Using Low Levels of Stochastic Vestibular Stimulation to Improve Balance Function

RESEARCH ARTICLE Using Low Levels of Stochastic Vestibular Stimulation to Improve Balance Function Rahul Goel1, Igor Kofman2, Jerome Jeevarajan3, Yiri De Dios2, Helen S. Cohen4, Jacob J. Bloomberg3, Ajitkumar P. Mulavara5* 1 Department of Health and Human Performance, University of Houston, Houston, Texas, United States of America, 2 Wyle Science, Technology and Engineering Group, Houston, Texas, United States of America, 3 Neuroscience Laboratory, NASA Johnson Space Center, Houston, Texas, United States of America, 4 Department of Otolaryngology–Head and Neck Surgery, Baylor College of Medicine, Houston, Texas, United States of America, 5 Universities Space Research Association, Houston, Texas, United States of America * Abstract OPEN ACCESS Citation: Goel R, Kofman I, Jeevarajan J, De Dios Y, Cohen HS, Bloomberg JJ, et al. (2015) Using Low Levels of Stochastic Vestibular Stimulation to Improve Balance Function. PLoS ONE 10(8): e0136335. doi:10.1371/journal.pone.0136335 Editor: Maurice J. Chacron, McGill University, CANADA Received: March 19, 2015 Accepted: August 2, 2015 Published: August 21, 2015 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This study was supported in part by a grant from the National Space Biomedical Research Institute through NASA NCC 9–58—SA 02801 to Jacob Bloomberg, NASA NCC 9–58—SA 02001 to Ajitkumar Mulavara and by a grant from the National Institute of Health through RO1-DC009031 to Helen Cohen. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Wyle Science, Technology and Engineering Group provided support in the form of salaries for authors IK and YD but did Low-level stochastic vestibular stimulation (SVS) has been associated with improved postural responses in the medio-lateral (ML) direction, but its effect in improving balance function in both the ML and anterior-posterior (AP) directions has not been studied. In this series of studies, the efficacy of applying low amplitude SVS in 0–30 Hz range between the mastoids in the ML direction on improving cross-planar balance function was investigated. Forty-five (45) subjects stood on a compliant surface with their eyes closed and were instructed to maintain a stable upright stance. Measures of stability of the head, trunk, and whole body were quantified in ML, AP and combined APML directions. Results show that binaural bipolar SVS given in the ML direction significantly improved balance performance with the peak of optimal stimulus amplitude predominantly in the range of 100–500 μA for all the three directions, exhibiting stochastic resonance (SR) phenomenon. Objective perceptual and body motion thresholds as estimates of internal noise while subjects sat on a chair with their eyes closed and were given 1 Hz bipolar binaural sinusoidal electrical stimuli were also measured. In general, there was no significant difference between estimates of perceptual and body motion thresholds. The average optimal SVS amplitude that improved balance performance (peak SVS amplitude normalized to perceptual threshold) was estimated to be 46% in ML, 53% in AP, and 50% in APML directions. A miniature patch-type SVS device may be useful to improve balance function in people with disabilities due to aging, Parkinson’s disease or in astronauts returning from long-duration space flight. Introduction Stochastic resonance (SR) is a phenomenon based on the concept of maximizing the flow of information through a non-linear system by the presence of non-zero level of noise [1–3]. Stochastic resonance has been shown to improve function in a variety of human physiological PLOS ONE | DOI:10.1371/journal.pone.0136335 August 21, 2015 1 / 24 Improving Balance with Low Levels of Stochastic Vestibular Stimulation not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. Competing Interests: The authors acknowledge that one or more of the authors are employed by a commercial company, Wyle Science, Technology and Engineering Group and this does not alter their adherence to PLOS ONE policies on sharing data and materials. systems including motor, cardiovascular, visual, hearing, and balance function. Stochastic electrical stimulation of the vestibular system (stochastic vestibular stimulation, SVS), using SR principles, has been shown to improve heart rate responsiveness in healthy subjects [4], visual processing in healthy [5] as well as stroke patients [6, 7], cardiac and motor function in patients with central neurodegenerative disorders [8], and postural responses in patients with Parkinson’s disease (PD) [9, 10]. Over the past century the transcutaneous delivery of electric currents to the vestibular afferents commonly referred to as galvanic vestibular stimulation (GVS) has been used to study and understand the function of the vestibular system (for review see [11]). Bilateral bipolar vestibular electrical stimulation applied across the mastoid bones with a constant current profile has generally been shown to induce plane-specific body sway in the medio-lateral (ML) or anterior-posterior (AP) direction depending on if subject’s head is facing forward or if it is turned to the side (i.e., over the left or right shoulder), respectively [12, 13]. However, in contrast, stochastic vestibular stimulation (SVS) has been used to examine disruption of control of nominal body responses in posture, balance, and gait to unpredictable vestibular perturbations [12, 14, 15]. Studies have shown that using 3–5 mA peak binaural bipolar current levels of modified sum-of-sine’s current profile across the mastoid processes in the ML direction disrupted balance function in both ML and AP directions [16]. In our previous work, the application of low levels of bipolar SVS with peak currents in 100 to 400 μA range between the mastoids, on healthy subjects, while standing on an unstable surface, resulted in significant improvement of balance performance in the ML direction [17]. Other studies have investigated the potential of low levels of SVS to improve balance control in PD patients in both ML and AP directions. Pal’s study [9] found reduction of sway in the AP direction when SVS was applied to patients with PD during a balance task. In that study, the cathode was placed on both the mastoids and the anode was placed on the C7 vertebra, in a ‘bicathodal’ configuration, delivering stimulation to the vestibular end organs in the AP direction on both sides (...truncated)