Frontal brain activation changes due to dual-tasking under partial body weight support conditions in older adults with multiple sclerosis

BackgroundGait impairments present while dual-tasking in older adults with multiple sclerosis (MS) have been associated with an increased risk of falls. Prior studies have examined prefrontal cortex (PFC) activity using functional near infrared spectroscopy (fNIRS) while dual-tasking in older adults with and without cognitive impairment. While the benefits of partial body weight support (PBWS) on gait have been clearly outlined in the literature, the potential use of PBWS to improve the ability to dual task in older adults with and without MS has not been examined. The aim of this study was to examine the effects of PBWS on the PFC activation while dual-tasking in older adults with and without MS.MethodsTen individuals with MS (mean 56.2 ± 5.1 yrs., 8 females) and 12 healthy older adults (HOA) (mean 63.1 ± 4.4 yrs., 9 females) participated in this study. PFC activation (i.e., oxygenated hemoglobin-HbO2) was measured using fNIRS. Assessments were done under two treadmill walking conditions: no body weight support (NBWS) and PBWS. Under each condition, participants were asked to walk at a comfortable speed (W) or walk and talk (WT). Linear mixed models were used to test for differences between cohorts, conditions, and tasks.ResultsHbO2 levels differed significantly between task (p < .001), cohort (p < .001), and BWS (p = .02). HbO2 levels increased under higher cognitive demands (i.e., W vs WT), in individuals with MS, and under different conditions (i.e., NBWS vs PBWS). Post-hoc analysis demonstrated a significant difference between cohorts during the WT and NBWS condition (p = .05). When examining the relative change in HbO2 levels during each task, a significant interaction between task, BWS, and cohort across time was observed (p < 0.01). While HOA increased PFC activation across time, MS exhibited a maintenance of PFC activation patterns during the WT under PBWS condition.ConclusionsThis study establishes the potential impact of PBWS on PFC activation patterns under dual-tasking conditions and sheds light on the ability for PBWS to be used as a therapeutic tool in individuals with neurological conditions to decrease cognitive demands while dual-tasking and thus decrease the risk of falls.

[1]  Meltem Izzetoglu,et al.  Motion artifact cancellation in NIR spectroscopy using discrete Kalman filtering , 2010, Biomedical engineering online.

[2]  R. Passingham,et al.  The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study , 1998, NeuroImage.

[3]  Scott A Langenecker,et al.  fMRI of healthy older adults during Stroop interference , 2004, NeuroImage.

[4]  Jurgen A. H. R. Claassen,et al.  Effects of Aging on Cerebral Oxygenation during Working-Memory Performance: A Functional Near-Infrared Spectroscopy Study , 2012, PloS one.

[5]  Jeffrey M. Hausdorff,et al.  Executive control deficits as a prodrome to falls in healthy older adults: a prospective study linking thinking, walking, and falling. , 2010, The journals of gerontology. Series A, Biological sciences and medical sciences.

[6]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[7]  Wendy A Rogers,et al.  Cognitive and Motor Mechanisms Underlying Older Adults' Ability to Divide Attention While Walking , 2011, Physical Therapy.

[8]  E. Field-Fote Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury. , 2001, Archives of physical medicine and rehabilitation.

[9]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[10]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[11]  P M Matthews,et al.  The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis , 2000, Annals of neurology.

[12]  R. Passingham Attention to action. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  R. Klaren,et al.  Walking and cognition, but not symptoms, correlate with dual task cost of walking in multiple sclerosis. , 2014, Gait & posture.

[14]  Jeannette R. Mahoney,et al.  fNIRS study of walking and walking while talking in young and old individuals. , 2011, The journals of gerontology. Series A, Biological sciences and medical sciences.

[15]  G. Scotti,et al.  Functional Magnetic Resonance Imaging Correlates of Fatigue in Multiple Sclerosis , 2002, NeuroImage.

[16]  M. Woollacott,et al.  The influence of a concurrent cognitive task on the compensatory stepping response to a perturbation in balance-impaired and healthy elders. , 2002, Gait & posture.

[17]  R. Motl,et al.  Brain activation changes during locomotion in middle-aged to older adults with multiple sclerosis , 2016, Journal of the Neurological Sciences.

[18]  Meral Mirza,et al.  Balance performance in three forms of multiple sclerosis , 2006, Neurological research.

