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

BackgroundStochastic 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.MethodsTen 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.ResultsFor 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.ConclusionsSR 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 registrationClinicalTrials.gov identifier NCT02456376; 28 May 2015 (Retrospectively registered); https://clinicaltrials.gov/ct2/show/NCT02456376.

[1]  J. Collins,et al.  Noise-enhanced human sensorimotor function , 2003, IEEE Engineering in Medicine and Biology Magazine.

[2]  L. M. Nashner,et al.  Stance posture control in select groups of children with cerebral palsy: Deficits in sensory organization and muscular coordination , 2004, Experimental Brain Research.

[3]  Tim Kiemel,et al.  Controlling human upright posture: velocity information is more accurate than position or acceleration. , 2004, Journal of neurophysiology.

[4]  B. Dan,et al.  A report: the definition and classification of cerebral palsy April 2006 , 2007, Developmental medicine and child neurology. Supplement.

[5]  Rahul Goel,et al.  Using Low Levels of Stochastic Vestibular Stimulation to Improve Balance Function , 2015, PloS one.

[6]  P. Weinhold,et al.  The impact of stochastic resonance electrical stimulation and knee sleeve on impulsive loading and muscle co-contraction during gait in knee osteoarthritis. , 2011, Clinical biomechanics.

[7]  A. Villringer,et al.  Electrical noise modulates perception of electrical pulses in humans: sensation enhancement via stochastic resonance. , 2014, Journal of neurophysiology.

[8]  R. Ware,et al.  Impact of tactile dysfunction on upper-limb motor performance in children with unilateral cerebral palsy. , 2012, Archives of physical medicine and rehabilitation.

[9]  R. Ware,et al.  Tactile function in children with unilateral cerebral palsy compared to typically developing children , 2012, Disability and rehabilitation.

[10]  Qualls,et al.  Muscle activation characteristics of stance balance control in children with spastic cerebral palsy. , 1998, Gait & posture.

[11]  Yoshio Okada,et al.  Cortical Somatosensory Reorganization in Children with Spastic Cerebral Palsy: A Multimodal Neuroimaging Study , 2014, Front. Hum. Neurosci..

[12]  Scott E. Ross,et al.  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 , 2006, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[13]  G. Savelsbergh,et al.  Use of Sensory Information During Postural Control in Children With Cerebral Palsy: Systematic Review , 2015, Journal of motor behavior.

[14]  J. Rose,et al.  Postural balance in children with cerebral palsy , 2002 .

[15]  Contribution of hip joint proprioception to static and dynamic balance in cerebral palsy: a case control study , 2013, Journal of NeuroEngineering and Rehabilitation.

[16]  Brad Manor,et al.  A shoe insole delivering subsensory vibratory noise improves balance and gait in healthy elderly people. , 2015, Archives of physical medicine and rehabilitation.

[17]  N. A. Rocha,et al.  Relationship between static postural control and the level of functional abilities in children with cerebral palsy , 2014, Brazilian journal of physical therapy.

[18]  D. Nozaki,et al.  How does stochastic resonance work within the human brain? – Psychophysics of internal and external noise , 2010 .

[19]  Carla Caballero,et al.  What COP and Kinematic Parameters Better Characterize Postural Control in Standing Balance Tasks? , 2015, Journal of motor behavior.

[20]  Katherine M. Becker,et al.  Children with cerebral palsy have uncharacteristic somatosensory cortical oscillations after stimulation of the hand mechanoreceptors , 2015, Neuroscience.

[21]  André Fabio Kohn,et al.  Imperceptible electrical noise attenuates isometric plantar flexion force fluctuations with correlated reductions in postural sway , 2011, Experimental Brain Research.

[22]  H. Liao,et al.  Relations of Balance Function and Gross Motor Ability for Children with Cerebral Palsy , 2003, Perceptual and motor skills.

[23]  Cynthia J Wright,et al.  Customized noise-stimulation intensity for bipedal stability and unipedal balance deficits associated with functional ankle instability. , 2013, Journal of athletic training.

[24]  A. Faisal,et al.  Noise in the nervous system , 2008, Nature Reviews Neuroscience.

[25]  M. Ghofrani,et al.  Test-retest reliability of linear and nonlinear measures of postural stability during visual deprivation in healthy subjects , 2017, Journal of physical therapy science.

[26]  André Fabio Kohn,et al.  Effectiveness of electrical noise in reducing postural sway: a comparison between imperceptible stimulation applied to the anterior and to the posterior leg muscles , 2014, European Journal of Applied Physiology.

