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Aging of the somatosensory system. a translational perspective

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  • 1. PerspectiveAging of the Somatosensory System:A Translational PerspectiveScott W Shaffer, Anne L Harrison SW Shaffer, PT, OCS, ECS, is a doctoral candidate in the Rehabil-Balance in the elderly population is a major concern given the often catastrophic and itation Sciences Doctoral Pro-disabling consequences of fall-related injuries. Structural and functional declines of gram, College of Health Sciences,the somatosensory system occur with aging and potentially contribute to postural University of Kentucky, 900 Lime-instability in older adults. The objectives of this article are: (1) to discuss the evidence stone Ave, Room 210A, Lexington,regarding age-related anatomical and physiological changes that occur in the periph- KY 40536-0200 (USA). Address all correspondence to Mr Shaffer at:eral proprioceptive and cutaneous systems, (2) to relate the basic science research to scott.shaffer@uky.edu.the current evidence regarding clinical changes associated with normal aging, and(3) to review the evidence regarding age-related proprioceptive and cutaneous AL Harrison, PT, PhD, is Associate Professor and Director, Division ofclinical changes and relate it to research examining balance performance in older Physical Therapy, Department ofadults. The article is organized by an examination of the receptors responsible for Rehabilitation Sciences, Universityactivating afferent pathways (muscle spindle, golgi tendon organ, and articular and of Kentucky.cutaneous receptors) and the corresponding sensory afferent fibers and neurons. It [Shaffer SW, Harrison AL. Agingintegrates basic science laboratory findings with clinical evidence suggesting that of the somatosensory system: aadvanced aging results in a decline in cutaneous sensation and proprioception. The translational perspective. Physpotential relationship between postural instability and sensory impairments in older Ther. 2007;87:193–207.]adults also is discussed. Current laboratory and clinical evidence suggests that aging © 2007 American Physical Therapyresults in: (1) diverse and nonuniform declines in the morphology and physiological Associationfunction of the various sensory structures examined, (2) preferential loss of distallarge myelinated sensory fibers and receptors, and (3) impaired distal lower-extrem-ity proprioception, vibration and discriminative touch, and balance. These findingsprovide foundational knowledge that emphasizes the importance of using reliableand valid sensory testing protocols for older adults and the need for further researchthat clarifies the relationship between sensory impairment and balance.February 2007 Volume 87 Number 2 Physical Therapy f 193
  • 2. Aging of the Somatosensory System: A Translational PerspectiveB alance is a fundamental skill majority of activities of daily living, but the patients’ functional abilities in that is often compromised with must integrate information from mul- order to plan interventions that opti- advancing age.1 Balance im- tiple sensory systems as task com- mize function and reduce fall risk.pairment in older adults increases plexity and challenge to postural sta- The complexity of this evaluative taskthe risk for falls,2 which ultimately bility increase. is increased by the heterogeneouscan lead to increased morbidity,3 characteristics within the older adultmortality,3,4 and health care costs.5 Multimodal afferent input is inte- population and the reality thatOne third of adults over the age of grated at various levels of the cen- apparently healthy older adults may65 years fall each year, and fall- tral nervous system, resulting in well have idiopathic changes andrelated costs are expected to exceed efferent processing for the coordi- diverse impairments that potentially$32 billion by the year 2020.5 Falls nated firing of multiple alpha moto- contribute to a decline in balance.in older adults also are associated neurons and their correspondingwith decreased confidence in move- muscle fibers. Specifically, process- The reality of what is normal forment and balance.6,7 Loss of confi- ing occurs reflexively at the level of elderly people underscores the impor-dence, or fear of falling, often results the spinal cord or is sent cranially to tance of addressing subtle and not-in decreased physical activity that, in subcortical or cortical areas for more so-subtle balance problems with allturn, may perpetuate further decline refined voluntary movements. The older adults. A 2003 meta-analysisin postural stability and quality of speed at which these events occur provides evidence that multidisci-life.8 Consequently, researchers and belies the complexity required for plinary and multifactorial risk factorclinicians have an intense interest in adequate functional outcomes. For screening and intervention programsidentifying the components that example, research suggests that for community-dwelling older adultscontribute to postural instability and older adults who cannot recover are likely to prevent falls.18 Addition-falls in older adults. from external environmental chal- ally, research suggests that balance lenges (eg, a “trip”) within 145 and mobility measures may help dis-Postural control represents a com- milliseconds are likely to fall, under- tinguish between the effects of agingplex interplay between the sensory scoring the cause for concern in the and disease states such as peripheraland motor systems and involves per- normal age-related declines noted in nerve disease,19 thus helping clini-ceiving environmental stimuli, re- the functioning of the sensory or cians identify patients who may besponding to alterations in the body’s motor systems.14 moving along a continuum towardorientation within the environment, further balance impairment and falland maintaining the body’s center Impairments in sensation, strength risk (Fig. 1).of gravity within the base of sup- (force-generating capacity of a mus-port.9,10 Sensory information about cle), reaction time, vestibular func- When faced with a multidimensionalthe status of the body within the en- tion, and vision occur with aging and problem such as balance impair-vironment emanates primarily from are believed to collectively contrib- ment, the more knowledge that athe proprioceptive, cutaneous, visual, ute to the increased likelihood of fall- person has about both the physio-and vestibular systems. Researchers11–13 ing.15–17 Physical therapists are faced logical and clinical foundations ofhave concluded that individuals rely with the challenging task of examin- the problem, the broader the poten-primarily on proprioceptive and cuta- ing older adults for the presence of tial avenues for developing effectiveneous input to maintain normal quiet sensorimotor impairments and then assessments and interventions for allstance and to safely accomplish the accurately relating these deficits to older adults. Translational research directly linking age-related physio- logical change in somatosensory sys- tems with functional outcomes in humans is scant, no doubt due to the challenges inherent in examin- ing physiological correlates in live human subjects. Currently, no re- views were identified that have addressed the collective body of knowledge surrounding cutaneousFigure 1.Balance impairment in older adults. The goals of physical therapy are to enable a shift and proprioceptive declines thattoward normal function for those with pathology and optimal function for those with occur with aging, even though thesenormal age-related balance decline.194 f Physical Therapy Volume 87 Number 2 February 2007
