Aging of the Somatosensory System: A Translational Perspective

Balance in the elderly population is a major concern given the often catastrophic and disabling consequences of fall-related injuries. Structural and functional declines of the somatosensory system occur with aging and potentially contribute to postural instability in older adults. The objectives of this article are: (1) to discuss the evidence regarding age-related anatomical and physiological changes that occur in the peripheral proprioceptive and cutaneous systems, (2) to relate the basic science research to the current evidence regarding clinical changes associated with normal aging, and (3) to review the evidence regarding age-related proprioceptive and cutaneous clinical changes and relate it to research examining balance performance in older adults. The article is organized by an examination of the receptors responsible for activating afferent pathways (muscle spindle, golgi tendon organ, and articular and cutaneous receptors) and the corresponding sensory afferent fibers and neurons. It integrates basic science laboratory findings with clinical evidence suggesting that advanced aging results in a decline in cutaneous sensation and proprioception. The potential relationship between postural instability and sensory impairments in older adults also is discussed. Current laboratory and clinical evidence suggests that aging results in: (1) diverse and nonuniform declines in the morphology and physiological function of the various sensory structures examined, (2) preferential loss of distal large myelinated sensory fibers and receptors, and (3) impaired distal lower-extremity proprioception, vibration and discriminative touch, and balance. These findings provide foundational knowledge that emphasizes the importance of using reliable and valid sensory testing protocols for older adults and the need for further research that clarifies the relationship between sensory impairment and balance.

[1]  N. Cauna,et al.  The structure of human digital pacinian corpuscles (corpus cula lamellosa) and its functional significance. , 1958, Journal of anatomy.

[2]  P J Dyck,et al.  A quantitative study of Meissner's corpuscles in man , 1966, Neurology.

[3]  M. Swash,et al.  The effect of age on human skeletal muscle. Studies of the morphology and innervation of muscle spindles. , 1972, Journal of the neurological sciences.

[4]  B. Tomlinson,et al.  The extensor digitorum brevis: histological and histochemical aspects , 1972, Journal of neurology, neurosurgery, and psychiatry.

[5]  K. Oota,et al.  A HISTOPATHOLOGICAL STUDY OF THE HUMAN SPINAL GANGLIA. NORMAL VARIATIONS IN AGING , 1974, Acta pathologica japonica.

[6]  R. Bossemeyer,et al.  Quantitative evaluation of joint motion sensation in an aging population. , 1978, Journal of gerontology.

[7]  R T Verrillo,et al.  Change in vibrotactile thresholds as a function of age. , 1979, Sensory processes.

[8]  M F Bruce,et al.  The relation of tactile thresholds to histology in the fingers of elderly people. , 1980, Journal of neurology, neurosurgery, and psychiatry.

[9]  A Prochazka,et al.  Muscle spindle function during normal movement. , 1981, International review of physiology.

[10]  S. Ochs,et al.  Axoplasmic transport in aged rats , 1982, Experimental Neurology.

[11]  P. Karanjia,et al.  Passive joint position sense after total hip replacement surgery , 1983, Annals of neurology.

[12]  P. Taylor Non-linear effects of age on nerve conduction in adults , 1984, Journal of the Neurological Sciences.

[13]  L. Kazis,et al.  The prevalence of knee osteoarthritis in the elderly. The Framingham Osteoarthritis Study. , 1987, Arthritis and rheumatism.

[14]  M. Tinetti,et al.  Risk factors for falls among elderly persons living in the community. , 1988, The New England journal of medicine.

[15]  Long-latency enhancement of quadriceps excitability from stimulation of skin afferents in young and old adults. , 1989, Journal of gerontology.

[16]  L. Nashner,et al.  Dynamic posturography in the diagnosis and management of dizziness and balance disorders. , 1990, Neurologic clinics.

[17]  F O Black,et al.  Age-related changes in human posture control: sensory organization tests. , 1990, Journal of vestibular research : equilibrium & orientation.

[18]  Peterka Rj,et al.  AGE-RELATED CHANGES IN HUMAN POSTURE CONTROL: SENSORY ORGANIZATION TESTS , 1990 .

[19]  H. Johansson,et al.  Receptors in the knee joint ligaments and their role in the biomechanics of the joint. , 1991, Critical reviews in biomedical engineering.

[20]  S. Lord,et al.  Physiological Factors Associated with Falls in an Elderly Population , 1991, Journal of the American Geriatrics Society.

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

[22]  R. P. Fabio,et al.  Influence of sensory inputs on standing balance in community-dwelling elders with a recent history of falling. , 1992, Physical therapy.

[23]  D. Downham,et al.  What is the effect of ageing on type 2 muscle fibres? , 1992, Journal of the Neurological Sciences.

