2. Aging of the Somatosensory System: A Translational Perspective
B
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 task
the risk for falls,2 which ultimately bility increase. is increased by the heterogeneous
can lead to increased morbidity,3 characteristics within the older adult
mortality,3,4 and health care costs.5 Multimodal afferent input is inte- population and the reality that
One third of adults over the age of grated at various levels of the cen- apparently healthy older adults may
65 years fall each year, and fall- tral nervous system, resulting in well have idiopathic changes and
related 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 corresponding
with decreased confidence in move- muscle fibers. Specifically, process- The reality of what is normal for
ment 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 all
turn, may perpetuate further decline refined voluntary movements. The older adults. A 2003 meta-analysis
in 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 factor
clinicians have an intense interest in adequate functional outcomes. For screening and intervention programs
identifying the components that example, research suggests that for community-dwelling older adults
contribute 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 aging
plex interplay between the sensory scoring the cause for concern in the and disease states such as peripheral
and 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 be
sponding to alterations in the body’s motor systems.14 moving along a continuum toward
orientation within the environment, further balance impairment and fall
and 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 multidimensional
the 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 a
the 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 of
have 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 effective
neous input to maintain normal quiet sensorimotor impairments and then assessments and interventions for all
stance 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 cutaneous
Figure 1.
Balance impairment in older adults. The goals of physical therapy are to enable a shift and proprioceptive declines that
toward normal function for those with pathology and optimal function for those with occur with aging, even though these
normal age-related balance decline.
194 f Physical Therapy Volume 87 Number 2 February 2007
3. Aging of the Somatosensory System: A Translational Perspective
Table 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 appropriate
roles in postural stability.13 don organ, and articular and cutane- reflexive and voluntary movements.20,21
ous receptors), as well as by an
Therefore, the objectives of this arti- examination of the peripheral path- Muscle spindles are composed of a
cle are: (1) to review the evidence ways themselves. connective tissue capsule and intra-
regarding normal age-related physio- fusal fibers, which are juxtaposed
logical and anatomical changes that Muscle Spindle and parallel to extrafusal or ordinary
occur 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 end
relate the basic science research to mechanoreceptors that provide the and noncontractile centrally and are
the current evidence regarding clin- nervous system with information composed of the nuclear bag and the
ical changes associated with normal about the muscle’s length and veloc- nuclear chain fibers. The bag and
aging, 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 static
ceptive and cutaneous clinical joint movement (kinesthesia) and muscle states to the central nervous
changes and relate it to research joint position sense ( JPS). Collec- system via type Ia and II myelinated
examining balance performance in tively, these functions are referred to fibers.22 The gamma ( ) motoneurons
older adults. The article is organized as “proprioception,” and it appears synapse on the contractile region of
by 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 tension
February 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 fibers
include the nuclei bag 1 and bag 2 fibers together with the smaller chain fibers. Ends ables for the quadriceps femoris or
of the bag fibers extend beyond the capsule while chain fibers are within the limits of biceps muscle, implying that age
the 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. Reprinted
from Proske U. The mammalian muscle spindle. New Physiol Sci. 1997;12:37– 42, with Some authors28,29 have theorized
permission 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 proportion
cle 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 with
the intrafusal fibers, Ia and II afferent thickness and a loss of total intrafusal age. The transition of type II to type
fibers, and alpha-gamma motor units fibers per spindle. The authors also I extrafusal fibers may be partially
requires precise and integrated action observed spherical axonal swellings explained by the loss of type II axons
by the central nervous system. Spe- and expanded motor end plates and and reinnervation of these muscle
cifically, “alpha-gamma coactivation” postulated that spindle modifications fibers by surviving type I axons.26,29
is dependent upon sensory informa- may be the result of dennervation.25 Further study is needed to confirm
tion from the muscle spindle cor- whether the loss of innervation is
rectly 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 aging
nal cord interneurons.23 The direct clarification and suggest that mor- muscle spindle and what level and
synapse 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 anatomical
stretch 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 balance
facilitating or inhibiting multiple studied the morphometric character- dysfunction.
muscles to ensure uninterrupted and istics of 72 muscle spindles obtained
coordinated 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 demonstrating
converging 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 occur
interneurons, 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 the
cle 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) and
ment throughout the length of the for any of the outcome variables. nuclear chain fibers (P .0001) per
muscle.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 adults
Changes 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 Perspective
Table 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
osteoarthritis66–68
a
JPS joint position sense.