  • 3. Aging of the Somatosensory System: A Translational PerspectiveTable 1.Axon Classification, Axon Diameter, Receptor Types, and Functiona Sensory and Sensory Diameter End Organ/Receptor Function Motor Fibersb Fibersc (nm) A-alpha Ia 10–20 M: extrafusal fibers Muscle contraction S: nuclear bag and chain Detect changes in the length and intrasfusal fibers velocity of muscle stretch Ib 10–20 S: GTO Detect muscle tension S: GTO ligament receptors Detect tension in ligaments A-beta II 4–12 S: nuclear bag 2 and chain Detect changes in length of fibers muscle stretch S: Meissner’s corpuscle (skin) Vibration and discriminative touch S: pacinian corpuscle (skin) Vibration and discriminative touch S: Merkel disk (skin) Pressure on the skin S: Ruffini’s endings (skin) Skin stretch S: Ruffini’s joint receptor Extremes of range of motion and more to passive than active motion S: pacinian joint receptor Joint range of motion A-gamma 2–8 M: dynamic-nuclear bag 1 fibers Muscle spindle alignment M: static-nuclear bag 2 and Muscle spindle alignment chain fibers A-delta III 1–5 S: free nerve endings (skin and Crude touch, pain, temperature joints) C IV 1 S: free nerve endings (skin and Detect pain, temperature joints)a M motor branch, S sensory branch, GTO golgi tendon organs.b Erlanger J, Gasser HS. Electrical Signs of Nervous Activity. Philadelphia, Pa: University of Pennsylvania Press; 1937.c Lloyd D. Neuro patterns controlling transmission of ipsilateral hindlimb reflexes in cat. J Neurophysiol. 1943;6:293–315.systems appear to play regulatory pathways (muscle spindle, golgi ten- back that translates to appropriateroles in postural stability.13 don organ, and articular and cutane- reflexive and voluntary movements.20,21 ous receptors), as well as by anTherefore, the objectives of this arti- examination of the peripheral path- Muscle spindles are composed of acle are: (1) to review the evidence ways themselves. connective tissue capsule and intra-regarding normal age-related physio- fusal fibers, which are juxtaposedlogical and anatomical changes that Muscle Spindle and parallel to extrafusal or ordinaryoccur in the peripheral propriocep- Structure and Function muscle fibers (Tab. 1, Fig. 2). Intra-tive and cutaneous systems, (2) to Muscle spindles are stretch-sensitive fusal fibers are contractile on the endrelate the basic science research to mechanoreceptors that provide the and noncontractile centrally and arethe current evidence regarding clin- nervous system with information composed of the nuclear bag and theical changes associated with normal about the muscle’s length and veloc- nuclear chain fibers. The bag andaging, and (3) to review the evi- ity of contraction, thus contributing chain fibers transmit afferent infor-dence regarding age-related proprio- to an individual’s ability to discern mation regarding dynamic and staticceptive and cutaneous clinical joint movement (kinesthesia) and muscle states to the central nervouschanges and relate it to research joint position sense ( JPS). Collec- system via type Ia and II myelinatedexamining balance performance in tively, these functions are referred to fibers.22 The gamma ( ) motoneuronsolder adults. The article is organized as “proprioception,” and it appears synapse on the contractile region ofby an examination of the receptors that muscle spindles play an impor- the intrafusal fibers and maintain sen-responsible for activating afferent tant role in providing afferent feed- sitivity by initiating increased tensionFebruary 2007 Volume 87 Number 2 Physical Therapy f 195
  • 4. Aging of the Somatosensory System: A Translational Perspective diameter was identified in a subject who was 93 years of age. A signifi- cant decline in the number of intra- fusal fibers (P .04) also was ob- served in the deltoid muscle with the smallest quantity of fibers seen in an individual who was 82 years of age. No significant shifts were ob-Figure 2. served in any of the outcome vari-The structural components of the mammalian muscle spindle. The intrafusal fibersinclude the nuclei bag 1 and bag 2 fibers together with the smaller chain fibers. Ends ables for the quadriceps femoris orof the bag fibers extend beyond the capsule while chain fibers are within the limits of biceps muscle, implying that agethe capsule. Large Ia afferent fibers wrap around the nucleated portion of all 3 intrafusal may have a regional effect on spe-fiber types. Smaller type II afferent fibers terminate to side and predominantly supply cific muscles.bag 2 and chain fibers. Gamma dynamic ( D) efferent fibers innervate bag 1 fibers,whereas gamma static ( s) efferent fibers innervate bag 2 and chain fibers. Reprintedfrom Proske U. The mammalian muscle spindle. New Physiol Sci. 1997;12:37– 42, with Some authors28,29 have theorizedpermission from the American Physiological Society. that muscle-specific spindle alter- ations may be the result of local denervation, as research has dem-in the intrafusal fibers when the mus- logic changes to the muscle spindle. onstrated an increased proportioncle is actively shortened.22 In 1972, Swash and Fox25 reported of type I extrafusal muscle fibers that aged human muscle spindles observed within the deltoid and ex-The interdependent relationship among exhibited increased spindle capsule tensor digitorum brevis muscles withthe intrafusal fibers, Ia and II afferent thickness and a loss of total intrafusal age. The transition of type II to typefibers, and alpha-gamma motor units fibers per spindle. The authors also I extrafusal fibers may be partiallyrequires precise and integrated action observed spherical axonal swellings explained by the loss of type II axonsby the central nervous system. Spe- and expanded motor end plates and and reinnervation of these musclecifically, “alpha-gamma coactivation” postulated that spindle modifications fibers by surviving type I axons.26,29is dependent upon sensory informa- may be the result of dennervation.25 Further study is needed to confirmtion from the muscle spindle cor- whether the loss of innervation isrectly synapsing on the appropriate The findings of a recent study by the causative factor leading to mor-alpha-gamma motoneurons and spi- Kararizou et al26 provide further phological changes within the agingnal cord interneurons.23 The direct clarification and suggest that mor- muscle spindle and what level andsynapse on alpha motoneurons re- phologic changes within the muscle region (distal versus proximal lower-sults in the classic monosynaptic spindle may be specific to certain extremity muscles) of anatomicalstretch reflex, while synapses on muscles and only evident during loss is associated with impaired pro-spinal cord