[24]  R. Sattin Falls among older persons: a public health perspective. , 1992, Annual review of public health.

[25]  G E Stelmach,et al.  Improved foot position sense as a result of repetitions in older adults. , 1993, Journal of gerontology.

[26]  P. Salo,et al.  Age‐related loss of knee joint afferents in mice , 1993, Journal of neuroscience research.

[27]  L. Larsson,et al.  Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. , 1993, The Journal of physiology.

[28]  S. Lord,et al.  Age-associated differences in sensori-motor function and balance in community dwelling women. , 1994, Age and ageing.

[29]  J. Kaye,et al.  Neurologic evaluation of the optimally healthy oldest old. , 1994, Archives of neurology.

[30]  Matthew Q. Patterson,et al.  Dimensions of spatial acuity in the touch sense: changes over the life span. , 1995, Somatosensory & motor research.

[31]  Sandra Hobson,et al.  Prevention of Falls Among the Community-Dwelling Elderly: , 1995 .

[32]  Marjorie H. Woollacott,et al.  Motor Control: Theory and Practical Applications , 1995 .

[33]  J. Judge,et al.  Dynamic balance in older persons: effects of reduced visual and proprioceptive input. , 1995, The journals of gerontology. Series A, Biological sciences and medical sciences.

[34]  K. Kanda,et al.  Dynamic and static sensitivities of muscle spindle primary endings in aged rats to ramp stretch , 1995, Neuroscience Letters.

[35]  S. Robbins,et al.  Proprioception and stability: foot position awareness as a function of age and footwear. , 1995, Age and ageing.

[36]  J C Stevens,et al.  Spatial acuity of the body surface over the life span. , 1996, Somatosensory & motor research.

[37]  S. G. Lee,et al.  Moderate peripheral neuropathy impairs weight transfer and unipedal balance in the elderly. , 1996, Archives of physical medicine and rehabilitation.

[38]  X. Navarro,et al.  Functional changes of the peripheral nervous system with aging in the mouse , 1996, Neurobiology of Aging.

[39]  R. Marks Further evidence of impaired position sense in knee osteoarthritis. , 1996, Physiotherapy research international : the journal for researchers and clinicians in physical therapy.

[40]  F Englander,et al.  Economic dimensions of slip and fall injuries. , 1996, Journal of forensic sciences.

[41]  Uwe Proske,et al.  The Mammalian Muscle Spindle , 1997 .

[42]  G. M. Story,et al.  Afferent‐inherent regulation of myosin heavy chain isoforms in rat muscle spindles , 1997, Muscle & nerve.

[43]  B. Ulfhake,et al.  Alterations in mystacial pad innervation in the aged rat , 1997, Experimental Brain Research.

[44]  J. Walro,et al.  Stability of myosin heavy chain isoforms in selectively denervated adult rat muscle spindles , 1997, The Anatomical record.

[45]  Y. Pai,et al.  Effect of age and osteoarthritis on knee proprioception. , 1997, Arthritis and rheumatism.

[46]  J. Kaye,et al.  Balance in the healthy elderly: posturography and clinical assessment. , 1997, Archives of neurology.

[47]  J. Zuckerman,et al.  The effect of intraarticular anesthesia and elastic bandage on elbow proprioception. , 1998, Journal of shoulder and elbow surgery.

[48]  Y. Morisawa Morphological study of mechanoreceptors on the coracoacromial ligament , 1998, Journal of orthopaedic science : official journal of the Japanese Orthopaedic Association.

[49]  B. Ulfhake,et al.  Loss of primary sensory neurons in the very old rat: Neuron number estimates using the disector method and confocal optical sectioning , 1998, The Journal of comparative neurology.

[50]  R. Fitzpatrick,et al.  Lateral Stability, Sensorimotor Function and Falls in Older People , 1999, Journal of the American Geriatrics Society.

[51]  J. Bullock-Saxton,et al.  Joint reposition sense in subjects with unilateral osteoarthritis of the knee , 1999, Clinical rehabilitation.

[52]  D. Ceballos,et al.  Morphometric and ultrastructural changes with ageing in mouse peripheral nerve , 1999, Journal of anatomy.

[53]  P. Stern Neuroscience Fundamentals for Rehabilitation , 1999 .

[54]  D. Ceballos,et al.  Influence of aging on peripheral nerve function and regeneration , 2000, Journal of the peripheral nervous system : JPNS.

[55]  B. Ulfhake,et al.  Regulation of NGF‐family ligands and receptors in adulthood and senescence: correlation to degenerative and regenerative changes in cutaneous innervation , 2000, The European journal of neuroscience.

