Older adults with a history of falling exhibit altered cortical oscillatory mechanisms during continuous postural maintenance

Background and aim: The significant risk of falling in older adults 65 years or older presents a substantial problem for these individuals, their caretakers, and the healthcare system at large. As the proportion of older adults in the United States is only expected to grow over the next few decades, a better understanding of physiological and cortical changes that make an older adult more susceptible to a fall is crucial. Prior studies have displayed differences in postural dynamics and stability in older adults with a fall history (FH) and those that have never fallen (NF), suggesting surplus alterations that occur in some older adults (i.e. FH group) in addition to the natural aging process.
Methods: The present study measured postural dynamics while FH, NF and young adult (YA) groups performed continuous postural maintenance. In addition, EEG activity was recorded while participants performed upright postural stance to examine any group differences in cortical areas involved in postural control.
Results: As expected, older participants (FH and NF) exhibited worse postural stability, as evidenced by increased excursion, compared to the YA group. Further, while NF and YA show increased alpha activity in occipital areas during the most demanding postural task (eyes closed), FH group did not show any differences in occipital alpha power between postural tasks.
Conclusions: As alpha activity reflects suppression of bottom-up processing and thus diversion of cognitive resources toward postural centers during more demanding postural maintenance, deficits in this regulatory function in the FH group is a possible impaired cortical mechanism putting these individuals at greater fall risk.
Relevance for patients: Impaired inhibitory function in older adults may impact postural control and increase their risk of falling. Interventions that aim at addressing cortical processing deficits may improve postural stability and facilitate independent living in this population.
[1] Winter DA. Human Balance and Posture Control during Standing and Walking. Gait Posture 1995;3:193-214.
[2] Horak FB. Postural Orientation and Equilibrium: What do we need to Know about Neural Control of Balance to Prevent Falls? Age Ageing 2006;35:ii7-11.
[3] Marsden JF. Cerebellar Ataxia. Handb Clin Neurol 2018;159:261-81.
[4] Schlick C, Schniepp R, Loidl V, Wuehr M, Hesselbarth K, Jahn K. Falls and Fear of Falling in Vertigo and Balance Disorders: A Controlled Cross-Sectional Study. J Vestib Res 2015;25:241-51.
[5] Peel NM. Epidemiology of Falls in Older Age. Can J Aging 2011;30:7-19.
[6] Rubenstein LZ. Falls in Older People: Epidemiology, Risk Factors and Strategies for Prevention. Age Ageing 2006;35.
[7] Stevens JA, Mack KA, Paulozzi LJ, Ballesteros MF. Self-Reported Falls and Fall-Related Injuries among Persons Aged ≥65 Years-United States, 2006. J Saf Res 2008;39:345-9.
[8] Bergland A, Wyller TB. Risk Factors for Serious Fall Related Injury in Elderly Women Living at Home. Inj Prev 2004;10:308-13.
[9] Piirtola M, Era P. Force Platform Measurements as Predictors of Falls among Older People a Review. Gerontology 2006;52:1-16.
[10] Setti A, Burke KE, Kenny RA, Newell FN. Is Inefficient Multisensory Processing Associated with Falls in Older People? Exp Brain Res 2011;209:375-84.
[11] Merriman NA, Whyatt C, Setti A, Craig C, Newell FN. Successful Balance Training is Associated with Improved Multisensory Function in Fall-Prone Older Adults. Comput Hum Behav 2015;45:192-203.
[12] Stapleton J, Setti A, Doheny EP, Kenny RA, Newell FN. A Standing Posture is Associated with Increased Susceptibility to the Sound-Induced Flash Illusion in FallProne Older Adults. Exp Brain Res 2014;232:423-34.
[13] Klimesch W. Alpha-Band Oscillations, Attention, and Controlled Access to Stored Information. Trends Cogn Sci 2012;16:606-17.
[14] Ozdemir RA, Contreras-Vidal JL, Lee BC, Paloski WH. Cortical Activity Modulations Underlying Age-Related Performance Differences during Posture-Cognition Dual Tasking. Exp Brain Res 2016;234:3321-34.
[15] Chang CJ, Yang TF, Yang SW, Chern JS. Cortical Modulation of Motor Control Biofeedback among the Elderly with High Fall Risk during a Posture Perturbation Task with Augmented Reality. Front Aging Neurosci 2016;8:80.
[16] Slobounov S, Hallett M, Stanhope S, Shibasaki H. Role of Cerebral Cortex in Human Postural Control: An EEG Study. Clin Neurophysiol 2005;116:315-23.
[17] Fino PC, Mojdehi AR, Adjerid K, Habibi M, Lockhart TE, Ross SD. Comparing Postural Stability Entropy Analyses to Differentiate Fallers and Non-Fallers. Ann Biomed Eng 2016;44:1636-45.
