Download Proprioception - e

eBooks
Proprioception: The Forgotten
Sixth Sense
Chapter: Exercise and Proprioception
Edited by: Defne Kaya
Published Date: April, 2016
Published by OMICS Group eBooks
731 Gull Ave, Foster City, CA 94404, USA
Copyright © 2016 OMICS Group
All book chapters are Open Access distributed under the Creative Commons Attribution
3.0 license, which allows users to download, copy and build upon published articles
even for commercial purposes, as long as the author and publisher are properly credited,
which ensures maximum dissemination and a wider impact of our publications. However,
users who aim to disseminate and distribute copies of this book as a whole must not seek
monetary compensation for such service (excluded OMICS Group representatives and
agreed collaborations). After this work has been published by OMICS Group, authors have
the right to republish it, in whole or part, in any publication of which they are the author,
and to make other personal use of the work. Any republication, referencing or personal use
of the work must explicitly identify the original source.
Notice:
Statements and opinions expressed in the book are those of the individual
contributors and not necessarily those of the editors or publisher. No responsibility
is accepted for the accuracy of information contained in the published chapters.
The publisher assumes no responsibility for any damage or injury to persons or
property arising out of the use of any materials, instructions, methods or ideas
contained in the book.
A free online edition of this book is available at www.esciencecentral.org/ebooks
Additional hard copies can be obtained from orders @ www.esciencecentral.org/ebooks
I
eBooks
Exercise and Proprioception
Filiz Can*
Hacettepe University, Faculty of Health Sciences, Deaprtment of Physical Therapy
and Rehabilitation, Orthopaedic Unit, Samanpazarı, Ankara, Turkey
*Corresponding author: Filiz Can, PT, PhD, Full Proffesor, Hacettepe University,
Faculty of Health Sciences, Deaprtment of Physical Therapy and Rehabilitation,
Orthopaedic Unit, Samanpazarı, Ankara, Turkey, E-mail:[email protected]
Abstract
Proprioception is the afferent information to the central nervous system provided by
specialized nerve endings called mechanoreceptors that contributes to the conscious and
unconscious sensation, automatic control of movement, posture, and balance. Over the
years, proprioception has been put forward in many different views on the origin part
of the studies. The results of the studies from the literature have been mostly based on
physiological basis of propriception, testing procedures, loss of proprioception with aging,
degenerative joint disases, injuries or surgical interventions.
Proprioception contributes to the motor programming for neuromuscular control required
for precision movements and also contributes to muscle reflex, providing dynamic joint
stability. Therefore, exercise seems crucial for rehabilitation of the proprioceptive defisits or
loss of proprioception. Although proprioceptive or kinesthetic exercises are mostly included
in therapeutic exercise programs for treating upper or lower extremity injuries, there is still
lack of evidence based information about effect of exercise on proprioception.
This chapter aims to explain possible effects of exercise on proprioception and to discuss
the literature results related with proprioception using various type of exercises. This
paper enlightens the latest views on the role of exercises peripheral afferents and central
signals involved in the proprioceptive system. The sections describes in details the effect
of different muscle contraction types like isotonic, isometric, isokinetic on joint position
sense and kinaesthetic sense. It also describes relationship between proprioception and the
most common exercises such as strengthening exercises or resistive exercises, stretching
exercises, close kinetic chain exercises, proprioceptive exercises, pliometrics and Tai Chi.
Keywords:
Proprioception
Exercise; Joint Position Sense; Kinaesthetic Sense; Motor Control;
Introduction
Although much of therapeutic intervention is focused on the restoration of safe effective
function by improving movement capabilities, it must be remembered that efferent and
afferent systems work very closely together to achieve this goal. Somatosensation is the
sensory system most closely linked with motor activity. Somatosensation refers to tactile
1
sensation (simple touch and tactile discrimination) and proprioception or position sense.