ference in nuclear bag fibers. The fibers, but not in bag 2 or chain et al21 examined the afferent
authors 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 the
static sensitivity of the spindle and symmetrical across all intrafusal fiber medial gastrocnemius muscle of
ultimately the ability to correctly types. It also is intriguing that similar middle-aged (n 10, 10 –14 months
interpret muscle length and JPS.27 MyHC adaptations occur in rats in of age) and old (n 14, 28 –30
Interestingly, previous physiological response to hind-limb unloading33 months of age) rats. Older rats had
studies30,31 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 muscle
Liu and colleagues27 also examined logical spindle modifications and length, implying a decline in spindle
myosin 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. Morphological
key contractile muscle proteins and sory impairments and postural insta- changes such as increased capsular
major determinants of maximum bility occur with advanced aging,16,36 thickness and a decreased number of
shortening velocity of muscle cells.32 osteoarthritis (OA),37–39 and periph- intrafusal fibers may account for the
The 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 with
fied expression in aged muscle spin- research may assist in determining aging.21
dles when compared with those the influence that exercise has on the
from 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 human
types 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 they
fibers. 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 modifications
February 2007 Volume 87 Number 2 Physical Therapy f 197
6. Aging of the Somatosensory System: A Translational Perspective
are not uniform across all muscles or respond to tension. Free nerve end- Proprioception: Clinical
intrafusal fiber types. Future transla- ings respond to extreme mechan- Age-Related Change
tional 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 kinesthesia
muscle 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 at
associated with improved propriocep- cally blocking or removing articular which motion is detected during
tion, function, and balance in older receptors does not significantly im- various velocities and ranges of
adults. 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 position
Golgi 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 provides
The 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: Anatomical
sessment of joint movement. The and Physiological Age-Related Verschueren et al52 examined
GTO is located at the muscle- Change dynamic JPS for passive ankle plantar
tendon interface and relays afferent Only 2 studies were found that have flexion tested at various velocities
information about tensile forces critically analyzed the relationship (15°, 20°, 25°, 30°/s). A total of
within 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 (mean
changes ( 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 having
passive stretch.43 The activation of examined the mechanoreceptors subjects open their hand when the
the 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 greater
are inhibitory to the alpha moto- shoulder surgery. The author re- (P .05) deviation from the specific
neuron 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 with
in 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 increased
Articular or joint proprioceptors cently conducted similar histological variance in performance, but were
respond to mechanical deformation analysis of anterior cruciate liga- no different from younger adults in
of the joint capsule and ligaments. ments (ACLs) from young (2 months, their ability to reach the prescribed
Joint receptors include the rapidly n 5), adult (12 months, n 4), and target angle. Sixty-five of the older
adapting pacinian corpuscles (PCs), old (60 months, n 5) rabbits. They adults and 15 of the younger adults
slower-adapting Ruffini’s endings, identified a significant (P .05) step- were retested while also having
ligament receptors, and free nerve wise decrease in the numbers of vibration (60 Hz) applied to the
endings. The Ruffini’s endings are Ruffini’s, pacinian, and golgi tendon- tibialis anterior tendon. Vibration
activated 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, but
passive motion. Pacinian corpuscles ceptors that were visualized in older not young adults, suggesting that
respond to mechanical stimulation rabbits also demonstrated irregular the age-related decline in dynamic
during movement, but not when the and flattened margins. JPS was a combination of reduced
joint is held in a constant position. cutaneous and spindle function.
Ligament receptors are structurally Finally, the authors analyzed the
and functionally similar to GTOs and
198 f Physical Therapy Volume 87 Number 2 February 2007
7. Aging of the Somatosensory System: A Translational Perspective
effects of knowledge of results Bullock-Saxton et al,55 for example, ported by these studies involving
practice and determined that both errors in knee JPS during full weight knee and ankle JPS, in addition to
younger and older adults sig- bearing did not differ between research showing that perception of
nificantly 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 significantly
demonstrate that dynamic JPS may years) participants with normal different between young and old
improve in older adults who un- lower-extremity function. The lack adults.60
dergo 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 aging
investigators also included measures
tested in partial weight bearing and peripheral nerve disease often
of balance (single-leg stance time),
(30% of full weight bearing), there occur from distal to proximal. One
electromyographic (EMG) muscle
were differences (P .05) between of the leading mechanisms for the
activity, 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 distal
questionnaire [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 axonal
strongly associated (R2 .92) with
ankle in older adults (n 46, mean transport was slowed from a mean
single-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) in
had 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 transport
the passive proprioceptive position-
was not able to discriminate be- also is delayed in distal axons with
ing task. Increased EMG activity was
tween older adults who had not aging.61 The interdependency of the
not 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 axonal
adults’ inability to relax may have
mean age 73.12 years),56 possibly transport reinforces that most likely
been a mechanism to increase sensi-
due to the complexity of issues con- all of these areas play a role in the
tivity 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 with
previous 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 linked
a 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. Studies
Older adults also demonstrated im- to the same extent as distal joints.
involving orthopedic pathologies
proved 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 articular
performance. The next logical step healthy elderly subjects (mean
receptors.64 –71 For example, Adachi
in 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 the
and 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.59
of weight bearing may influence the
The hypothesis of a distal-to-proximal
level 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 shown
February 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, and
The cutaneous receptors. The superficial fine touch receptors have small receptor alpha motoneuron activity.78
fields and include the Meissner’s corpuscles, Merkel disks, and hair follicle receptors.
