimal intensity mean values for CP and TD groups. Black bars represent the SR sensory threshold and gray bars the SR optimal stimulation intensity. Error bars represent standard errors. Independent samples t-tests did not reveal significant differences between the two groups. (b) Scatter plot of the SR optimal intensity level and the difference between the COPVr of the optimal SR intensity over the no stimulation condition. Each black data point reflects a child with CP and each white data point reflect a child with TD. The black line is crossing y-axis at 0 and represents no change in the COPVr data following the application of SR stimulation. Data points falling above the black line suggest diminished postural sway, whereas those below the line suggest improved postural sway
Fig. 4
Fig. 4
Representative data from a child with CP (a) and a TD individual (b), showing center of pressure stabilograms during quiet stance with their eyes open. Two experimental condition are shown for: control-no stimulation-condition (solid line), and SR Optimal Stimulation condition (dotted line). In the optimal SR stimulation condition the 95% confidence ellipse area of the COP sway was decreased by 16.53mm2 for the child with CP and by 0.91mm2 for the TD child compared to the no stimulation condition

References

    1. Shumway-Cook A, Woollacott MH. Motor control: translating research into clinical practice. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2012.
    1. Kurz MJ, Becker KM, Heinrichs-Graham E, Wilson TW. Neurophysiological abnormalities in the sensorimotor cortices during the motor planning and movement execution stages of children with cerebral palsy. Dev Med Child Neurol. 2014;56:1072–1077. doi: 10.1111/dmcn.12513.
    1. Jacobs JV, Horak FB. Cortical control of postural responses. J Neural Transm. 2007;114:1339–1348. doi: 10.1007/s00702-007-0657-0.
    1. Bleyenheuft Y, Gordon AM. Precision grip control, sensory impairments and their interactions in children with hemiplegic cerebral palsy: a systematic review. Res Dev Disabil. 2013;34:3014–3028. doi: 10.1016/j.ridd.2013.05.047.
    1. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, et al. A report: the definition and classification of cerebral palsy. Dev Med Child Neurol Suppl. 2007;109 April:8–14.
    1. Day SM, Wu YW, Strauss DJ, Shavelle RM, Reynolds RJ. Change in ambulatory ability of adolescents and young adults with cerebral palsy. Dev Med Child Neurol. 2007;49:647–653. doi: 10.1111/j.1469-8749.2007.00647.x.
    1. Pavão SL, Nunes GS, Santos AN, Rocha NACF. Relationship between static postural control and the level of functional abilities in children with cerebral palsy. Brazilian J Phys Ther. 2014;18:300–307. doi: 10.1590/bjpt-rbf.2014.0056.
    1. Donker SF, Ledebt A, Roerdink M, Savelsbergh GJ, Beek PJ. Children with cerebral palsy exhibit greater and more regular postural sway than typically developing children. Exp Brain Res. 2008;184:363–370. doi: 10.1007/s00221-007-1105-y.
    1. Liao H, Hwang A. Relations of Balance Function and Gross Motor. 2003;:1173–1184.
    1. Jeffries L, Fiss A, McCoy SW, Bartlett DJ. Description of primary and secondary impairments in young children with cerebral palsy. Pediatr Phys Ther. 2016;28:7–14. doi: 10.1097/PEP.0000000000000221.
    1. Nashner LM, Shumway-Cook A, Marin O. Stance posture control in select groups of children with cerebral palsy: deficits in sensory organization and muscular coordination. Exp Brain Res. 1983;49:393–409. doi: 10.1007/BF00238781.
    1. Burtner PA, Qualls C, Woollacott MH. Muscle activation characteristics of stance balance control in children with spastic cerebral palsy. Gait Posture. 1998;8:163–174. doi: 10.1016/S0966-6362(98)00032-0.