Proprioception is a sensation that encompasses sensation of joint motion or acceleration
(kinesthesia) and joint position sense. Proprioception is the sense of the position of body
parts in space; kinesthesia refers to the sense of body movement [1,2].
Definition of proprioception an afferent input from proprioceptors – the sensory organs,
which are activated and transmit afferent information about mechanical stimuli generated
within musculoskeletal framework. These terms have been interchanged widely in the
literature. It has been referred to proprioception as an awareness of the position and/or
movement of the body. This includes the position of the body with respect to gravity, and the
position of one body part relative to another. It also includes information about the degree
of angulation of all joints in all planes and their rates of movement [2-4].
Proprioceptive sensation includes position, displacement, velocity, acceleration,
muscular effort (force) and/or sense of heaviness.
Proprioceptive deficits have been associated with aging, arthrosis, anterior cruciate
ligament disruption, ankle sprains, shoulder injuries, and back pain. Kinesthetic sensibility
is also decreased by fatigueness [4-9].
Damage to joint connective tissue may result in disruption of afferent mechanoreceptors
and impairment of proprioception. Data about movement is conveyed to the nervous system
via proprioception, exteroception (light touch, pain sensation), audition, vision, and the
vestibular system. Information from a multitude of receptors is integrated in the route or
in the central nervous system. The sensory and motor systems are intimately intertwined.
Each voluntary movement requires ongoing adjustments to compensate for limb inertia and
mechanics. This helps to ensure an appropriate, accurate movement outcome, and includes
a continuous flow of sensory information about the position or orientation of limbs and
the degree of muscle contraction, thus contributed to proprioception. Articular ligaments
perform more than a mechanical function; they provide neurological afferent feedback that
directly mediates joint position sense and muscular reflex stabilization about the joint. In
other words, articular ligaments contribute to proprioceptive sense.
Information about joint position and movement is derived in the periphery from a
number of different sources. These sensory receptors include the muscle spindle, Golgi
Tendon Organ (GTO), joint receptors, and cutaneous receptors. These receptors function as
an orchestra in which different receptors respond to different thresholds of stimulation, so
there is a constant flow of information about joint position and movement. Feedback from
the periphery is essential for certain types of movement [2-4].
Muscle Receptors and Proprioception
The sense of limb position, it is generally agreed, is provided by signals from skin, joint
and muscle receptors. The muscle receptors responsible include the primary and secondary
endings of muscle spindles, primary endings being concerned with signalling position and
movement, secondary endings largely signalling position [4-10].
The primary receptor for proprioception is the muscle spindle. Thus, motor actitivity
of the muscle will effect muscle spindle. In general, the muscle spindle is a very sensitive
muscle length detector capable of providing critical information for determining position
and motion of body segments.
Muscle spindles are distributed throughout skeletal muscle and attach to the tendon
or a muscle fiber. Spindles have two types of afferent endings, primary or Group Ia,
and secondary or Group II. When a muscle spindle is stretched, both types of endings
are stimulated. The primary endings are sensitive to changes in the length of the muscle
and changes in the rate of stretch (dynamic). Secondary endings are most sensitive to the
length of the muscle (static). Recall that muscle spindles have their own intrafusal muscle
fibers that are innervated by gamma motor neurons. Gamma activation works to shorten the
2
intrafusal fibers on either end of the central portion. Since muscle spindles are stimulated
only by stretch, the intrafusal fibers help to keep the spindle on stretch even when the skeletal
muscle is shortening. Such innervation ensures the sensitivity of the spindle regardless of the
state of the muscle — shortening, lengthening, or static. Via polysynaptic connections, the
muscle spindle helps to modulate the alpha motor neuron that supplies its muscle, facilitates
agonist muscles, and inhibits antagonist muscles. It also provides ongoing peripheral feedback
to the central nervous system, as described earlier [4,11].