[56]  J. Bullock-Saxton,et al.  The influence of age on weight-bearing joint reposition sense of the knee , 2000, Experimental Brain Research.

[57]  R. Mynark,et al.  Comparison of Heteronymous Monosynaptic Ia Facilitation in Young and Elderly Subjects in Supine and Standing Positions , 2000, The International journal of neuroscience.

[58]  G. Engh,et al.  Comparison of Proprioception in Arthritic and Age-Matched Normal Knees* , 2000, The Journal of bone and joint surgery. American volume.

[59]  Scott M. Lephart,et al.  Proprioception and neuromuscular control in joint stability , 2000 .

[60]  P. Fransson,et al.  Changes in postural control in healthy elderly subjects are related to vibration sensation, vision and vestibular asymmetry. , 2001, Acta oto-laryngologica.

[61]  T. M. Owings,et al.  Mechanisms leading to a fall from an induced trip in healthy older adults. , 2001, The journals of gerontology. Series A, Biological sciences and medical sciences.

[62]  S. Swinnen,et al.  The effect of aging on dynamic position sense at the ankle , 2002, Behavioural Brain Research.

[63]  Romeo Chua,et al.  The role of cutaneous receptors in the foot. , 2002, Advances in experimental medicine and biology.

[64]  J. Richardson The clinical identification of peripheral neuropathy among older persons. , 2002, Archives of physical medicine and rehabilitation.

[65]  N. Adachi,et al.  Mechanoreceptors in the anterior cruciate ligament contribute to the joint position sense , 2002, Acta orthopaedica Scandinavica.

[66]  P Capodaglio,et al.  Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. , 2002, Journal of applied physiology.

[67]  J. T. Inglis,et al.  Distribution and behaviour of glabrous cutaneous receptors in the human foot sole , 2002, The Journal of physiology.

[68]  S. Bolanowski,et al.  Effect of aging on the subjective magnitude of vibration , 2002, Somatosensory & motor research.

[69]  M. Falempin,et al.  Expression of Myosin Heavy Chain Isoforms Along Intrafusal Fibers of Rat Soleus Muscle Spindles After 14 Days of Hindlimb Unloading , 2002, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[70]  W. Erwin,et al.  Evidence for a neuropathic contribution to the development of spontaneous knee osteoarthrosis in a mouse model , 2002, Acta orthopaedica Scandinavica.

[71]  R. Hinman,et al.  Balance impairments in individuals with symptomatic knee osteoarthritis: a comparison with matched controls using clinical tests. , 2002, Rheumatology.

[72]  J. Richardson Factors Associated With Falls in Older Patients With Diffuse Polyneuropathy , 2002, Journal of the American Geriatrics Society.

[73]  H. Johansson,et al.  Spinal and supraspinal effects of activity in ligament afferents. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[74]  P. Low,et al.  Morphometry of dorsal root ganglion in chronic experimental diabetic neuropathy. , 2002, Diabetes.

[75]  Dale H Carnegie,et al.  Symptomatic reversal of peripheral neuropathy in patients with diabetes. , 2002, Journal of the American Podiatric Medical Association.

[76]  R. Seerattan,et al.  Selective joint denervation promotes knee osteoarthritis in the aging rat , 2002, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[77]  B. Ulfhake,et al.  Evidence for loss of myelinated input to the spinal cord in senescent rats , 2002, Neurobiology of Aging.

[78]  S. Kilbreath,et al.  Kinesthesia at the knee: the effect of osteoarthritis and bandage application. , 2002, Arthritis and rheumatism.

[79]  S. Bhan,et al.  Balance and Gait in Total Hip Replacement: A Pilot Study , 2003, American journal of physical medicine & rehabilitation.

[80]  R. Cumming,et al.  Interventions for preventing falls in elderly people. , 2003, The Cochrane database of systematic reviews.

[81]  L. K. Boulgarides,et al.  Use of clinical and impairment-based tests to predict falls by community-dwelling older adults. , 2003, Physical therapy.

[82]  Hiroshi Moriyama,et al.  The aging of human Meissner's corpuscles as evidenced by parallel sectioning. , 2003, Okajimas folia anatomica Japonica.

[83]  Marty Alvarez-Reeves,et al.  Decline of tactile acuity in aging: a study of body site, blood flow, and lifetime habits of smoking and physical activity , 2003, Somatosensory & motor research.

[84]  L. M. Ward,et al.  Regional variation and changes with ageing in vibrotactile sensitivity in the human footsole. , 2003, The journals of gerontology. Series A, Biological sciences and medical sciences.