[18] Gates S, Smith LA, Fisher JD, Lamb SE. Systematic Review of Accuracy of Screening Instruments for Predicting Fall Risk among Independently Living Older Adults. J Rehabil Res Dev 2008;45:1105-16.
[19] Howcroft J, Lemaire ED, Kofman J, McIlroy WE. Elderly Fall Risk Prediction Using Static Posturography. PLoS One 2017;12:e0172398.
[20] Kwan E, Straus SE. Assessment and Management of Falls in Older People. CMAJ 2014;186:E610-21.
[21] Paillard T, Noé F. Techniques and Methods for Testing the Postural Function in Healthy and Pathological Subjects. Biomed Res Int 2015;2015:891390.
[22] Baum SH, Stevenson RA. Shifts in Audiovisual Processing in Healthy Aging. Curr Behav Neurosci Rep 2017;4:198-208.
[23] Brooks CJ, Anderson AJ, Roach NW, McGraw PV, McKendrick AM. Age-Related Changes in Auditory and Visual Interactions in Temporal Rate Perception. J Vis 2015;15:2.
[24] Tinetti ME, Speechley M, Ginter SF. Risk Factors for Falls among Elderly Persons Living in the Community. N Eng J Med 1988;319:1701-7.
[25] Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool for Mild Cognitive Impairment. J Am Geriat Soc 2005;53:695-9.
[26] Brainard D. The Psychophysics Toolbox. Spat Vis 1997;10:433-6.
[27] Pelli D. The Video Toolbox Software for Visual Psychophysics: Transforming Numbers into Movies. Spat Vis 1997;10:437-42.
[28] Podsiadlo D, Richardson S. The Timed “Up and Go”: A Test of Basic Functional Mobility for Frail Elderly Persons. J Am Geriatr Soc 1991;39:142-8.
[29] Yardley L, Beyer N, Hauer K, Kempen G, Piot-Ziegler C, Todd C. Development and Initial Validation of the Falls Efficacy Scale-International (FES-I). Age Ageing 2005;34:614-9.
[30] Delgado DA, Lambert BS, Boutris N, McCulloch PC, Robbins AB, Moreno MR, et al. Validation of Digital Visual Analog Scale Pain Scoring with a Traditional PaperBased Visual Analog Scale in Adults. J Am Acad Orthop Surg Glob Res Rev 2018;2:e088.
[31] Senderecka M. Emotional Enhancement of Error Detection the Role of Perceptual Processing and Inhibition Monitoring in Failed Auditory Stop Trials. Cogn Affect Behav Neurosci 2018;18:1-20.
[32] Costa M, Goldberger AL, Peng CK. Multiscale Entropy Analysis of Biological Signals. Phys Rev E Stat Nonlin Soft Matter Phys 2005;71:021906.
[33] 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;43:956-66.
[34] Busa MA, van Emmerik REA. Multiscale Entropy: A Tool for Understanding the Complexity of Postural Control. J Sport Health Sci 2016;5:44-51.
[35] Rossion B, Jacques C, Liu-Shuang J. Fast Periodic Presentation of Natural Images Reveals a Robust FaceSelective Electrophysiological Response in the Human Brain. J Vis 2015;15:18.
[36] Yokoyama H, Kaneko N, Ogawa T, Kawashima N, Watanabe K, Nakazawa K. Cortical Correlates of Locomotor Muscle Synergy Activation in Humans: An Electroencephalographic Decoding Study. iScience 2019;15:623-39.
[37] Krebber M, Harwood J, Spitzer B, Keil J, Senkowski D. Visuotactile Motion Congruence Enhances GammaBand Activity in Visual and Somatosensory Cortices. Neuroimage 2015;117:160-9.
[38] Lange J, Oostenveld R, Fries P. Perception of the Touch-Induced Visual Double-Flash Illusion Correlates with Changes of Rhythmic Neuronal Activity in Human Visual and Somatosensory Areas. Neuroimage 2011;54:1395-405.
[39] Nowak M, Hinson E, van Ede F, Pogosyan A, Guerra A, Quinn A, et al. Driving Human Motor Cortical Oscillations Leads to Behaviorally Relevant Changes in Local GABAA Inhibition: A tACS-TMS Study. J Neurosci 2017;37:4481-92.
[40] Solis-Escalante T, van der Cruijsen J, de Kam D, van Kordelaar J, Weerdesteyn V, Schouten AC. Cortical Dynamics during Preparation and Execution of Reactive Balance Responses with Distinct Postural Demands. Neuroimage 2019;188:557-71.
[41] Scurry AN, Chifamba K, Jiang F. Electrophysiological Dynamics of Visual-Tactile Temporal Order Perception in Early Deaf Adults. Front Neurosci 2020;14:544472.
[42] Setti A, Finnigan S, Sobolewski R, McLaren L, Robertson IH, Reilly RB, et al. Audiovisual Temporal Discrimination is Less Efficient with aging: An EventRelated Potential Study. Neuroreport 2011;22:554-8.