Golgi Tendon Organs (GTO) are found in the muscle tendon near the musculotendinous
junction. They are sensitive to tension and the rate of change of tension, and provide feedback
about muscle force [2-4]. Golgi Tendon Organs (GTOs) are sensory receptors located at the
junction between muscle fibers and tendon. They are connected in series to a group of skeletal
muscle fibers. Stretching of the GTO straightens the collagen fibers, thus compressing the
nerve endings and causing them to be activated. Whereas muscle spindles are most sensitive to
changes in muscle length, GTOs are most sensitive to changes in muscle tension [5,11].
Therefore muscle spindles are more sensitive to muscle length, whereas GTOs respond more
to tension and force. During motor tasks, muscles will change length and/or create tension,
which activates proprioceptors to help monitor joint motion. Such information is conveyed to
the central nervous system via conscious and unconscious systems. Information is carried from
the periphery into the dorsal horn of the spinal cord. Conscious proprioception travels along
with tactile discrimination via the dorsal column-medial [4].
Rymer and D’Almeida suggest that afferent discharges from the GTO as a result of muscle
force contribute to proprioception [12]. Dietz and Duysens showed that the GTO significantly
contributes sensory information to the regulation of stance phase of gait cyclus and all gait
pattern [13].
Periarticular mechanoreceptors (ligament and capsule) and cutaneous mechanoreceptors
provide secondary proprioceptive information. Movement enhances kinesthetic acuity, indicating
a primary role of muscle spindles. However, it must be noted that there are varying types and
amounts of proprioceptive information avaliable to the Central Nervous System (CNS) and this
sensory information may be dealt with in a manner that will provide the relevant information for
the determination of segment position and motion for a particular task [2,3,5].
Proprioception and motor control
Proprioception is the afferent information to the Central Nervous System (CNS) provided
by specialized nerve endings called mechanoreceptors that contributes to the conscious
and unconscious sensation, automatic control of movement, posture, and balance [14,15].
Proprioception plays an important role in moderating the function of the muscles. Intact
joint position sense enables joint stabilization and appropriate muscle activation resulting in
smooth motion [2,5,16]. According to the studies of Lephart and others, both conscious and
unconscious proprioception are essential for proper joint function in sports, for activities of
daily life, and for some occupational tasks as well as for reflex stabilization [12,15].
Proprioception contributes to the motor programming for neuromuscular control
required for precision movements and also contributes to muscle reflex, providing dynamic
joint stability [16].
Proprioception describes the awareness of posture, movement and changes in equilibrium
and the knowledge of position, weight, and resistance of objects in relation to the body [5,14].
Proprioception would seem to be a complex sensory function for processing kinetic and
kinematic information from the trunk, head, and limbs, conveyed to and processed at all
levels of the Central Nervous System (CNS) resulting in accurate placement and movement
of body segments in space. As a sensory system, proprioception appears to provide an
important mechanism that contributes to motor control [5,11,16].
3
At the spinal level the motor control is presented as a direct response – reflex activity to
the efferent input from proprioreceptors. The proprioceptive signals arriving to the dorsal
horn can directly synapse to either ALPHA or GAMMA motor neurons giving a reflex activity
at the muscle [2].
Motor control system focuses on the collaboration of multiple systems to achieve a
targeted movement or movement tasks (Figure 1). Participating systems for motor control
vary depending on the task and goal. Most crucial systems for motor control are sensorimotor
system, musculoskeletal system, central nervous system or regulation system in addition to
commanding, comparing and enviromental systems [5].
Control of human movement, including volitional actions and responses to perturbations,
is mediated at all levels of the CNS, utilizing peripheral sensory information to monitor
movements tasks in an efficient and effective manner. Sensory organs in cutaneous,
articular, and musculotendinous tissues provide peripheral sensory information or inputs
about the relative motion and position of body segments during static and dynamic activity.
Sensorial inputs provide information to effect limb positioning, balance, and posture during
normal human movement [2,15,16]. Balance requires the continuous adjustment of muscle
activity and joint position to retain the body’s center of gravity over the base of support
[11,17]. Regarding balance, proprioception is paramount to its sensory control [14,16].