[19]  K. Aminian,et al.  Relationships between dual-task related changes in stride velocity and stride time variability in healthy older adults. , 2006, Human movement science.

[20]  Meltem Izzetoglu,et al.  Online fronto-cortical control of simple and attention-demanding locomotion in humans , 2015, NeuroImage.

[21]  F. Horak,et al.  Body-worn motion sensors detect balance and gait deficits in people with multiple sclerosis who have normal walking speed. , 2012, Gait & posture.

[22]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. II. Subcortical structures and learning by trial and error. , 1997, Journal of neurophysiology.

[23]  H. Makizako,et al.  Brain activation during dual-task walking and executive function among older adults with mild cognitive impairment: a fNIRS study , 2013, Aging Clinical and Experimental Research.

[24]  B. Phillips,et al.  Gait and balance impairment in early multiple sclerosis in the absence of clinical disability , 2006, Multiple sclerosis.

[25]  Torsten Schubert,et al.  Neural mechanisms of concurrent stimulus processing in dual tasks , 2009, NeuroImage.

[26]  I. Miyai,et al.  Treadmill training with body weight support: its effect on Parkinson's disease. , 2000, Archives of physical medicine and rehabilitation.

[27]  Robert W Motl,et al.  Multiple Sclerosis Walking Scale-12 and oxygen cost of walking. , 2010, Gait & posture.

[28]  Ichiro Miyai,et al.  Gait capacity affects cortical activation patterns related to speed control in the elderly , 2009, Experimental Brain Research.

[29]  Morgan K. Boes,et al.  Walking and thinking in persons with multiple sclerosis who vary in disability. , 2011, Archives of physical medicine and rehabilitation.

[30]  M. Woollacott,et al.  Attention and the control of posture and gait: a review of an emerging area of research. , 2002, Gait & posture.

[31]  R. Meeusen,et al.  Treadmill Training in Multiple Sclerosis: Can Body Weight Support or Robot Assistance Provide Added Value? A Systematic Review , 2012, Multiple sclerosis international.

[32]  L. Ferrucci,et al.  A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. , 1994, Journal of gerontology.

[33]  J. Breitner,et al.  Detection of dementia in the elderly using telephone screening of cognitive status , 1993 .

[34]  Olivier Beauchet,et al.  Dual-Task-Related Gait Changes in , 2004, Gerontology.

[35]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[36]  P. Reuter-Lorenz,et al.  Neurocognitive Aging and the Compensation Hypothesis , 2008 .

[37]  R. Motl,et al.  Mobility and cognitive correlates of dual task cost of walking in persons with multiple sclerosis , 2014, Disability and rehabilitation.

[38]  R. Motl,et al.  Accuracy of the actibelt(®) accelerometer for measuring walking speed in a controlled environment among persons with multiple sclerosis. , 2012, Gait & posture.

[39]  Yaakov Stern,et al.  Age-related differences in executive control of working memory , 2004, Memory & cognition.

[40]  P. Kannus,et al.  Prevention of falls and consequent injuries in elderly people , 2005, The Lancet.

[41]  R. N. Spreng,et al.  Executive functions and neurocognitive aging: dissociable patterns of brain activity , 2012, Neurobiology of Aging.

[42]  M. Morey,et al.  A Pilot Study of Partial Unweighted Treadmill Training in Mobility-Impaired Older Adults , 2014, BioMed research international.

[43]  Ricardo M L Barros,et al.  Gait Training Combining Partial Body-Weight Support, a Treadmill, and Functional Electrical Stimulation: Effects on Poststroke Gait , 2007, Physical Therapy.

[44]  David A. Boas,et al.  Noninvasive Imaging of Cerebral Activation with Diffuse Optical Tomography , 2009 .

[45]  Kaarin J Anstey,et al.  Different cognitive profiles for single compared with recurrent fallers without dementia. , 2009, Neuropsychology.

[46]  M. D’Esposito,et al.  Working Memory Impairments in Multiple Sclerosis: Evidence From a Dual-Task Paradigm , 1996 .

[47]  Jeffrey M. Hausdorff,et al.  The role of executive function and attention in gait , 2008, Movement disorders : official journal of the Movement Disorder Society.

[48]  Xiaonan Xue,et al.  The relationship between specific cognitive functions and falls in aging. , 2007, Neuropsychology.

[49]  David A. Boas,et al.  Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters , 2003, NeuroImage.