interneurons result in advanced aging. The investigators prioception and ultimately balancefacilitating or inhibiting multiple studied the morphometric character- dysfunction.muscles to ensure uninterrupted and istics of 72 muscle spindles obtainedcoordinated movements.24 Alpha and from individuals (26 –93 years of Liu et al27 have expanded on pre-gamma motoneurons also receive age) postmortem, with samples vious research by demonstratingconverging information from articular taken from the deltoid (n 23), bi- that microstructural and biochemi-receptors, cutaneous receptors, spinal ceps (n 22), quadriceps femoris cal age-related modifications occurinterneurons, and higher centers to en- (n 22), and extensor digitorum bre- within the postmortem human mus-sure accurate feedback regarding mus- vis (n 5) muscles. Statistical analysis cle spindle. They reported that thecle length and velocity of contraction combining data from all 4 muscles total number of biceps brachii mus-and thus appropriate force develop- failed to exhibit significant changes cle intrafusal fibers (P .0004) andment throughout the length of the for any of the outcome variables. nuclear chain fibers (P .0001) permuscle.23 However, individual muscle analysis spindle were significantly decreased revealed that spindles from the del- for older adults (n 21 total samples;Muscle Spindle: Anatomical and toid muscle (P .03) and the exten- n 5 subjects, age 69 – 83 years)Physiological Age-Related sor digitorum brevis muscle (P .04) as compared with younger adultsChanges had a significant reduction in spindle (n 36 total samples; n 10 subjects,Various investigators25–27 have sug- diameter as a function of age. In age 19 – 48 years).27 In contrast,gested that aging results in morpho- addition, the smallest muscle spindle there was no significant group dif-196 f Physical Therapy Volume 87 Number 2 February 2007
  • 5. Aging of the Somatosensory System: A Translational PerspectiveTable 2.Proprioceptive Somatosensation: Age-Related Anatomical, Physiological, and Clinical Changesa Model Muscle Spindle Changes Articular Receptor Clinical Proprioception Changes Human Increased capsular thickness25 2 in all joint receptor types in 2 JPS in the great toe60 2 number of intrafusal fibers25 coracoacromioclavicular 2 JPS ankle in weight bearing56 2 spindle diameter in deltoid and ligaments in patients and non–weight bearing52,53 extensor digitorum brevis muscles; no undergoing shoulder 2 JPS in the knee in partial weight changes in quadriceps femoris or arthroscopy49 bearing but not full weight biceps muscles26 bearing55 2 number of total intrafusal fibers and 2 JPS in older adults with knee chain fibers in biceps muscle; no osteoarthritis65,70 changes in the number of bag fibers27 No changes in hip JPS58 Modifications in myosin heavy chain content27 Alterations in distal sensory axons25 Animal Impaired spindle sensitivity with aging21 2 in pacinian, Ruffini’s, and golgi tendon–like receptors in older rabbits’ anterior cruciate ligments50 2 joint receptors and afferent input in mice with osteoarthritis66–68a JPS joint position sense.ference in nuclear bag fibers. The fibers, but not in bag 2 or chain et al21 examined the afferentauthors suggested that the loss of fibers, suggesting that modifications response of muscle spindles to vary-nuclear chain fibers may impair the seen with aging are not necessarily ing levels of stretch applied to thestatic sensitivity of the spindle and symmetrical across all intrafusal fiber medial gastrocnemius muscle ofultimately the ability to correctly types. It also is intriguing that similar middle-aged (n 10, 10 –14 monthsinterpret muscle length and JPS.27 MyHC adaptations occur in rats in of age) and old (n 14, 28 –30Interestingly, previous physiological response to hind-limb unloading33 months of age) rats. Older rats hadstudies30,31 have revealed a decline and denervation.34,35 significantly (P .001) lower dis-in static ankle JPS in older adults. charge rates than middle-aged rats The potential link between patho- when compared at the same muscleLiu and colleagues27 also examined logical spindle modifications and length, implying a decline in spindlemyosin heavy chain (MyHC) protein aging, decreased weight bearing, static sensitivity. The dynamic index,content of the spindle fibers. Myosin and peripheral neuropathy are a measure of spindle dynamic sensi-heavy chain isoforms were used intriguing considering that various tivity, also was significantly (P .005)because they have been shown to be investigators have identified that sen- lower for aged rats. Morphologicalkey contractile muscle proteins and sory impairments and postural insta- changes such as increased capsularmajor determinants of maximum bility occur with advanced aging,16,36 thickness and a decreased number ofshortening velocity of muscle cells.32 osteoarthritis (OA),37–39 and periph- intrafusal fibers may account for theThe investigators identified that 3 eral nerve disease.40 – 42 More impor- dampening of static and dynamic mus-types of MyHC isoforms had modi- tantly, collaborative bench and clinical cle spindle sensitivity that is seen withfied expression in aged muscle spin- research may assist in determining aging.21dles when compared with those the influence that exercise has on thefrom young subjects.27 Specifically, aging muscle spindle and whether These studies provide initial evidence cardiac MyHC expression was modifications, such as those in MyHC that selective morphological and func-decreased in all 3 intrafusal fiber isoforms, translate to improved pro- tional changes do occur in humantypes in older spindles, whereas prioception and postural stability in muscle spindles during aging (Tab. 2).fetal MyHC isoform expression was older adults. The findings are important to rehabil-decreased only in bag 2 intrafusal itation professionals because theyfibers. Additionally, slow MyHC Aged muscle spindles also appear to imply that the muscle spindle is a plas-expression was increased in bag 1 exhibit impaired sensitivity. Miwa tic structure and that modificationsFebruary 2007 Volume 87 Number 2 Physical Therapy f 197