Therotically, joint proprioception is essential for accurate modulation and activation
of muscles, thus providing adequate neuromuscular control of joint position and joint
movement, and ultimately the performance of physical tasks. When proprioceptive acuity
decreases, functional ability can only be maintained if there is sufficient muscle strength to
compensate for the decrease in accuracy of modulation and activation of muscles.
This implies that functional ability may be more strongly affected in the presence of both
proprioceptive inaccuracy and muscle weakness [18,19].
Commanding
System
Central
Nervous System
or
Regulation System
sSSysteSystem
Movement
or
Task
Comparing
System
Enviromental
System
Musculoskeletal
System
Sensorimotor
System
Figure 1: Motor Control System for human movement.
Therefore, damage to the proprioception system is thought to be the major causes of
functional instability. Trauma to ligamentous tissues that contain mechanoreceptors may
result in partial deafferentation, which can lead to proprioceptive deficits and subsequently
contributes to functional instabilities [15,16,19,20].
Greater proprioceptive loss may be observed in older adults with lower physical ability
levels. Decreased proprioception in the lower extremities increases body sway, which in
older adults may increase the risk of falling. Furthermore, strong relationships between hip
proprioception error, postural sway, and fear of falling in older adults with greater mobility
impairments may be observed [4,7].
4
The decrease of joint proprioception can also lead to abnormal joint biomechanics during
functional activities which could lead to, over a period of time, degenerative joint disease
[9,21]. In the study of Erdem and Can (2007), the patients with cervical spondylosis have
shown decreased or diminished joint position sense compared with the healthy individuals.
They have found that there is positive relationship between cervical spondylosis and error
in joint position sense while there is negative corelation between muscle strength and error
in joint position sense. The results of this study has proven the negative effect of decreased
proprioception on normal joint biomechanics resulted with degeneration of the joints [22].
Erden has also revealed that osteoarthritis in knee joint influences joint position sense
negatively and knee arthroplasty surgery decreases joint position sense and kinesthetic
sensation [21].
In a study on knee joint laxity in osteoarthritis [18], patients with high knee joint
laxity showed a stronger relationship between muscle strength and functional ability
than osteoarthritis patients with low knee joint laxity. Patients with poor proprioception
showed more limitation in their functional ability, but this relationship was rather weak. In
patients with poor proprioception, muscle weakness had a stronger impact on limitations
in functional ability than in patients with accurate proprioception. This suggests that high
knee joint laxity and impaired proprioception have a similar influence on the relationship
between muscle strength and functional ability [23].
The loss of neuro­
muscular control results from damage to the mechanoreceptors
within the capsuloligamentous structures of the joint and from interruption of the afferent
sensory pathways that play a crucial role in producing smooth, coordinated movement [16].
Knowlodge of the basic physiology of how these muscular and joint mechanoreceptors work
together in the production of smooth controlled cooordinated motion is critical in developing
a rehabilitation training program [4,5,11].
Physical Activity and Proprioception
It is well established that physical activity contributes to improved health in elderly
individuals [21] but it is unclear whether similar benefits apply to proprioceptive function.
There is some evidence that the ability to use proprioceptive feedback about the ankle
joint is enhanced in physically active older adults [24].
Preliminary evidence provides further support for the notion that age related declines in
proprioceptive function may be ameliorated by a physically active lifestyle. These findings
also under score the importance of taking into account general physical activity levels when
measuring sensorimotor performance in older populations [25-27].
The results taken from the literature provide valuable information changes in regarding
movement-related proprioception in older adults. Not only do the findings extend our
understanding regarding the extent of age-related proprioceptive declines, but provide
preliminary evidence of the value of physical activity in maintaining somatosensory function.
These results show clinical value of the physical activity [24,25,27].