[50]  T. Ribeiro,et al.  Effects of treadmill training with partial body weight support and the proprioceptive neuromuscular facilitation method on hemiparetic gait: a randomized controlled study. , 2013, European journal of physical and rehabilitation medicine.

[51]  H. Johansen-Berg,et al.  Prefrontal Cortex Activation While Walking Under Dual-Task Conditions in Stroke , 2016, Neurorehabilitation and neural repair.

[52]  K. Kubota,et al.  Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study , 2001, NeuroImage.

[53]  Thad W. Buster,et al.  Partial body weight support treadmill training speed influences paretic and non-paretic leg muscle activation, stride characteristics, and ratings of perceived exertion during acute stroke rehabilitation. , 2016, Human movement science.

[54]  Jeffrey M. Hausdorff,et al.  Dual tasking, gait rhythmicity, and Parkinson's disease: Which aspects of gait are attention demanding? , 2005, The European journal of neuroscience.

[55]  Jeffrey M. Hausdorff,et al.  Gait variability and fall risk in community-living older adults: a 1-year prospective study. , 2001, Archives of physical medicine and rehabilitation.

[56]  C. Randolph,et al.  The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): preliminary clinical validity. , 1998, Journal of clinical and experimental neuropsychology.

[57]  Stefan Hesse,et al.  Treadmill Training with Partial Body Weight Support: Influence of Body Weight Release on the Gait of Hemiparetic Patients , 1997 .

[58]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  Wolfgang Schramm,et al.  Team , 2018, Spaces of Intensity.

[60]  R. Motl,et al.  Dual task cost of walking is related to fall risk in persons with multiple sclerosis , 2013, Journal of the Neurological Sciences.

[61]  Jeannette R. Mahoney,et al.  Neuroimaging of mobility in aging: a targeted review. , 2014, The journals of gerontology. Series A, Biological sciences and medical sciences.

[62]  L. Rubenstein Falls in older people: epidemiology, risk factors and strategies for prevention. , 2006, Age and ageing.

[63]  Kaoru Takakusaki,et al.  Forebrain control of locomotor behaviors , 2008, Brain Research Reviews.

[64]  J. Kurtzke Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[65]  Jeffrey M. Hausdorff,et al.  Dual-task decrements in gait: contributing factors among healthy older adults. , 2008, The journals of gerontology. Series A, Biological sciences and medical sciences.

[66]  Charles Hall,et al.  Validity of Divided Attention Tasks In Predicting Falls in Older Individuals: A Preliminary Study , 2002, Journal of the American Geriatrics Society.

[67]  H. Barbeau,et al.  A new approach to retrain gait in stroke patients through body weight support and treadmill stimulation. , 1998, Stroke.

[68]  Carole Dufouil,et al.  White matter lesions volume and motor performances in the elderly , 2009, Annals of neurology.

[69]  M. O’Sullivan,et al.  Activate your online subscription , 2001, Neurology.

[70]  J. Barela,et al.  Gait training with partial body weight support during overground walking for individuals with chronic stroke: a pilot study , 2011, Journal of NeuroEngineering and Rehabilitation.

[71]  Roee Holtzer,et al.  Functional connectivity associated with gait velocity during walking and walking‐while‐talking in aging: A resting‐state fMRI study , 2015, Human brain mapping.

[72]  M. D’Esposito,et al.  The Influence of Working-Memory Demand and Subject Performance on Prefrontal Cortical Activity , 2002, Journal of Cognitive Neuroscience.

[73]  M. Filippi,et al.  Adaptive functional changes in the cerebral cortex of patients with nondisabling multiple sclerosis correlate with the extent of brain structural damage , 2002, Annals of neurology.

[74]  O. Beauchet,et al.  Dual-task-related gait changes in transitionally frail older adults : The type of the walking-associated cognitive task matter , 2005 .

[75]  Differences in dual-task performance and prefrontal cortex activation between younger and older adults , 2013, BMC Neuroscience.

[76]  Mee-Young Kim,et al.  Effects of conventional overground gait training and a gait trainer with partial body weight support on spatiotemporal gait parameters of patients after stroke , 2015, Journal of physical therapy science.

[77]  R. Klaren,et al.  Cognitive motor interference during walking in multiple sclerosis using an alternate-letter alphabet task. , 2014, Archives of physical medicine and rehabilitation.