    1. Auld ML, Boyd R, Moseley GL, Ware R, Johnston LM. Tactile function in children with unilateral cerebral palsy compared to typically developing children. Disabil Rehabil. 2012;34:1488–1494. doi: 10.3109/09638288.2011.650314.
    1. Auld ML, Boyd RN, Moseley GL, Ware RS, Johnston LM. Impact of tactile dysfunction on upper-limb motor performance in children with unilateral cerebral palsy. Arch Phys Med Rehabil. 2012;93:696–702. doi: 10.1016/j.apmr.2011.10.025.
    1. Auld ML, Ware RS, Boyd RN, Moseley GL, Johnston LM. Reproducibility of tactile assessments for children with unilateral cerebral palsy. Phys Occup Ther Pediatr. 2012;32:151–166. doi: 10.3109/01942638.2011.652804.
    1. Wingert JR, Burton H, Sinclair RJ, Brunstrom JE, Damiano DL. Tactile sensory abilities in cerebral palsy: deficits in roughness and object discrimination. Dev Med Child Neurol. 2008;50:832–838. doi: 10.1111/j.1469-8749.2008.03105.x.
    1. Wingert JR, Burton H, Sinclair RJ, Brunstrom JE, Damiano DL. Joint-position sense and kinesthesia in cerebral palsy. Arch Phys Med Rehabil. 2009;90:447–453. doi: 10.1016/j.apmr.2008.08.217.
    1. McLaughlin JF, Felix SD, Nowbar S, Ferrel A, Bjornson K, Hays RM. Lower extremity sensory function in children with cerebral palsy. Pediatr Rehabil. 2005;8:45–52. doi: 10.1080/13638490400011181.
    1. Pavão, S. L., Silva, F. P. d. S., Savelsbergh, G. J. P., & Rocha NACF. Use of sensory information during postural control in children with cerebral palsy_Systematic review. J Mot Behav 2015;47:291–011.
    1. Hoon AH, Jr, Stashinko EE, Nagae LM, Lin DD, Keller J, Bastian A, et al. Sensory and motor deficits in children with cerebral palsy born preterm correlate with diffusion tensor imaging abnormalities in thalamocortical pathways. Dev Med Child Neurol. 2009;51:697–704. doi: 10.1111/j.1469-8749.2009.03306.x.
    1. Papadelis C, Ahtam B, Nazarova M, Nimec D, Snyder B, Grant PE, et al. Cortical somatosensory reorganization in children with spastic cerebral palsy: a multimodal neuroimaging study. Front Hum Neurosci. 2014;8 September:725.
    1. Kurz MJ, Heinrichs-Graham E, Arpin DJ, Becker KM, Wilson TW. Aberrant synchrony in the somatosensory cortices predicts motor performance errors in children with cerebral palsy. J Neurophysiol. 2014;111:573–579. doi: 10.1152/jn.00553.2013.
    1. Kurz MJ, Heinrichs-Graham E, Becker KM, Wilson TW. The magnitude of the somatosensory cortical activity is related to the mobility and strength impairments seen in children with cerebral palsy. J Neurophysiol. 2015;113:3143–3150. doi: 10.1152/jn.00602.2014.
    1. Burton H, Dixit S, Litkowski P, Wingert JR. Functional connectivity for somatosensory and motor cortex in spastic diplegia. Somatosens Mot Res. 2009;26:90–104. doi: 10.3109/08990220903335742.
    1. Zarkou A. Somatosensory deficits affect balance and motor function in children with cerebral palsy: stochastic resonance stimulation can modulate Somatosensation to enhance balance: University of Delware; 2017.
    1. Damiano DL, Wingert JR, Stanley CJ, Curatalo L. Contribution of hip joint proprioception to static and dynamic balance in cerebral palsy: a case control study. J Neuroeng Rehabil. 2013;10:57. doi: 10.1186/1743-0003-10-57.
    1. Dewar R, Love S, Johnston LM. Exercise interventions improve postural control in children with cerebral palsy: a systematic review. Dev Med Child Neurol. 2015;57:504–520. doi: 10.1111/dmcn.12660.