However, the beneficial effect of regular exercise on lower limb proprioception of older
adults is not consensual. It seems that only the regular practice of forms of exercise
emphasizing awareness of joint position and movement, such as Tai Chi, and not the most
common exercises practiced in the Western society, such as walking, jogging, running and
swimming improve proprioception [24,26,28-30].
Although there are limited studies showed effect of physical activity on proprioception,
the studies on this topic have suggested that lower extremity proprioception can be
increased with physical activity [24,28,29] and that proprioceptive training can improve
balance [7,28,29].
5
Effects of Exercise/ Exercise Training on Proprioception
The use of specific proprioceptive or kinesthetic exercises as a component of therapeutic
exercise for rehabilitation has been advocated for many musculoskeletal dysfunctions,
especially in the lower extremity, as an important means of adressing proprioceptive deficits
and restoring normal function after injury and surgery [1,15,31].
Studies have shown that kinesthetic sensibility is decreased by fatigue [9,32,33] and
increased by long term physical exercise [24,26,34]. Thus, proprioceptive or kinesthetic
exercises are commonly recommended as an indispensable component of therapeutic
exercise programs for improving propriception after injury and/or preventing re-injury
[1,31]. For these purposes proprioceptive or kinesthetic exercises are mostly included in
therapeutic exercises programs for treating upper or lower extremity injuries [5].
While many therapeutic exercise programs emphasize proprioceptive or kinesthetic
training as a necessary component for restoration of normal function [15,35], the evidence
is unclear as to whether reported proprioceptive deficits actually result in clinically or
functionally significant movement deficits [30]. Hovewer, there is little evidence to suggest
that proprioception, as determined by reproduction of position or threshold to detection of
passive motion, can be improved by specific proprioceptive exercises.
According to Hurley hyphothesis, abnormal articular afferent information may decrease
α- motoneurone excitability following joint damage, reducing voluntary muscle activation.
If joint damage is extensive, the resulting large reduction in activation may prevent
the threshold for stimulation of muscle hypertrophy from being reached, which impedes
rehabilitation. Abnormal articular afferent information may also decrease γ-motoneurone
excitability causing proprioceptive deficits. Rehabilitation which increases α- motorneurone
excitability, improving proprioception [8].
Ashton-Miller et al., have investigated proprioception and effetcs of proprioceptive
therapeutic exercises and they have concluded that current exercises aimed at improving
proprioception have not been demonstrated to achieve that goal [30]. Hovewer, it is clear
that sensory information from the muscle spindles of muscles involved in movement to
contribute to movement control at all CNS levels [5]. In general, motor commands are
noted to be modifiable via muscle spindle input throughout the CNS, while signals from
joint and cutaneous receptors provide sensory information at subcortical levels. Combined
information from these receptors about position and motion, both during or after motion,
provides a basis for efficiency and plasticity of the motor control system in regulating goaloriented movement for a given task within a specific environment. Whether therapeutic
exercises modify these mechanoreceptors either morphologically or neurologically, is a
question that still needs to be answered [5]. No studies have directly measuered the effects
of specific proprioceptive training protocols on measures such as reproduction of position
and threshold to detection of passive motion at the knee joint.
Hovewer, it is widely acknowledged that regular physical exercise promotes beneficial
effects in many physiologic systems. Regarding proprioception, the results from the
literature support the valuable role of physical exercise performed on a regular basis in the
attenuation of the age related decline of knee position sense [14,36]. Ribeiro F et al., have
examined the effects of age and regular exercise on knee proprioception assessed through
measurement of joint position using active positioning sense in their study. Older subjects
have been trained with aerobic, flexibility and strengthening exercises while young subjects
have practiced soccer or volleyball with a frequency of three times a week for at least 45–60
minutes. At the end of the stuy, they found that regular physical exercise has a positive
impact on knee joint position sense both in younger and older subjects. They also revealed
that age has a deleterious effect on knee joint position sense and regular physical exercise
can attenuate the age-related decline in knee position sense [14].