[85]  G. Allison,et al.  Is there a difference in hip joint position sense between young and older groups? , 2003, The journals of gerontology. Series A, Biological sciences and medical sciences.

[86]  Günther Deuschl,et al.  Falls in frequent neurological diseases--prevalence, risk factors and aetiology. , 2004, Journal of neurology.

[87]  Hylton B Menz,et al.  Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. , 2004, Archives of physical medicine and rehabilitation.

[88]  C. Oatis,et al.  Role of physical therapy in management of knee osteoarthritis , 2004, Current opinion in rheumatology.

[89]  D. Guez,et al.  Clinical and electrophysiological study of the peripheral nervous system in the elderly , 1993, Journal of Neurology.

[90]  N. Benjuya,et al.  Aging-induced shifts from a reliance on sensory input to muscle cocontraction during balanced standing. , 2004, The journals of gerontology. Series A, Biological sciences and medical sciences.

[91]  A. Harrison The influence of pathology, pain, balance, and self-efficacy on function in women with osteoarthritis of the knee. , 2004, Physical therapy.

[92]  Meg E Morris,et al.  Effects of age on balance control during walking. , 2004, Archives of physical medicine and rehabilitation.

[93]  R. Shields,et al.  Influence of age on dynamic position sense: evidence using a sequential movement task , 2005, Experimental Brain Research.

[94]  T. Forst,et al.  Impact of low frequency transcutaneous electrical nerve stimulation on symptomatic diabetic neuropathy using the new Salutaris device. , 2004, Diabetes, nutrition & metabolism.

[95]  J. Colebatch,et al.  Evidence for reflex and perceptual vestibular contributions to postural control , 2004, Experimental Brain Research.

[96]  J. Prendergast,et al.  Improvement of sensory impairment in patients with peripheral neuropathy. , 2004, Endocrine practice : official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists.

[97]  L Turner-Stokes,et al.  Exercise for people with peripheral neuropathy. , 2004, The Cochrane database of systematic reviews.

[98]  John P Hirdes,et al.  Restriction in activity associated with fear of falling among community-based seniors using home care services. , 2004, Age and ageing.

[99]  Susan M Murray,et al.  Physiological risk factors for falls in older people with lower limb arthritis. , 2004, The Journal of rheumatology.

[100]  M. Farooqi,et al.  Restoration of sensation, reduced pain, and improved balance in subjects with diabetic peripheral neuropathy: a double-blind, randomized, placebo-controlled study with monochromatic near-infrared treatment. , 2004, Diabetes care.

[101]  Hiroshi Yorifuji,et al.  Morphological and biochemical changes of neurofilaments in aged rat sciatic nerve axons , 2004, Journal of neurochemistry.

[102]  F. Gomez-Pinilla,et al.  Voluntary exercise increases axonal regeneration from sensory neurons. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[103]  I. Melzer,et al.  Postural stability in the elderly: a comparison between fallers and non-fallers. , 2004, Age and ageing.

[104]  E. Bosi,et al.  Effectiveness of frequency-modulated electromagnetic neural stimulation in the treatment of painful diabetic neuropathy , 2005, Diabetologia.

[105]  P. Korkusuz,et al.  Decrease in the numbers of mechanoreceptors in rabbit ACL: the effects of ageing , 2006, Knee Surgery, Sports Traumatology, Arthroscopy.

[106]  E. Kararizou,et al.  Morphometric study of the human muscle spindle. , 2005, Analytical and quantitative cytology and histology.

[107]  L. Draganich,et al.  Osteoarthritis of the Knees Increases the Propensity to Trip on an Obstacle , 2005, Clinical orthopaedics and related research.

[108]  Harriet G Williams,et al.  Are Measures Employed in the Assessment of Balance Useful for Detecting Differences among Groups that Vary by Age and Disease State? , 2005, Journal of geriatric physical therapy.

[109]  S R Lord,et al.  The physiology of falling: assessment and prevention strategies for older people. , 2005, Journal of science and medicine in sport.

[110]  L. Thornell,et al.  Fiber Content and Myosin Heavy Chain Composition of Muscle Spindles in Aged Human Biceps Brachii , 2005, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[111]  Sung H You,et al.  Joint position sense in elderly fallers: a preliminary investigation of the validity and reliability of the SENSERite measure. , 2005, Archives of physical medicine and rehabilitation.

[112]  J. Zuckerman,et al.  The effect of degenerative arthritis and prosthetic arthroplasty on shoulder proprioception. , 2005, Journal of shoulder and elbow surgery.

[113]  Stephen D. Perry,et al.  Evaluation of age-related plantar-surface insensitivity and onset age of advanced insensitivity in older adults using vibratory and touch sensation tests , 2006, Neuroscience Letters.