  • 6. Aging of the Somatosensory System: A Translational Perspectiveare not uniform across all muscles or respond to tension. Free nerve end- Proprioception: Clinicalintrafusal fiber types. Future transla- ings respond to extreme mechan- Age-Related Changetional research that investigates the ical deformation and inflammation. Proprioception can be assessed clin-influence of rehabilitation strategies The overall contribution of joint re- ically through examination of aware-on functional adaptations of the aging ceptors to proprioception contin- ness of JPS and joint kinesthesiamuscle spindle is warranted and ues to be debated as some reports (motion). Joint kinesthesia is deter-may assist in defining the mechanisms have demonstrated that anestheti- mined by establishing a threshold atassociated with improved propriocep- cally blocking or removing articular which motion is detected duringtion, function, and balance in older receptors does not significantly im- various velocities and ranges ofadults. pair the ability to detect motion.44 – 46 movement. Joint position sense is It is accepted that joint receptors evaluated by having the individual are primarily activated at the end experience a specific joint positionGolgi Tendon Organ and range of motion,46 but may have a (angle) and then reproduce the po-Articular Receptors larger influence on proprioception sition actively or react during pas-Structure and Function through interneuronal connections sive movement.51 Table 2 providesThe golgi tendon organ (GTO) and to gamma motoneurons, thus biasing a summary of anatomical, physio-articular receptors provide addi- spindle sensitivity.47,48 logical, and clinical changes to pro-tional proprioceptive information prioceptive somatosensation.that is important for accurate as- Articular Receptors: Anatomicalsessment of joint movement. The and Physiological Age-Related Verschueren et al52 examinedGTO is located at the muscle- Change dynamic JPS for passive ankle plantartendon interface and relays afferent Only 2 studies were found that have flexion tested at various velocitiesinformation about tensile forces critically analyzed the relationship (15°, 20°, 25°, 30°/s). A total ofwithin the tendon. Golgi tendon between the aging process and 102 older (mean age 62.5 years,organs are sensitive to very slight structural modifications within ar- SD 5.0) and 24 young (meanchanges ( 1 g) in tension and are ticular receptors, and none were age 21.7 years, SD 2.0) men com-responsive to tension that occurs found that examined age-related pleted the proprioceptively con-either by active contraction or by changes in the GTO. Morisawa49 trolled task, which included havingpassive stretch.43 The activation of examined the mechanoreceptors subjects open their hand when thethe GTO results in Ib afferent neu- (Ruffini’s, pacinian, golgi tendon-like ipsilateral ankle reached the pre-ron activation (Tab. 1). This affer- ligament receptors, and free nerve scribed target angle. The oldest cat-ent information synapses in the spi- endings) from the coracoacromial egory of adults (70 years of age)nal cord on interneurons which ligaments of 23 patients pending exhibited significantly greaterare inhibitory to the alpha moto- shoulder surgery. The author re- (P .05) deviation from the specificneuron of the associated muscle, ported a general decline in the num- target angle and variability in perfor-resulting in decreased tension with- bers of all receptor types as subjects mance when compared within the muscle and tendon. increased in age from 20 to 78 years younger adults. Adults aged 60 to 70 of age. Aydog and colleagues50 re- years also demonstrated increasedArticular or joint proprioceptors cently conducted similar histological variance in performance, but wererespond to mechanical deformation analysis of anterior cruciate liga- no different from younger adults inof the joint capsule and ligaments. ments (ACLs) from young (2 months, their ability to reach the prescribedJoint receptors include the rapidly n 5), adult (12 months, n 4), and target angle. Sixty-five of the olderadapting pacinian corpuscles (PCs), old (60 months, n 5) rabbits. They adults and 15 of the younger adultsslower-adapting Ruffini’s endings, identified a significant (P .05) step- were retested while also havingligament receptors, and free nerve wise decrease in the numbers of vibration (60 Hz) applied to theendings. The Ruffini’s endings are Ruffini’s, pacinian, and golgi tendon- tibialis anterior tendon. Vibrationactivated at the extremes of joint like ligament receptors across age resulted in a marked increase in posi-movement and respond more to groups. Pacinian and Ruffini’s re- tioning errors for older adults, butpassive motion. Pacinian corpuscles ceptors that were visualized in older not young adults, suggesting thatrespond to mechanical stimulation rabbits also demonstrated irregular the age-related decline in dynamicduring movement, but not when the and flattened margins. JPS was a combination of reducedjoint is held in a constant position. cutaneous and spindle function.Ligament receptors are structurally Finally, the authors analyzed theand functionally similar to GTOs and198 f Physical Therapy Volume 87 Number 2 February 2007
  • 7. Aging of the Somatosensory System: A Translational Perspectiveeffects of knowledge of results Bullock-Saxton et al,55 for example, ported by these studies involvingpractice and determined that both errors in knee JPS during full weight knee and ankle JPS, in addition toyounger and older adults sig- bearing did not differ between research showing that perception ofnificantly improved (P .05) follow- young (20 –35 years), middle-aged joint motion at the first metatarso-ing practice trials. These findings (40 –55 years), and older (60 –75 phalangeal joint was significantlydemonstrate that dynamic JPS may years) participants with normal different between young and oldimprove in older adults who un- lower-extremity function. The lack adults.60dergo focused practice. of a change with age may reflect that weight bearing maximizes afferent Further clinical research that defines input from multiple joints and all reliable and valid assessment mea-Madhavan and Shields53 expanded types of proprioceptors (joint recep- sures for distal (great toe and ankle)on this testing protocol by testing tors, muscle spindle, GTO, and cuta- JPS is needed, as predominant pro-velocities from 10° to 90°/s. The neous input). When subjects were prioceptive changes seen in aginginvestigators also included measures tested in partial weight bearing and peripheral nerve disease oftenof balance (single-leg stance time), (30% of full weight bearing), there occur from distal to proximal. Oneelectromyographic (EMG) muscle were differences (P .05) between of the leading mechanisms for theactivity, and self-report of function older adults and participants in the age-related progression of sensory(36-Item Short-Form Health Survey middle-aged and young groups, im- and motor impairments from distalquestionnaire [SF-36]). Older adults plying that accuracy of knee JPS is to proximal appears to be the reduc-had decreased dynamic ankle JPS, weight dependent.55 Interestingly, tion in the rate of axonal trans-and proprioceptive decline was multiplanar weight-bearing JPS at the port.61– 63 For example, fast axonalstrongly associated (R2 .92) with ankle in older adults (n 46, mean transport was slowed from a meansingle-leg stance time (eyes closed). age 73.12 years) exhibited a signif- of 453 mm/d (SD 16) in 3-month-Furthermore, elderly participants icant reduction from young control old rats to 406 mm/d (SD 16) inhad co-contraction of the plantar subjects (n 10, mean age 22.20 38-month-old rats.63 The rate of dis-flexors and dorsiflexors throughout years). However, JPS at the ankle tal neurofilament protein transportthe passive proprioceptive position- was not able to discriminate be- also is delayed in distal axons withing task. Increased EMG activity was tween older adults who had not aging.61 The interdependency of thenot seen in younger adults, and the fallen and those with a history of a cell body, neurotrophic signaling,authors hypothesized that older fall within the past year (n 22, myelin, distal receptors, and axonaladults’ inability to relax may have mean age 73.12 years),56 possibly transport reinforces that most likelybeen a mechanism to increase sensi- due to the complexity of issues con- all of these areas play a role in thetivity or “gain” in the muscle spindle. tributing to falls risk.57 distal-to-proximal decline of sensa- tion that is seen in aging.These findings are consistent withprevious research showing that co- The current literature involving No studies were found that have spe-contractions about the ankle serve as aging and lower-extremity proprio- cifically examined or directly linkeda compensatory strategy for elderly ception also provides evidence that age-related articular receptor physio-people to maintain postural control.54 proximal joints may not be affected logical change and function. StudiesOlder adults also demonstrated im- to the same extent as distal joints. involving orthopedic pathologiesproved performance with practice, Pickard et al58 compared hip JPS such as ACL sprains and lower-providing additional evidence that in 30 healthy young control sub- extremity OA provide some informa-short-term training may enhance test jects (mean age 21.7 years) and 29 tion about the function of articularperformance. The next logical step healthy elderly subjects (mean receptors.64 –71 For example, Adachiin this research would be to examine age 75 years). Both active and pas- et al64 reported a modest, but signif-whether proprioceptive training ac- sive hip abduction and adduction JPS icant, correlation (r .41, P .03)tually influences functional measures were tested, and the results demon- between a decline in JPS and theand carries over to reduce the risk of strated that there were no significant total number of ACL mechanorecep-falls in older adults. group differences. Total hip replace- tors located in patients who under- ment (with capsulectomy) also has went knee arthroscopy (n 29, been shown to have a minimal ef-There is evidence that the amount age 14 – 47 years). fect on overall hip proprioception.59of weight bearing may influence the The hypothesis of a distal-to-proximallevel of age-related proprioceptive Previous studies involving older loss of proprioception also is sup-decline for the knee. In a study by adults with knee OA have shownFebruary 2007 Volume 87 Number 2 Physical Therapy f 199
  • 8. Aging of the Somatosensory System: A Translational Perspective Ruffini’s ending (Fig. 3). These 4 receptors, in combination with hair cells, deliver important feedback about the environment (Tab. 1).43 Cutaneous receptors are not typi- cally thought of as proprioceptors, but the information they provide supplements the JPS and move- ment.43 For example, the cutaneous receptors on the plantar surface of the foot deliver information about the site and force of weight-bearing activities,31,76,77 and research by Burke et al78 has demonstrated that cutaneous receptors influence mus- cle activity in the lower extremities. The investigators demonstrated that cutaneous stimulation of the ipsilat- eral or contralateral lower extremity increased the quadriceps femoris muscle excitability and the reflex response. This finding implies that communication occurs among the cutaneous receptors, the muscle-Figure 3. spindle gamma efferent system, andThe cutaneous receptors. The superficial fine touch receptors have small receptor alpha motoneuron activity.78fields and include the Meissner’s corpuscles, Merkel disks, and hair follicle receptors.The subcutaneous fine touch receptors have larger receptor fields and include thepacinian corpuscles and Ruffini’s endings. All of the fine touch receptors transmit Cutaneous Receptors:information via medium myelinated A or type II fibers. Free nerve endings are Anatomical and Physiologicallocated throughout the skin and provide information about coarse touch, pain, and Age-Related Changetemperature. The information from free nerve endings is transmitted by thinly (A ) or Research involving large myelin-nonmyelinated (C) fibers. Reprinted from Lundy-Eckman L. Neuroscience: Fundamen-tals of Rehabilitation. 2nd ed. Philadelphia, Pa: WB Saunders Co; 2002:99 –122, with related mechanoreceptors appearspermission of Elsevier. to be warranted because previous research suggests that aging affects these fibers and receptors to a greater extent than unmyelinated nerve fi-decreased numbers of articular derestimate the actual rate of occur- bers that transmit nociception.79 Inreceptors and neuronal degenera- rence.74 This high prevalence under- addition, due to their relatively largetion.66 – 68 Animal studies66,67 sug- scores the importance of conducting size, the majority of studies involvinggest that denervation and mechano- clinical trials with older adults with the effects of age on cutaneousreceptor loss actually precede joint lower-extremity OA, proprioceptive receptor decline have involved PCsdegeneration and may potentially be decline, and postural instability in and MCs.a causative factor in knee OA. order to better identify patient sub-Patients with unilateral knee OA also groups who are likely to respond to As early as 1958, Cauna and Man-exhibited decreased JPS when com- balance training.75 nan80 presented initial evidencepared against healthy controls,65 and that human PCs decrease in numberknee OA in humans is associated Cutaneous Receptors with advanced age. Structural adap-with impaired proprioception,69 –71 Structure and Function tations with aging are supported bypostural instability,38,72 and increased The cutaneous mechanoreceptors physiologic studies, such as that ofrisk for falls.73 Radiographic evidence that innervate glabrous or hairless Verrillo,81 which have shown thatof knee OA has been demonstrated skin are the rapidly adapting Meiss- vibrotactile sensitivity involving PCin more than 30% of the population ner’s corpuscle (MC), the slowly pathways becomes impaired withover 60 years of age, and it has been adapting Merkel disk, rapidly adapt- age. More recent work has shownsuggested that radiography may un- ing PC, and the slowly adapting that, at a vibration frequency of 250200 f Physical Therapy Volume 87 Number 2 February 2007