    1. Lee C-W, Kim SG, Na SS. The effects of hippotherapy and a horse riding simulator on the balance of children with cerebral palsy. J Phys Ther Sci. 2014;26:423–425. doi: 10.1589/jpts.26.423.
    1. Kurz MJ, Wilson TW. Neuromagnetic activity in the somatosensory cortices of children with cerebral palsy. Neurosci Lett. 2011;490:1–5. doi: 10.1016/j.neulet.2010.11.053.
    1. Kurz MJ, Becker KM, Heinrichs-Graham E, Wilson TW. Children with cerebral palsy have uncharacteristic somatosensory cortical oscillations after stimulation of the hand mechanoreceptors. Neuroscience. 2015;305:67–75. doi: 10.1016/j.neuroscience.2015.07.072.
    1. Trivedi R, Gupta RK, Shah V, Tripathi M, Rathore RKS, Kumar M, et al. Treatment-induced plasticity in cerebral palsy: a diffusion tensor imaging study. Pediatr Neurol. 2008;39:341–349. doi: 10.1016/j.pediatrneurol.2008.07.012.
    1. Riquelme I, Zamorano A, Montoya P. Reduction of pain sensitivity after somatosensory therapy in adults with cerebral palsy. Front Hum Neurosci. 2013;7 June:276.
    1. Hänggi P. Stochastic resonance in biology. How noise can enhance detection of weak signals and help improve biological information processing. ChemPhysChem. 2002;3:285–290. doi: 10.1002/1439-7641(20020315)3:3<285::AID-CPHC285>;2-A.
    1. Moss F, Ward LM, Sannita WG. Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol. 2004;115:267–281. doi: 10.1016/j.clinph.2003.09.014.
    1. Sasaki H, Sakane S, Ishida T, Todorokihara M, Kitamura T, Aoki R. Subthreshold noise facilitates the detection and discrimination of visual signals. Neurosci Lett. 2008;436:255–258. doi: 10.1016/j.neulet.2008.03.036.
    1. Aihara T, Kitajo K, Nozaki D, Yamamoto Y. How does stochastic resonance work within the human brain? - psychophysics of internal and external noise. Chem Phys. 2010;375:616–624. doi: 10.1016/j.chemphys.2010.04.027.
    1. Iliopoulos F, Nierhaus T, Villringer A. Electrical noise modulates perception of electrical pulses in humans: sensation enhancement via stochastic resonance. J Neurophysiol. 2014;111:1238–1248. doi: 10.1152/jn.00392.2013.
    1. Méndez-Balbuena I, Huidobro N, Silva M, Flores A, Trenado C, Quintanar L, et al. Effect of mechanical tactile noise on amplitude of visual evoked potentials: multisensory stochastic resonance. J Neurophysiol. 2015;114:2132–2143. doi: 10.1152/jn.00457.2015.
    1. Lugo E, Doti R, Faubert J. Ubiquitous crossmodal stochastic resonance in humans: auditory noise facilitates tactile, visual and proprioceptive sensations. PLoS One. 2008;3:e2860. doi: 10.1371/journal.pone.0002860.
    1. Manjarrez E, Mendez I, Martinez L, Flores A, Mirasso CR. Effects of auditory noise on the psychophysical detection of visual signals: cross-modal stochastic resonance. Neurosci Lett. 2007;415:231–236. doi: 10.1016/j.neulet.2007.01.030.
    1. Collins JJ, Priplata a a, Gravelle DC, Niemi J, Harry J, Lipsitz L a Noise-enhanced human sensorimotor function IEEE Eng Med Biol Mag 2003;22:76–83.
    1. Magalhães FH, André ·, Kohn F, Magalhães FH, Kohn AF Imperceptible electrical noise attenuates isometric plantar flexion force fluctuations with correlated reductions in postural sway Exp Brain Res 2012;217:175–186.