[27]  Peter Hänggi,et al.  Stochastic resonance in biology. How noise can enhance detection of weak signals and help improve biological information processing. , 2002, Chemphyschem : a European journal of chemical physics and physical chemistry.

[28]  J. Collins,et al.  Noise-enhanced balance control in older adults , 2002, Neuroreport.

[29]  Katherine M. Becker,et al.  The magnitude of the somatosensory cortical activity is related to the mobility and strength impairments seen in children with cerebral palsy. , 2015, Journal of neurophysiology.

[30]  L. Johnston,et al.  Exercise interventions improve postural control in children with cerebral palsy: a systematic review , 2015, Developmental medicine and child neurology.

[31]  S. Mccoy,et al.  Description of Primary and Secondary Impairments in Young Children With Cerebral Palsy , 2016, Pediatric physical therapy : the official publication of the Section on Pediatrics of the American Physical Therapy Association.

[32]  H. Sasaki,et al.  Subthreshold noise facilitates the detection and discrimination of visual signals , 2008, Neuroscience Letters.

[33]  Frank Huethe,et al.  Broad-band Gaussian noise is most effective in improving motor performance and is most pleasant , 2014, Front. Hum. Neurosci..

[34]  M. Schieppati,et al.  Sensorimotor integration during stance: Processing time of active or passive addition or withdrawal of visual or haptic information , 2012, Neuroscience.

[35]  Daniel A Bloch,et al.  Postural balance in children with cerebral palsy. , 2002, Developmental medicine and child neurology.

[36]  S. E. Ross,et al.  Postural Stability Benefits From Training With Stochastic Resonance Stimulation in Stable and Unstable Ankles , 2012 .

[37]  Max J Kurz,et al.  Neurophysiological abnormalities in the sensorimotor cortices during the motor planning and movement execution stages of children with cerebral palsy , 2014, Developmental medicine and child neurology.

[38]  Yan Peng,et al.  Scorpion Venom Heat-Resistant Peptide (SVHRP) Enhances Neurogenesis and Neurite Outgrowth of Immature Neurons in Adult Mice by Up-Regulating Brain-Derived Neurotrophic Factor (BDNF) , 2014, PloS one.

[39]  P. Weinhold,et al.  The effects of stochastic resonance electrical stimulation and neoprene sleeve on knee proprioception , 2009, Journal of orthopaedic surgery and research.

[40]  Sachin Dixit,et al.  Functional connectivity for somatosensory and motor cortex in spastic diplegia , 2009, Somatosensory & motor research.

[41]  Robert S Ware,et al.  Reproducibility of Tactile Assessments for Children with Unilateral Cerebral Palsy , 2012, Physical & occupational therapy in pediatrics.

[42]  Anna M. Zamorano,et al.  Reduction of Pain Sensitivity After Somatosensory Therapy in Adults with Cerebral Palsy , 2013, Front. Hum. Neurosci..

[43]  M. Woollacott,et al.  Comprar Motor Control. Translating Research Into Clinical Practice (International Edition) 5th Ed. | Anne Shumway-Cook | 9781496347725 | Lippincott Williams & Wilkins , 2016 .

[44]  Rafael Doti,et al.  Ubiquitous Crossmodal Stochastic Resonance in Humans: Auditory Noise Facilitates Tactile, Visual and Proprioceptive Sensations , 2008, PloS one.

[45]  Joshua L. Haworth,et al.  Children with moderate to severe cerebral palsy may not benefit from stochastic vibration when developing independent sitting , 2017, Developmental neurorehabilitation.

[46]  O. Arias-Carrión,et al.  Effect of mechanical tactile noise on amplitude of visual evoked potentials: multisensory stochastic resonance. , 2015, Journal of neurophysiology.

[47]  Peter Agada,et al.  Dynamic Reweighting of Three Modalities for Sensor Fusion , 2014, PloS one.

[48]  F. Prince,et al.  Intrasession reliability of center of pressure measures of postural steadiness in healthy elderly people. , 2004, Archives of physical medicine and rehabilitation.

[49]  E. Delahunt,et al.  Effect of noise stimulation below and above sensory threshold on postural sway during a mildly challenging balance task. , 2018, Gait & posture.

[50]  T.E. Prieto,et al.  Measures of postural steadiness: differences between healthy young and elderly adults , 1996, IEEE Transactions on Biomedical Engineering.