The subcutaneous fine touch receptors have larger receptor fields and include the
pacinian 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 Physiological
located throughout the skin and provide information about coarse touch, pain, and Age-Related Change
temperature. 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 appears
permission 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 In
receptors and neuronal degenera- rence.74 This high prevalence under- addition, due to their relatively large
tion.66 – 68 Animal studies66,67 sug- scores the importance of conducting size, the majority of studies involving
gest that denervation and mechano- clinical trials with older adults with the effects of age on cutaneous
receptor loss actually precede joint lower-extremity OA, proprioceptive receptor decline have involved PCs
degeneration 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 evidence
pared against healthy controls,65 and that human PCs decrease in number
knee 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 by
postural instability,38,72 and increased The cutaneous mechanoreceptors physiologic studies, such as that of
risk for falls.73 Radiographic evidence that innervate glabrous or hairless Verrillo,81 which have shown that
of knee OA has been demonstrated skin are the rapidly adapting Meiss- vibrotactile sensitivity involving PC
in more than 30% of the population ner’s corpuscle (MC), the slowly pathways becomes impaired with
over 60 years of age, and it has been adapting Merkel disk, rapidly adapt- age. More recent work has shown
suggested that radiography may un- ing PC, and the slowly adapting that, at a vibration frequency of 250
200 f Physical Therapy Volume 87 Number 2 February 2007
9. Aging of the Somatosensory System: A Translational Perspective
Table 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 testing89–92
Hz (resulting in preferential activa- times over those of young control Cutaneous
tion of PCs), older adults who were subjects. Somatosensation:
healthy (n 5, mean age 68.6 years) Clinical Age-Related Change
required 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 receptors
19.2 dB) to achieve the same ner’s receptors are reduced in num- with age, multiple studies77,81,82,86 – 88
sensation-perceived magnitude as ber with aging. In addition, both have demonstrated that older adults
younger 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 and
Meissner’s corpuscles also exhibit of Bolton et al,83 the vast majority of monofilament sensitivity in young
structural modifications and an physiological research involving MCs adults (n 7, age 23–26 years) and
overall 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 metatarsal
et 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 and
als ranging in age from 11 to 89 2002 report by Kennedy and Inglis76 100 Hz) and monofilament testing
years. 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 the
the great toe and little finger MC years), who were healthy. Microneu- young adults. When analyzing results
mean concentrations (number of rographic recordings of the tibial only from older adults ( 65 years of
MCs/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 seventies
index 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 not
between 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 concluded
from this study also demonstrated the large degree of dynamic sensitiv- that vibration perception threshold
a significant weak-to-moderate corre- ity that is needed for proper weight testing may provide a more sensitive
lation 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 These
Bruce 85 combined histological and this theory and the degree of lower- findings,77 combined with previous
sensation testing and determined extremity cutaneous receptor de- research,81,82 support the view that
that older adults not only had cline that is associated with im- older adults lose vibratory sensation
decreased MCs in the index finger, paired balance. with age and that vibratory testing
but also exhibited impaired touch should be considered when screening
thresholds that were elevated 21⁄2
February 2007 Volume 87 Number 2 Physical Therapy f 201
10. Aging of the Somatosensory System: A Translational Perspective
for 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 40
effect 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 al86
main 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 Sensory
Discriminative touch (ie, 2-point sen- extremities of subjects over 80 years
sation) has been found to be com- Innervation: Anatomical, of age. As compared with young
promised with aging.89 –92 Stevens et Physiological, and Clinical adults (21–29 years of age), older
al92 assessed 2-point gap discrimina- Age-Related Change adults (63– 80 years of age) showed
tion in 5 body regions (volar fore- Mechanoreceptors that summate to significant (P .05) reductions only
arm, 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 that
faces of the forefoot) in 60 healthy within peripheral axons to cell bod- sensory fibers are affected prior to
older 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 years
young adults (18 –28 years of age). tion then travels along the proximal of age) demonstrated significant
Older subjects exhibited an average axons of the DRG into the spinal (P .01) global declines in both
decline in the foot, fingertip, and fore- cord. These steps require healthy motor and sensory nerve conduction
arm 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 and
vious 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 age
greater in the distal extremities.89,90 groups. The age-related increase in
Additionally, there was no significant A reduction in the number and den- the H-reflex latency implies that the
difference between the dorsal and sity of myelinated peripheral nerve spinal reflex loop was delayed,96 and
ventral surfaces of the foot or finger, fibers and a decrease in thickness of other authors97 have postulated that
providing 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 a
tear 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 clinical
finger.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 improved
that a recent study identified that the that myelin thickness, the number of laboratory techniques for counting