6
Several mechanisms by which exercise ameliorates joint proprioception can be point
towards based on the best evidence available. Since central and peripheral components of
proprioception are implicated in the proprioceptive age-related decline, it is not surprising
that they are also both involved in the improvement of proprioception observed in result of
engagement in regular physical exercise. At peripheral level exercise induces morphological
adaptations in the muscle spindle. There are adaptations on a microlevel, the intrafusal
muscle fibers could show some metabolic changes, and on a more macrolevel, the latency of
the stretch reflex response decrease and the amplitude increase [27].
At central level, exercise can modify proprioception through the modulation of the muscle
spindle gain and the induction of plastic modifications in the central nervous system. During
physical exercise there is an increase in the muscle spindle output through γ (gamma)
route, hence enhancing proprioception by facilitating its cortical projection. Thus, regular
exercise can increase the muscle spindle output, which could induce plastic changes in
the central nervous system, such as increased strength of synaptic connections and/or
structural changes in the organization and numbers of connections among neurons. The
demands of regular exercise and more specifically regular and repetitive afferent inputs
from the mechanoreceptors could be able to induce plastic changes in the cortex hence
modifying the cortical maps of the body over time (increasing the cortical representation of
the joints leading to enhanced joint proprioception [2,30]. At peripheral level exercise induces
morphological adaptations in the muscle spindle. There are adaptations on a microlevel, the
intrafusal muscle fibers could show some metabolic changes, and on a more macrolevel, the
latency of the stretch reflex response decrease and the amplitude increase [37].
Ribeiro and Oliveira have suggested that: (i) regular physical exercise has a positive
impact on knee joint position sense both in younger and older subjects; (ii) age has a
deleterious effect on knee position sense; and (iii) regular physical exercise can attenuate
the age-related decline in knee position sense [14].
Active and Passive exercises in proprioception
Based on current neurophysiologic findings, active and passive motions throughout a
joint’s range of motion should elicit appropriate levels of sensory input from cutaneous,
capsuloligamentous and, musculotendinous mechanoreceptors. Active exercises at all
levels of intensity will elicit appropriate sensory input from proprioceptors in the muscle,
providing information for motor skill performance [5].
The exact mechanism of how proprioceptive input from these receptors influences motor
output are complex and various models exist that might explain the process involved [5].
Any number of exercises will elicit proprioception training based on the fact that
deformation of the joint mechanoreceptors occurs with active, active assisted, and passive
movements and provides sensory input to improve neural mechanisms [16].
Performing Range of Motion (ROM) exercises on an immobilized joint and weight
shifting early after an ankle sprain or surgery on the ACL are examples of early forms of
proprioception training [15,38].
Friemert et al., (2006) examined the effects of active motion and passive motion on
joint position sense in patient with anterior cruciate ligament injury post-operatively. They
found significant improvements in joint position sense when compared with joint position
sense pre-operatively after continuous active motion exercise. The joint position sense also
improved after performing repetitive passive motion via continuous passive motion device,
although the results did not reach a significant level. They claimed that the improvement
might come from additional physical therapy sessions [39].
Contrary to this result, another study results showed a statistically significant increase
in absolute repositioning error following repetitive active movement, but a decrease
7
following repetitive passive movement intervention. The subjects have performed passive
movement with 60 repetitive knee flexion–extension at a speed of 120˚/s. In doing passive
movement with this velocity, stretch reflexes might be elicited from the rapid movement of
the knee joint. This fast repetitive movement would also impose stretch onto joint capsules,
and cause stimulation and facilitation to the muscle and joint mechanoreceptors. This
study concluded that a repetitive passive movement protocol is capable of improving knee
joint position sense. Meanwhile, the negative effect from the muscle receptors following
the repetitive active movement overwhelms the positive effect from the repetitive passive
movement intervention. It supports the clinical utilization of repetitive passive movement to
promote proprioception. This utilization can be implemented for proprioceptive training in
sports activities, plus injury prevention and rehabilitation [40].