  • 9. Aging of the Somatosensory System: A Translational PerspectiveTable 3.Cutaneous Somatosensation: Age-Related Anatomical, Physiological, and Clinical Changes Model Pacinian Corpuscle Meissner’s Corpuscle Clinical Cutaneous Testing Human 2 number with increasing age80 2 concentration with increasing Diminished vibration perception age83 threshold testing77,86–88 2 vibration perception thresholds 2 size and number with increasing Diminished monofilament and perceived magnitude of age84 testing77 vibration at frequencies that activate pacinian channels81,82 2 number in the finger and Diminished 2-point discrimination impaired touch thresholds85 testing89–92Hz (resulting in preferential activa- times over those of young control Cutaneoustion of PCs), older adults who were subjects. Somatosensation:healthy (n 5, mean age 68.6 years) Clinical Age-Related Changerequired significantly greater ampli- The current body of knowledge in- Consistent with the anatomical find-tudes of vibration (mean increase dicates that both pacinian and Meiss- ings of declining cutaneous receptors19.2 dB) to achieve the same ner’s receptors are reduced in num- with age, multiple studies77,81,82,86 – 88sensation-perceived magnitude as ber with aging. In addition, both have demonstrated that older adultsyounger subjects (n 5, mean age have been associated clinically with have impaired abilities to detect vi-23.5 years).82 declines in vibration perception or bration (Tab. 3). Perry77 compared the touch thresholds. With the exception level of plantar surface vibration andMeissner’s corpuscles also exhibit of Bolton et al,83 the vast majority of monofilament sensitivity in youngstructural modifications and an physiological research involving MCs adults (n 7, age 23–26 years) andoverall decline in number and cross- and PCs has been conducted on the older adults (n 95, age 65–73 years)sectional area with aging.83– 85 Bolton fingers. One study was found that at 4 test sites (great toe, first metatarsalet al83 studied punch skin biopsies examined the distribution and com- head, fifth metatarsal head, and heel).from the little finger and plantar position of cutaneous receptors in Older adults had insensitivity to quan-aspect of the great toe in 91 individu- the plantar surface of the feet.76 This titative vibration stimulation (25 andals ranging in age from 11 to 89 2002 report by Kennedy and Inglis76 100 Hz) and monofilament testingyears. Analysis revealed a progres- was conducted on 13 volunteers, (2.83– 6.85, or 0.07–300 g of force)sive age-related decrease in both aged 22 to 50 years (mean age 29.6 across all sites in comparison with thethe great toe and little finger MC years), who were healthy. Microneu- young adults. When analyzing resultsmean concentrations (number of rographic recordings of the tibial only from older adults ( 65 years ofMCs/mm2). Iwasaki et al84 analyzed nerve at the popliteal fossa were age), Perry observed a clear demarca-tissue specimens from the right used to classify receptor types and tion point in the early seventiesindex finger of 10 male subjects fields. The investigators found that (72–73 years of age) where vibration(mean age 71.7 years, SD 10.3) 70% of the skin receptors in the plan- perception thresholds doubled. How-and found a significant correlation tar foot were fast adapting. They sug- ever, monofilament testing did notbetween MC concentration (r gested that the high percentage of allow for the same level of discrimina- .674, P .05) and age. Findings fast-adapting receptors may reflect tion in older adults. Perry concludedfrom this study also demonstrated the large degree of dynamic sensitiv- that vibration perception thresholda significant weak-to-moderate corre- ity that is needed for proper weight testing may provide a more sensitivelation between MC cross-sectional bearing and balance control. Addi- measure to detect the onset of age-area (r .43, P .01) and age.84 tional study is needed to validate related plantar insensitivity.77 TheseBruce 85 combined histological and this theory and the degree of lower- findings,77 combined with previoussensation testing and determined extremity cutaneous receptor de- research,81,82 support the view thatthat older adults not only had cline that is associated with im- older adults lose vibratory sensationdecreased MCs in the index finger, paired balance. with age and that vibratory testingbut also exhibited impaired touch should be considered when screeningthresholds that were elevated 21⁄2February 2007 Volume 87 Number 2 Physical Therapy f 201
  • 10. Aging of the Somatosensory System: A Translational Perspectivefor distal sensory impairments in older prospective research will assist in parameters (NCVs, SNAPs, and wave-adults. Questions concerning the determining whether 2-point sensa- form durations) peaked at age 40effect that the loss of vibratory sense tion of the feet has a clinically rele- years and subsequently declined.has on balance and fall risk also re- vant role as an assessment measure Further study by Bouche et al86main unanswered and merit further in older adults. revealed that marked motor and sen-investigation. sory nerve conduction changes con- sistently occurred in the lower Peripheral SensoryDiscriminative touch (ie, 2-point sen- extremities of subjects over 80 yearssation) has been found to be com- Innervation: Anatomical, of age. As compared with youngpromised with aging.89 –92 Stevens et Physiological, and Clinical adults (21–29 years of age), olderal92 assessed 2-point gap discrimina- Age-Related Change adults (63– 80 years of age) showedtion in 5 body regions (volar fore- Mechanoreceptors that summate to significant (P .05) reductions onlyarm, upper and lower surfaces of the a critical level result in peripheral in sural ( 73%) and median ( 38%)forefinger, and plantar and dorsal sur- afferent neural signals that travel SNAP amplitudes, suggesting thatfaces of the forefoot) in 60 healthy within peripheral axons to cell bod- sensory fibers are affected prior toolder adults ( 65 years of age, mean ies located within the dorsal root motor fibers with aging. In contrast,and age range not reported) and 19 ganglion (DRG). Sensory informa- the oldest group of adults ( 80 yearsyoung adults (18 –28 years of age). tion then travels along the proximal of age) demonstrated significantOlder subjects exhibited an average axons of the DRG into the spinal (P .01) global declines in bothdecline in the foot, fingertip, and fore- cord. These steps require healthy motor and sensory nerve conductionarm of 91%, 70%, and 22%, respec- axons that can transmit information, velocities and response amplitudes.tively. These findings agree with pre- as well as dorsal root ganglion cells There also was a progressive andvious findings that the loss of tactile that process and pass information to significant increase in the tibial H-acuity occurs in older adults and is the spinal cord. reflex latency time among the 3 agegreater in the distal extremities.89,90 groups. The age-related increase inAdditionally, there was no significant A reduction in the number and den- the H-reflex latency implies that thedifference between the dorsal and sity of myelinated peripheral nerve spinal reflex loop was delayed,96 andventral surfaces of the foot or finger, fibers and a decrease in thickness of other authors97 have postulated thatproviding evidence against the the myelin in the remaining fibers this potentially contributes to pos-hypothesis that sensory differences have consistently been reported with tural instability.result more from physical wear and aging in several animal species (for atear to the skin of the plantar surface review, see Verdu et al62). There is The aging-associated decline in sen-of the foot and palmar aspect of the also a large body of literature demon- sory nerve conduction and clinicalfinger.92 strating age-related changes in large sensory testing was once thought to fiber structure and nerve conduction be due to the loss of sensory neu-A degradation of tactile acuity in velocity (NCV).62,86,93–95 Specifically, rons.98 However, contemporary re-aging may be clinically meaningful in studies involving mice have shown search that has utilized improvedthat a recent study identified that the