[43] Pinherio JC, Bates DM, DebRoy S, Sarkar D. The R Core Teamnlme: Linear and Nonlinear Mixed Effects Models. Sci Res 2020;3:1-117.
[44] Harrell FE Jr. CRAN - Package Hmisc. 2020. Available from: https://cran.r-project.org/package=Hmisc
[45] Paliwal Y, Slattum PW, Ratliff SM. Chronic Health Conditions as a Risk Factor for Falls among the CommunityDwelling US Older Adults: A Zero-Inflated Regression Modeling Approach. Biomed Res Int 2017;2017:5146378.
[46] Vu T, Finch CF, Day L. Patterns of Comorbidity in Community-Dwelling Older People Hospitalised for Fall-Related Injury: A Cluster Analysis. BMC Geriat 2011;11:45.
[47] Scurry A, Vercillo T, Nicholson A, Webster M, Jiang F. Aging Impairs Temporal Sensitivity, but not Perceptual Synchrony, Across Modalities. Multisens Res 2019;32:671-92.
[48] Bedard G, Barnett-Cowan M. Impaired Timing of Audiovisual Events in the Elderly. Exp Brain Res 2016;234:331-40.
[49] Scurry AN, Dutcher D, Werner J, Jiang F. Age-Related Effects on Cross-Modal Duration Perception. Multisen Res 2019;32:693-714.
[50] Yeh TT, Cluff T, Balasubramaniam R. Visual Reliance for Balance Control in Older Adults Persists when Visual Information is Disrupted by Artificial Feedback Delays. PLoS One 2014;9:e91554.
[51] Kang HG, Costa MD, Priplata AA, Starobinets OV, Goldberger AL, Peng CK, et al. Frailty and the Degradation of Complex Balance Dynamics during a Dual-Task Protocol. J Gerontol Series A Biol Sci Med Sci 2009;64:1304-11.
[52] Malcolm BR, Foxe JJ, Butler JS, de Sanctis P. The Aging Brain Shows Less Flexible Reallocation of Cognitive Resources during Dual-Task Walking: AMobile Brain/Body Imaging (MoBI) Study. Neuroimage 2015;117:230-42.
[53] Manor B, Costa MD, Hu K, Newton E, Starobinets O, Kang HG, et al. Physiological Complexity and System Adaptability: Evidence from Postural Control Dynamics of Older Adults. J Appl Physiol 2010;109:1786-91.
[54] Lipsitz LA, Goldberger AL. Loss of “Complexity” and Aging Potential Applications of Fractals and Chaos Theory to Senescence. JAMA 1992;267:1806-9.
[55] Wayne PM, Gow BJ, Costa MD, Peng CK, Lipsitz LA, Hausdorff JM, et al. Complexity-Based Measures Inform Effects of Tai Chi Training on Standing Postural Control: Cross-Sectional and Randomized Trial Studies. PLoS One 2014;9:e114731.
[56] Bigelow KE, Berme N. Development of a Protocol for Improving the Clinical Utility of Posturography as a FallRisk Screening Tool. J Gerontol Series A Biol Sci Med Sci 2011;66:228-33.
[57] Horak FB, Dimitrova D, Nutt JG. Direction-Specific Postural Instability in Subjects with Parkinson’s Disease. Exp Neurol 2005;193:504-21.
[58] Jacobs JV, Wu G, Kelly KM. Evidence for Beta Corticomuscular Coherence during Human Standing Balance: Effects of Stance Width, Vision, and Support Surface. Neuroscience 2015;298:1-11.
[59] Bok SK, Lee TH, Lee SS. The Effects of Changes of Ankle Strength and Range of Motion According to Aging on Balance. Ann Rehabil Med 2013;37:10-6.
[60] Maki BE, McIlroy WE. C ognitive Demands and Cortical Control of Human Balance-Recovery Reactions. J Neural Trans 2007;114:1279-96.
[61] Bergland A, Jarnlo GB, Laake K. Predictors of Falls in the Elderly by Location. Aging Clin Exp Res 2003;15:43-50.
[62] Maki B, Holliday P, Topper A. A Prospective Study of Postural Balance and Risk of Falling in An Ambulatory and Independent Elderly Population. J Gerontol 1994;49:M72- 84.
[63] Edwards AE, Guven O, Furman MD, Arshad Q, Bronstein AM. Electroencephalographic Correlates of Continuous Postural Tasks of Increasing Difficulty. Neuroscience 2018;395:35-48.
[64] Hülsdünker T, Mierau A, Strüder HK. Higher Balance Task Demands are Associated with an Increase in Individual Alpha Peak Frequency. Front Hum Neurosci 2016;9:85.
[65] Jensen O, Mazaheri A. Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition. Front Hum Neurosci 2010;4:186.