loss of 2-point sensation in the plan- large myelinated fibers, and sensory neurons challenges this idea.99,100
tar aspect of the toe was significantly NCV actually increase in young mice Recent experiments that analyzed
greater in “fallers” than in “nonfall- up to 12 months of age. In mice 12 to the total number of neurons from
ers.”91 The researchers conducted 20 months of age (middle to early old the cervical and lumbar DRGs of
balance 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%) decrease
years, 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 the
124 nonfallers (mean age 77.8 and fiber thickness, and sensory degree of sensory neuron loss and
years, 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 older
eral sway (28% more sway) and NCV and sensory nerve action po- rats exhibited significantly smaller
impaired 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 that
SD 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 Perspective
However, 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 may
rats with respect to unmyelinated opposed to lost also provides foun- exist between exercise duration and
DRG neurons.99 These findings pro- dational justification for examining neuronal outgrowth.109 Similar lines
vide some evidence to suggest that the influence of therapeutic inter- of research involving healthy aged
aging predominately results in atro- ventions (eg, exercise, sensory re- animals and those with neuropathy
phy of myelinated primary sensory education, modality application) on may provide additional evidence of
neurons. 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 a
analysis 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 patients
rats with DPN and healthy age- the treatment of people with dia- with polyneuropathy.
matched controls, but once cells betic peripheral neuropathy. Future
were grouped based on size, large research may focus on identifying
myelinated 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- Change
trols. 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 used
sis) than normal aging (cell atrophy, involves the influence of neurotro- CDP and other clinical examination
but 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. Judge
testing 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 CDP
tion, discriminative touch) may pro- reduction of neurotrophins within sensory organization test (SOT) and
vide the most sensitive measures for the skin and neurotrophin receptors found that errors in proprioception
identifying and discriminating sen- in primary sensory neurons is associ- had a greater effect on balance than
sory impairments due to aging ver- ated with aging and may contribute did errors in vision, with the oldest
sus 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 where
supports this concept, as deficits in rotrophins also play an essential role proprioception was reduced.
sensory testing domains (Achilles in activity-dependent plasticity and
reflex testing, 128-Hz vibration tun- are enlightening our understanding Using CPD, Peterka and Black113
ing fork testing at the great toe, or of how exercise influences the ner- found that balance equilibrium scores
JPS at the great toe) accurately vous system. For example, following for older adults up to 80 years of age
separated older adults with and with- a nerve crush injury, DRG neurons exhibited substantial changes only
out 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. Camicoli
ence of abnormal testing in 2 out of levels of neurotrophins and showed et al114 examined 48 healthy older
3 of these domains identified distal improved axonal regeneration (P subjects (33 subjects 80 years of
peripheral neuropathy with a sensi- .01 at 3 days; P .0001 at 7 days) age [mean age 88 years, SD 5] and
tivity of 94.1% and a specificity of when compared with sedentary ani- 15 subjects 80 years of age [mean
88.4%.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 Perspective
mance (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 significant
difference 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 than
older) 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 linking
available, 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 lower
maintain 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 demonstrative
oceptive errors by using visual cues. boundaries on steps and curbs. Al- These conclusions highlight the
ternately, these results combined importance of using and refining
Sensory 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, and
cline 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 within
between 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 for
old adults (mean age 89 years, tory strategies. These findings also additional research examining the
SD 4.3) and found that vibration emphasize the importance of distin- physiological changes that occur in
sense (big toe), balance (Romberg guishing between young-old and old- sensory structures and function over
test, 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 older
paired in the oldest participant group. amination and intervention strategies. adults.
Similarly, Anacker and Di Fabio116
found that time to fall while standing Both authors provided concept/idea/project
on a compliant surface (eyes open Summary and Conclusions design, writing, and consultation (including
and 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 contained
in a group of similarly aged older emerged in our review of the influ- herein are the private views of the authors
adults (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 the
SD 9), the reliance on accurate sensory systems:
Army or the Department of Defense.
proprioception information was
increased in fallers. (1) A diverse and nonuniform This article was received March 14, 2006, and
was accepted September 25, 2006.
decline of sensory structure and
Finally, Lord and colleagues15,17,36 physiological function occurs 10.2522/ptj.20060083
have shown that lower-limb propri- across the life span, with evi-
oception is significantly reduced in dence of accelerated declines
older adults with a history of falling. with advanced aging. References
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