[51]  A. Bastian,et al.  Sensory and motor deficits in children with cerebral palsy born preterm correlate with diffusion tensor imaging abnormalities in thalamocortical pathways , 2009, Developmental medicine and child neurology.

[52]  Jacek Cholewicki,et al.  The Effects of Stochastic Resonance Stimulation on Spine Proprioception and Postural Control in Chronic Low Back Pain Patients , 2009, Spine.

[53]  L. Desch,et al.  Sensory integration therapies for children with developmental and behavioral disorders. , 2013, Pediatrics.

[54]  Frank Huethe,et al.  Enhanced corticomuscular coherence by external stochastic noise , 2014, Front. Hum. Neurosci..

[55]  Yvonne W Wu,et al.  Change in ambulatory ability of adolescents and young adults with cerebral palsy , 2007, Developmental medicine and child neurology.

[56]  Paolo Bonato,et al.  Noise‐enhanced balance control in patients with diabetes and patients with stroke , 2006, Annals of neurology.

[57]  Jorge M. Serrador,et al.  Improving balance function using vestibular stochastic resonance: optimizing stimulus characteristics , 2011, Experimental Brain Research.

[58]  A. Zarkou Somatosensory deficits affect balance and motor function in children with cerebral palsy: stochastic resonance stimulation can modulate somatosensation to enhance balance , 2017 .

[59]  L. M. Ward,et al.  Stochastic resonance and sensory information processing: a tutorial and review of application , 2004, Clinical Neurophysiology.

[60]  Diane L Damiano,et al.  Tactile sensory abilities in cerebral palsy: deficits in roughness and object discrimination , 2008, Developmental medicine and child neurology.

[61]  E. Field-Fote Exciting recovery: augmenting practice with stimulation to optimize outcomes after spinal cord injury. , 2015, Progress in brain research.

[62]  Chae-Woo Lee,et al.  The Effects of Hippotherapy and a Horse Riding Simulator on the Balance of Children with Cerebral Palsy , 2014, Journal of physical therapy science.

[63]  Thomas T. Imhoff,et al.  Using electrical noise to enhance the ability of humans to detect subthreshold mechanical cutaneous stimuli. , 1998, Chaos.

[64]  K. Bjornson,et al.  Lower extremity sensory function in children with cerebral palsy , 2005, Pediatric rehabilitation.

[65]  R. Fitzpatrick,et al.  Stable human standing with lower‐limb muscle afferents providing the only sensory input. , 1994, The Journal of physiology.

[66]  M. Woollacott,et al.  Motor Control: Translating Research into Clinical Practice , 2006 .

[67]  Katherine M. Becker,et al.  Aberrant synchrony in the somatosensory cortices predicts motor performance errors in children with cerebral palsy. , 2014, Journal of neurophysiology.

[68]  P. Beek,et al.  Children with cerebral palsy exhibit greater and more regular postural sway than typically developing children , 2007, Experimental Brain Research.

[69]  Scott E Ross,et al.  Noise-enhanced postural stability in subjects with functional ankle instability , 2007, British Journal of Sports Medicine.

[70]  A. Gordon,et al.  Precision grip control, sensory impairments and their interactions in children with hemiplegic cerebral palsy: a systematic review. , 2013, Research in developmental disabilities.

[71]  Diane L Damiano,et al.  Joint-position sense and kinesthesia in cerebral palsy. , 2009, Archives of physical medicine and rehabilitation.

[72]  Section On Complementary Sensory Integration Therapies for Children With Developmental and Behavioral Disorders , 2012, Pediatrics.

[73]  T. Wilson,et al.  Neuromagnetic activity in the somatosensory cortices of children with cerebral palsy , 2011, Neuroscience Letters.

[74]  F. Horak,et al.  Cortical control of postural responses , 2007, Journal of Neural Transmission.

[75]  M. Burns,et al.  Case-Control Study , 2020, Definitions.

[76]  Claudio R. Mirasso,et al.  Effects of auditory noise on the psychophysical detection of visual signals: Cross-modal stochastic resonance , 2007, Neuroscience Letters.

[77]  Lorna M. Lopez,et al.  Modulation of Genetic Associations with Serum Urate Levels by Body-Mass-Index in Humans , 2015, PloS one.

[78]  M. Kumar,et al.  Treatment-induced plasticity in cerebral palsy: a diffusion tensor imaging study. , 2008, Pediatric neurology.