Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults

Proprioceptive information from the foot/ankle provides important information regarding body sway for balance control, especially in situations where visual information is degraded or absent. Given known increases in catastrophic injury due to falls with older age, understanding the neural basis of proprioceptive processing for balance control is particularly important for older adults. In the present study, we linked neural activity in response to stimulation of key foot proprioceptors (i.e., muscle spindles) with balance ability across the lifespan. Twenty young and 20 older human adults underwent proprioceptive mapping; foot tendon vibration was compared with vibration of a nearby bone in an fMRI environment to determine regions of the brain that were active in response to muscle spindle stimulation. Several body sway metrics were also calculated for the same participants on an eyes-closed balance task. Based on regression analyses, multiple clusters of voxels were identified showing a significant relationship between muscle spindle stimulation-induced neural activity and maximum center of pressure excursion in the anterior–posterior direction. In this case, increased activation was associated with greater balance performance in parietal, frontal, and insular cortical areas, as well as structures within the basal ganglia. These correlated regions were age- and foot-stimulation side-independent and largely localized to right-sided areas of the brain thought to be involved in monitoring stimulus-driven shifts of attention. These findings support the notion that, beyond fundamental peripheral reflex mechanisms, central processing of proprioceptive signals from the foot is critical for balance control.

[1]  D. Goble,et al.  Upper limb asymmetries in the utilization of proprioceptive feedback , 2005, Experimental Brain Research.

[2]  S. Swinnen,et al.  The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen , 2012, Human brain mapping.

[3]  Daniel J Goble,et al.  Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense. , 2010, Journal of experimental psychology. Human perception and performance.

[4]  Daniel J Goble,et al.  Deficits in the ability to use proprioceptive feedback in children with hemiplegic cerebral palsy , 2009, International journal of rehabilitation research. Internationale Zeitschrift fur Rehabilitationsforschung. Revue internationale de recherches de readaptation.

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

[6]  Jean-Pierre Roll,et al.  A new vibrator to stimulate muscle proprioceptors in fMRI , 2009, Human brain mapping.

[7]  Daniel J. Goble,et al.  Proprioceptive target matching asymmetries in left-handed individuals , 2009, Experimental Brain Research.

[8]  H. Leibowitz,et al.  The effects of visual factors and head orientation on postural steadiness in women 55 to 70 years of age. , 1992, Journal of gerontology.

[9]  J. Roll,et al.  Motor and parietal cortical areas both underlie kinaesthesia. , 2003, Brain research. Cognitive brain research.

[10]  D. Goble,et al.  Proprioceptive Acuity Assessment Via Joint Position Matching: From Basic Science to General Practice , 2010, Physical Therapy.

[11]  S. Swinnen,et al.  The neural control of bimanual movements in the elderly: Brain regions exhibiting age‐related increases in activity, frequency‐induced neural modulation, and task‐specific compensatory recruitment , 2010, Human brain mapping.

[12]  S. Lord,et al.  Postural stability and associated physiological factors in a population of aged persons. , 1991, Journal of gerontology.

[13]  D. Goble,et al.  Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement , 2007, Experimental Brain Research.

[14]  H Okada,et al.  Brain activation during maintenance of standing postures in humans. , 1999, Brain : a journal of neurology.

[15]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  Bernard Amblard,et al.  The polymodal sensory cortex is crucial for controlling lateral postural stability: evidence from stroke patients , 2000, Brain Research Bulletin.

[17]  Robert J. Peterka,et al.  Diabetic neuropathy and surface sway-referencing disrupt somatosensory information for postural stability in stance , 2002, Somatosensory & motor research.

[18]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

[19]  A. Elster,et al.  Relationship between balance and abnormalities in cerebral magnetic resonance imaging in older adults. , 1998, Archives of neurology.

[20]  H Okada,et al.  Absolute changes in regional cerebral blood flow in association with upright posture in humans: an orthostatic PET study. , 2001, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[21]  Michelle H Cameron,et al.  Postural Control in Multiple Sclerosis: Implications for Fall Prevention , 2010, Current neurology and neuroscience reports.

[22]  J. S. Schneider,et al.  A consideration of sensory factors involved in motor functions of the basal ganglia , 1985, Brain Research Reviews.

[23]  F. Horak,et al.  Contributions of altered sensation and feedback responses to changes in coordination of postural control due to aging. , 2002, Gait & posture.

[24]  R. Krampe,et al.  Working memory and postural control: adult age differences in potential for improvement, task priority, and dual tasking. , 2009, The journals of gerontology. Series B, Psychological sciences and social sciences.

[25]  I. Deary,et al.  Brain white matter lesions detected by magnetic resosnance imaging are associated with balance and gait speed , 2003 .

[26]  J. Rose,et al.  Postural sway reduction in aging men and women: Relation to brain structure, cognitive status, and stabilizing factors , 2009, Neurobiology of Aging.