that myelin thickness, the number of laboratory techniques for countingloss of 2-point sensation in the plan- large myelinated fibers, and sensory neurons challenges this idea.99,100tar aspect of the toe was significantly NCV actually increase in young mice Recent experiments that analyzedgreater in “fallers” than in “nonfall- up to 12 months of age. In mice 12 to the total number of neurons fromers.”91 The researchers conducted 20 months of age (middle to early old the cervical and lumbar DRGs ofbalance and 2-point sensation tests age), there are only mild age-related 3- and 30-month-old rats discov-on 19 participants (mean age 78.4 declines. Past 20 months (old age), ered only a small ( 12%) decreaseyears, SD 1.3) who had sustained at sensory nerves show a steady de- for older rats. There was no signifi-least 2 falls in a 6-month period and cline in the numbers of axons, myelin cant relationship between the124 nonfallers (mean age 77.8 and fiber thickness, and sensory degree of sensory neuron loss andyears, SD 0.53). Subjects who had NCV.62,93,95 behavioral deficits (eg, von Frey tac-sustained multiple falls had a signifi- tile testing and hotplate testing).cant (P .05) increase in mediolat- An age-related decline in sensory Myelin-related DRG neurons in oldereral sway (28% more sway) and NCV and sensory nerve action po- rats exhibited significantly smallerimpaired 2-point sensation (X 14.9 tentials (SNAPs) have been identified cross-sectional area ( 16% in lum-mm, SD 1.1 versus X 12.98 mm, in humans.86,94 Taylor94 found that bar DRGs, P .001), suggesting thatSD 0.3) versus controls. Further adult sensory nerve conduction neurons may atrophy with age.202 f Physical Therapy Volume 87 Number 2 February 2007
  • 11. Aging of the Somatosensory System: A Translational PerspectiveHowever, there was no significant The knowledge that sensory neurons that animals ran, implying that a po-difference between young and old in older adults may be atrophied as tentially important relationship mayrats with respect to unmyelinated opposed to lost also provides foun- exist between exercise duration andDRG neurons.99 These findings pro- dational justification for examining neuronal outgrowth.109 Similar linesvide some evidence to suggest that the influence of therapeutic inter- of research involving healthy agedaging predominately results in atro- ventions (eg, exercise, sensory re- animals and those with neuropathyphy of myelinated primary sensory education, modality application) on may provide additional evidence ofneurons. the physiological function of these the benefits of exercise in promoting cells and the resulting effect on sen- sensory neuronal health and func-Kishi et al101 found similar bias sation and physical performance. In- tion. Conducting further clinical tri-toward myelinated neurons in their terventions such as monochromatic als also appears warranted as aanalysis of rats with diabetic periph- infrared photo energy103–105 and elec- Cochrane Review110 recently con-eral neuropathy (DPN). In general, trical stimulation therapy,106,107 which cluded that there is inadequate evi-there was no difference in the total are aimed at improving distal sensa- dence to evaluate the effects of exer-number of L5 DRG neurons between tion, have shown some promise in cise on functional ability in patientsrats with DPN and healthy age- the treatment of people with dia- with polyneuropathy.matched controls, but once cells betic peripheral neuropathy. Futurewere grouped based on size, large research may focus on identifyingmyelinated DRG neurons in diabetic characteristics of older adults capa- Somatosensory Integration:rats exhibited a 43% decrease (P ble of recovering from sensory dys- Age-Related Clinical.01) compared with healthy con- function and those for whom com- Changetrols. The results suggest that large pensation rather than recovery is the Computerized dynamic posturogra-myelinated sensory neurons may be key to intervention. phy (CDP) was designed to discrim-preferentially affected by pathology inate among the influences on pos-and that the structural response of One of the leading hypotheses re- tural stability provided by the visual,sensory neurons to pathology is pro- garding the physiological basis for vestibular, and somatosensory sys-gressively worse (cell loss or necro- the age-related changes discussed tems.111 Various authors have usedsis) than normal aging (cell atrophy, involves the influence of neurotro- CDP and other clinical examinationbut limited numbers of cell death). phin-signaling components. Neuro- approaches to investigate the influ- trophins are polypeptides that are ence of sensory impairments on pos-These findings support the view that essential in the development and sur- tural instability in older adults. Judgetesting large myelinated pathways vival of neurons in both the central et al112 examined 110 older adults(eg, reflex, vibration, propriocep- and peripheral nervous systems. A (mean age 80 years) with the CDPtion, discriminative touch) may pro- reduction of neurotrophins within sensory organization test (SOT) andvide the most sensitive measures for the skin and neurotrophin receptors found that errors in proprioceptionidentifying and discriminating sen- in primary sensory neurons is associ- had a greater effect on balance thansory impairments due to aging ver- ated with aging and may contribute did errors in vision, with the oldestsus those due to peripheral nerve to the distal sensory impairments participants demonstrating the great-disease. Research by Richardson102 that are seen with aging.100,108 Neu- est difficulty in conditions wheresupports this concept, as deficits in rotrophins also play an essential role proprioception was reduced.sensory testing domains (Achilles in activity-dependent plasticity andreflex testing, 128-Hz vibration tun- are enlightening our understanding Using CPD, Peterka and Black113ing fork testing at the great toe, or of how exercise influences the ner- found that balance equilibrium scoresJPS at the great toe) accurately vous system. For example, following for older adults up to 80 years of ageseparated older adults with and with- a nerve crush injury, DRG neurons exhibited substantial changes onlyout electrodiagnostically confirmed from adults rats that exercised for a when both proprioceptive and vi-peripheral nerve disease. The pres- 3- to 7-day period contained higher sual cues were disrupted. Camicolience of abnormal testing in 2 out of levels of neurotrophins and showed et al114 examined 48 healthy older3 of these domains identified distal improved axonal regeneration (P subjects (33 subjects 80 years ofperipheral neuropathy with a sensi- .01 at 3 days; P .0001 at 7 days) age [mean age 88 years, SD 5] andtivity of 94.1% and a specificity of when compared with sedentary ani- 15 subjects 80 years of age [mean88.4%.102 mals.109 The total distance of axonal age 72 years, SD 3]) who per- regeneration was strongly correlated formed the CDP SOT and clinical (r .626, P .001) to the distance measures of balance and perfor-February 2007 Volume 87 Number 2 Physical Therapy f 203