    1. Magalhães FH, Kohn AF. Effectiveness of electrical noise in reducing postural sway: a comparison between imperceptible stimulation applied to the anterior and to the posterior leg muscles. Eur J Appl Physiol. 2014;114:1129–1141. doi: 10.1007/s00421-014-2846-5.
    1. Richardson KA, Imhoff TT, Grigg P, Collins JJ. Using electrical noise to enhance the ability of humans to detect subthreshold mechanical cutaneous stimuli. Chaos an Interdiscip. J Nonlinear Sci. 1998;8:599.
    1. Mulavara AP, Fiedler MJ, Kofman IS, Wood SJ, Serrador JM, Peters B, et al. Improving balance function using vestibular stochastic resonance: optimizing stimulus characteristics. Exp brain Res HirnforschungExperimentation cerebrale. 2011;210:303–312. doi: 10.1007/s00221-011-2633-z.
    1. Lipsitz LA, Lough M, Niemi J, Travison T, Howlett H, Manor B. A shoe insole delivering subsensory vibratory noise improves balance and gait in healthy elderly people. Arch Phys Med Rehabil. 2015;96:432–439. doi: 10.1016/j.apmr.2014.10.004.
    1. Ross SE. Noise-enhanced postural stability in subjects with functional ankle instability. Br J Sports Med. 2007;41:656–659. doi: 10.1136/bjsm.2006.032912.
    1. Ross SE, Guskiewicz KM. Effect of coordination training with and without stochastic resonance stimulation on dynamic postural stability of subjects with functional ankle instability and subjects with stable ankles. Clin J Sport Med. 2006;16:323–328. doi: 10.1097/00042752-200607000-00007.
    1. Collins AT, Blackburn JT, Olcott CW, Dirschl DR, Weinhold PS. The effects of stochastic resonance electrical stimulation and neoprene sleeve on knee proprioception. J Orthop Surg Res. 2009;4:3. doi: 10.1186/1749-799X-4-3.
    1. Priplata A a, Patritti BL, Niemi JB, Hughes R, Gravelle DC, Lipsitz L a, et al. Noise-enhanced balance control in patients with diabetes and patients with stroke. Ann Neurol. 2006;59:4–12. doi: 10.1002/ana.20670.
    1. Goel R, Kofman I, Jeevarajan J, De Dios Y, Cohen HS, Bloomberg JJ, et al. Using low levels of stochastic vestibular stimulation to improve balance function. PLoS One. 2015;10:1–24.
    1. Ross SE, Arnold BL. Postural stability benefits from training with stochastic resonance stimulation in stable and unstable ankles. Athl Train Sport Heal Care. 2012;4:207. doi: 10.3928/01484834-20120731-03.
    1. Kyvelidou A, Harbourne RT, Haworth J, Schmid KK, Stergiou N. Children with moderate to severe cerebral palsy may not benefit from stochastic vibration when developing independent sitting. Dev Neurorehabil. 2017;00:1–9. doi: 10.1080/17518423.2017.1290705.
    1. Ross SE, Linens SW, Wright CJ, Arnold BL. Customized noise-stimulation intensity for bipedal stability and unipedal balance deficits associated with functional ankle instability. J Athl Train. 2013;48:463–470. doi: 10.4085/1062-6050-48.3.12.
    1. Moss F. Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol. 2004;115:267–281. doi: 10.1016/j.clinph.2003.09.014.
    1. Collins A, Blackburn JT, Olcott C, Yu B, Weinhold P. The impact of stochastic resonance electrical stimulation and knee sleeve on impulsive loading and muscle co-contraction during gait in knee osteoarthritis. Clin Biomech. 2011;26:853–858. doi: 10.1016/j.clinbiomech.2011.04.011.