[27]  J. Roll,et al.  Relations between the directions of vibration-induced kinesthetic illusions and the pattern of activation of antagonist muscles , 2000, Brain Research.

[28]  J. Roll,et al.  Proprio-tactile integration for kinesthetic perception: An fMRI study , 2008, Neuropsychologia.

[29]  Ichiro Miyai,et al.  Role of the prefrontal cortex in human balance control , 2008, NeuroImage.

[30]  Martin Wiesmann,et al.  Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging , 2004, NeuroImage.

[31]  John Concato,et al.  Do Age and Comorbidity Affect Intensity of Pharmacological Therapy for Poorly Controlled Diabetes Mellitus? , 2005, Journal of the American Geriatrics Society.

[32]  S. Swinnen,et al.  Proprioceptive sensibility in the elderly: Degeneration, functional consequences and plastic-adaptive processes , 2009, Neuroscience & Biobehavioral Reviews.

[33]  N Teasdale,et al.  Gait of a deafferented subject without large myelinated sensory fibers below the neck , 1996, Neurology.

[34]  M. D. Crutcher,et al.  Primate globus pallidus and subthalamic nucleus: functional organization. , 1985, Journal of neurophysiology.

[35]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[36]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[37]  Daniel J. Goble,et al.  Dynamic proprioceptive target matching behavior in the upper limb: Effects of speed, task difficulty and arm/hemisphere asymmetries , 2009, Behavioural Brain Research.

[38]  Christianna S. Williams,et al.  The effect of falls and fall injuries on functioning in community-dwelling older persons. , 1998, The journals of gerontology. Series A, Biological sciences and medical sciences.

[39]  Thomas Brandt,et al.  Aging of human supraspinal locomotor and postural control in fMRI , 2012, Neurobiology of Aging.

[40]  J. Mugler,et al.  White matter abnormalities in mobility-impaired older persons , 2000, Neurology.

[41]  Patricia Romaiguère,et al.  Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration , 1999, Experimental Brain Research.

[42]  B. Bloem,et al.  Role of the Basal Ganglia in Balance Control , 2005, Neural plasticity.

[43]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[44]  Daniel J Goble,et al.  Development of upper limb proprioceptive accuracy in children and adolescents. , 2005, Human movement science.

[45]  S. Swinnen,et al.  Systems Neuroplasticity in the Aging Brain: Recruiting Additional Neural Resources for Successful Motor Performance in Elderly Persons , 2008, The Journal of Neuroscience.

[46]  S. Swinnen,et al.  Neural Basis of Aging: The Penetration of Cognition into Action Control , 2005, The Journal of Neuroscience.

[47]  Leslie G. Ungerleider,et al.  Dominance of the right hemisphere and role of area 2 in human kinesthesia. , 2005, Journal of neurophysiology.

[48]  Anders M. Dale,et al.  Consistent neuroanatomical age-related volume differences across multiple samples , 2011, Neurobiology of Aging.

[49]  D. Goble,et al.  The biological and behavioral basis of upper limb asymmetries in sensorimotor performance , 2008, Neuroscience & Biobehavioral Reviews.

[50]  J. Roll,et al.  Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study , 2004, Experimental Brain Research.

[51]  D. Goble,et al.  Upper limb asymmetries in the matching of proprioceptive versus visual targets. , 2008, Journal of neurophysiology.

[52]  J. Roll,et al.  Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography , 2004, Experimental Brain Research.

[53]  Eiichi Naito,et al.  Human limb‐specific and non‐limb‐specific brain representations during kinesthetic illusory movements of the upper and lower extremities , 2007, The European journal of neuroscience.

[54]  C. Richards,et al.  Brain activations during motor imagery of locomotor‐related tasks: A PET study , 2003, Human brain mapping.

[55]  R. Fitzpatrick,et al.  Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. , 1994, The Journal of physiology.

[56]  M. D. Crutcher,et al.  Single cell studies of the primate putamen , 2004, Experimental Brain Research.

[57]  F. Horak,et al.  The importance of somatosensory information in triggering and scaling automatic postural responses in humans , 2004, Experimental Brain Research.

[58]  Karl J. Friston,et al.  A critique of functional localisers , 2006, NeuroImage.

[59]  M. Tinetti,et al.  Risk Factors for Serious Injury During Falls by Older Persons in the Community , 1995, Journal of the American Geriatrics Society.

[60]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

[62]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[63]  D. McCloskey,et al.  Proprioceptive Illusions Induced by Muscle Vibration: Contribution by Muscle Spindles to Perception? , 1972, Science.

[64]  J. Nielsen,et al.  Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback , 2007, Nature Neuroscience.

[65]  M. Roesch,et al.  A new perspective on the role of the orbitofrontal cortex in adaptive behaviour , 2009, Nature Reviews Neuroscience.

[66]  A M Wing,et al.  Age differences in postural stability are increased by additional cognitive demands. , 1996, The journals of gerontology. Series B, Psychological sciences and social sciences.