  • 12. Aging of the Somatosensory System: A Translational Perspectivemance (Tinetti Balance Scale, single- and in muscle spindle sensitivity in of which rely upon large myelin-leg stand, gait speed over 9 m). The old-old rats.21 ated afferent fiber functioning.investigators identified a significantdifference in the adaptive ability of These findings suggest the need to (4) Age-related involvement of sen-the “old-old” (80 years of age and provide some older adults (particu- sory fibers occurs earlier thanolder) participants when proprio- larly the old-old) with compensatory motor fibers.ceptive input was disrupted, con- strategies that increase sensory in-firming again that even with vision formation during function, such as (5) Nominal evidence exists linkingavailable, the oldest participants increased cutaneous and proprio- impaired proprioception and cu-needed accurate proprioception to ceptive feedback through the use of taneous sensation in the lowermaintain balance while the young- orthoses or an assistive device, im- extremities with balance dys-old participants ( 80 years of age) proved lighting in all domains of function in older adults.were better able to adapt to propri- function, and visually demonstrativeoceptive errors by using visual cues. boundaries on steps and curbs. Al- These conclusions highlight the ternately, these results combined importance of using and refiningSensory impairment in older adults is with previously discussed informa- sensory measures (vibration, mono-also associated with functional de- tion suggest that, for some older filament, 2-point discrimination, andcline and fall risk. Kaye and col- adults (particularly the young-old), proprioception testing) that can reli-leagues115 compared a variety of interventions designed to enhance ably and accurately assess the func-functional and neurologic screens recovery of sensory and balance tion of large myelinated fibers withinbetween 17 young-old adults (mean function may be more appropriate the lower extremities of older adults.age 70 years, SD 2.6) and 34 old- than those focusing on compensa- They also emphasize the need forold adults (mean age 89 years, tory strategies. These findings also additional research examining theSD 4.3) and found that vibration emphasize the importance of distin- physiological changes that occur insense (big toe), balance (Romberg guishing between young-old and old- sensory structures and function overtest, one-leg standing), and function old adults when conducting research time and the effect that such changes(gait speed) were significantly im- and when developing appropriate ex- have on postural stability in olderpaired in the oldest participant group. amination and intervention strategies. adults.Similarly, Anacker and Di Fabio116found that time to fall while standing Both authors provided concept/idea/projecton a compliant surface (eyes open Summary and Conclusions design, writing, and consultation (includingand eyes closed) discriminated fall- The following provides a summary review of manuscript before submission).ers from nonfallers, suggesting that of the themes that consistently The opinions and assertions containedin a group of similarly aged older emerged in our review of the influ- herein are the private views of the authorsadults (n 47, mean age 80.5 years, ence of age on peripheral somato- and are not to be construed as official or as reflecting the views of the Department of theSD 9), the reliance on accurate sensory systems: Army or the Department of Defense.proprioception information wasincreased in fallers. (1) A diverse and nonuniform This article was received March 14, 2006, and was accepted September 25, 2006. decline of sensory structure andFinally, Lord and colleagues15,17,36 physiological function occurs 10.2522/ptj.20060083have shown that lower-limb propri- across the life span, with evi-oception is significantly reduced in dence of accelerated declinesolder adults with a history of falling. with advanced aging. ReferencesThe delineation between abilities 1 Shkuratova N, Morris ME, Huxham F. Effects of age on balance control duringof young-old and old-old adults is (2) There exists a preferential loss walking. Arch Phys Med Rehabil. 2004;consistent with clinical and bench 85:582–588. in anatomical structure andresearch findings demonstrating an 2 Tinetti ME, Speechley M, Ginter SF. Risk physiological function of large factors for falls among elderly personsaccelerated loss in JPS in old-old myelinated fibers and associated living in the community. N Engl J Med.adults ( 70 years of age),52 reduced 1988;319:1701–1707. receptors.NCV of motor and sensory nerves in 3 Sattin RW. Falls among older persons: a public health perspective. Annu Revold-old adults ( 80 years of age),86 (3) Ample clinical studies demon- Public Health. 1992;13:489 –508.and animal models demonstrating a strate that older adults exhibit 4 Speechley M, Tinetti M. Assessment ofreduction in myelin thickness, in the risk and prevention of falls among elderly impaired proprioception, vibra- persons: role of the physiotherapist.number of large myelinated fibers,62 tion, and discriminative touch, all Physiother Can. 1990;42:75–78.204 f Physical Therapy Volume 87 Number 2 February 2007
  • 13. Aging of the Somatosensory System: A Translational Perspective 5 Englander F, Hodson TJ, Terregrossa RA. 21 Miwa T, Miwa Y, Kanda K. Dynamic and 38 Hinman RS, Bennell KL, Metcalf BR, Economic dimensions of slip and fall static sensitivities of muscle spindle pri- Crossley KM. Balance impairments in in- injuries. J Forensic Sci. 1996;41: mary endings in aged rats to ramp dividuals with symptomatic knee osteoar- 733–746. stretch. Neurosci Lett. 1995;201: thritis: a comparison with matched con- 179 –182. trols using clinical tests. Rheumatology 6 Steinmetz HM, Hobson SJ. Prevention of (Oxford). 2002;41:1388 –1394. falls among the community-dwelling 22 Proske U. The mammalian muscle spin- elderly: an overview. Phys Occup Ther dle. New Physiol Sci. 1997;12:37– 42. 39 Pandya NK, Draganich LF, Mauer A, et al. Geriatr. 1994;12:13–29. Osteoarthritis of the knees increases the 23 Riemann BL, Guskiewicz KM. Proprio- propensity to trip on an obstacle. 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  • 14. Aging of the Somatosensory System: A Translational Perspective54 Benjuya N, Melzer I, Kaplanski J. Aging- 71 Pai YC, Rymer WZ, Chang RW, Sharma 88 Wells C, Ward LM, Chua R, Inglis JT. induced shifts from a reliance on sensory L. Effect of age and osteoarthritis on Regional variation and changes with age- input to muscle co-contraction during knee proprioception. Arthritis Rheum. ing in vibrotactile sensitivity in the human balanced standing. J Gerontol A Biol Sci 1997;40:2260 –2265. footsole. J Gerontol A Biol Sci Med Sci. Med Sci. 2004;59:166 –171. 2003;58:680 – 686. 72 Harrison AL. The influence of pathology,55 Bullock-Saxton JE, Wong WJ, Hogan N. pain, balance, and self-efficacy on func- 89 Stevens JC, Choo KK. Spatial acuity of The influence of age on weight-bearing tion in women with osteoarthritis of the the body surface over the life span. joint reposition sense of the knee. Exp knee. Phys Ther. 2004;84:822– 831. Somatosens Mot Res. 1996;13:153–166. 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