    1. Reeves NP, Cholewicki J, Lee AS, Mysliwiec LW. The effects of stochastic resonance stimulation on spine proprioception and postural control in chronic low back pain patients. Spine. 2009;34:316–321. doi: 10.1097/BRS.0b013e3181971e09.
    1. Severini G, Delahunt E. Effect of noise stimulation below and above sensory threshold on postural sway during a mildly challenging balance task. Gait Posture. 2018;63:27–32. doi: 10.1016/j.gaitpost.2018.04.031.
    1. Hwang S, Agada P, Kiemel T, Jeka JJ. Dynamic reweighting of three modalities for sensor fusion. PLoS One. 2014;9:1–8.
    1. Sozzi S, Do MC, Monti A, Schieppati M. Sensorimotor integration during stance: processing time of active or passive addition or withdrawal of visual or haptic information. Neuroscience. 2012;212:59–76. doi: 10.1016/j.neuroscience.2012.03.044.
    1. Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng. 1996;43:956–966. doi: 10.1109/10.532130.
    1. Ghofrani M, Olyaei G, Talebian S, Bagheri H, Malmir K. Test-retest reliability of linear and nonlinear measures of postural stability during visual deprivation in healthy subjects. J Phys Ther Sci. 2017;29:1766–1771. doi: 10.1589/jpts.29.1766.
    1. Lafond D, Corriveau H, Hébert R, Prince F. Intrasession reliability of center of pressure measures of postural steadiness in healthy elderly people. Arch Phys Med Rehabil. 2004;85:896–901. doi: 10.1016/j.apmr.2003.08.089.
    1. Caballero C, Barbado D, Moreno FJ. What COP and kinematic parameters better characterize postural control in standing balance tasks? J Mot Behav. 2015;47:550–562. doi: 10.1080/00222895.2015.1014545.
    1. John J, Kiemel T, Robert C, Fay H, Robert P. Controlling human upright posture: velocity information is more accurate than position or acceleration. J Neurophysiol. 2004;92:2368–2379. doi: 10.1152/jn.00983.2003.
    1. Gravelle DC, Laughton CA, Dhruv NT, Katdare KD, Niemi JB, Lipsitz LA, et al. Noise-enhanced balance control in older adults. Neuroreport. 2002;13:1853–1856. doi: 10.1097/00001756-200210280-00004.
    1. Fitzpatrick R, Rogers DK, Mccloskey DI. Stable human standing with lower-limb muscle afferents providing the only sensory input. J Physiol. 1994;480:395–403. doi: 10.1113/jphysiol.1994.sp020369.
    1. Rose J, Wolff DR, Jones VK, Bloch DA, Oehlert JW, Gamble JG. Postural balance in children with cerebral palsy. Dev Med Child Neurol. 2007;44:58–63. doi: 10.1111/j.1469-8749.2002.tb00260.x.
    1. Trenado C, Mendez-Balbuena I, Manjarrez E, Huethe F, Schulte-Mönting J, Feige B, et al. Enhanced corticomuscular coherence by external stochastic noise. Front Hum Neurosci. 2014;8:325.
    1. Trenado C, Mikulić A, Manjarrez E, Mendez-Balbuena I, Schulte-Mönting J, Huethe F, et al. Broad-band Gaussian noise is most effective in improving motor performance and is most pleasant. Front Hum Neurosci. 2014;8 February:22.
    1. Faisal AA, Selen LPJ, Wolpert DM. Noise in the nervous system. Nat Rev Neurosci. 2008;9:292–303. doi: 10.1038/nrn2258.
    1. Zimmer M, Desch L. Disabilities C on C with, medicine SOCAI, Pediatrics AA of Sensory integration therapies for children with developmental and behavioral disorders. Pediatrics. 2012;129:1186. doi: 10.1542/peds.2012-0876.
    1. Field-Fote EC. Exciting recovery: augmenting practice with stimulation to optimize outcomes after spinal cord injury. Sensorimotor Rehabil Crossroads Basic Clin Sci. 2015;218:103–126.

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