Strengthening / Resistive exercises and proprioception
In clinical practice, rehabilitation is often intended to increase muscle strength and
to enhance proprioceptive function [41]. It has been well documanted that the exercise
enhances motor performance levels in the individuals [42]. Due to enhanced motor
performance level with the exercises, joint position sense can be improved after exercise.
Whatever the mechanisms involved, enhanced motor performances after exercise can be due
not only to improved mechanical properties of the muscles, but also to better kinesthetic
sensibility [43].
Ankle strengthening exercises were found to improve inversion and plantarflexion joint
position sense in functionally unstable ankles. This may be a result of stimulation of joint
mechanoreceptors by the actual movement or a response of the receptors to the extremes in
range and local compression [42].
Hung-Maan Lee et al., found that Threshold for Detection of Passive Motion (TTDPM)
strongly correlated with dynamic single-limb stance balance in patients with Anterior
Cruciate Ligament (ACL) injuries. By contrast, dynamic single limb stance balance in these
individuals did not show significant correlation with knee laxity or the strength of the knee
muscles. Rehabilitation programs that improve TTDPM proprioceptive ability, therefore,
represent the most important approaches to improving dynamic single-limb stance balance
in patients with chronic ACL injuries [44].
Wong and Ng, examined and compared two modes of weight training (body building and
power-lifting) on the surface EMG of vasti muscles and knee joint position sense. The weight
training programs over a period of 8 weeks with 3 sessions per week were continuous,
repetitive and non-explosive. A comparison of the pre- and posttraining measurements in
both groups has revealed an improvement in knee joint proprioception [45].
Bouët and Gahéry have studied to determine how physical exercise may lead to changes
in perception of limb position, i.e. changes in accuracy of position sense. Exercise consisted
of pedaling during 10 min on a cycle ergometer. Their objective was to obtain warm-up
without any fatigue, so the subjects had to pedal at their own sustained and regular rhythm
without any imposed cadence as they aimed to give moderate muscular exercise. At the end
of the study, they have stated that position sense is improved after a moderate muscular
exercise. This enhancement was observed with a kinesthetic evaluation mode and an active
positioning of the reference leg. These original data, therefore, show that moderate exercise,
which clearly improves muscle performances can also act on the sensory systems by
improving kinesthesia. The well known improvement of motor performances after exercise
could then be due not only to improvement of mechanical properties of muscular tissue, but
also to better kinesthetic sensibility [43].
Closed Kinetic Chain (CKC) exercises
CKC or weight bearing exercises have been shown to increase muscle strength and
neuromuscular control of the lower extremity in young athletes [15,38].
8
To facilitate appropriate kinesthetic and propriceptive information to the central nervous
system, joint reposition exercises should be used to provide a maximal stimulation of the
peripheral mechanoreceptors. The use of close kinetic chain activities creates axial loads
that maximally stimulate the articular mechanoreceptors via the increase in compressive
forces. (Figures 2 and 3). The use of Closed Kinetic Chain (CKC) exercises not only enhances
joint congruency and neurosensory feedback but also minimizes the shearing stresses about
the joint. At the same time, the muscle receptors are facilitated by both the change in the
length and tension [11].
Figure 2: CKC exercise (Leg-Press).
Figure 3: CKC exercise (Mini-Squat).
Under different loading positions and angles, biomechanical properties of the knee
can affect the proprioceptive responces. Numanoğlu has tested joint position sense of the
knee under different loading positions and angles of the knee included CKC positions/
exercises in the patients with Patellofemoral Pain Syndrome (PFPS). The measurement has
been taken during supine and prone position, sitting, squatting and leg-press positions/
exercises at the angles of 30˚, 45˚, 60˚ and 90˚ which were CKC positions/exercises. Acuity
of the joint position sense in the patients with PFS has deteriorated in prone position and
sitting position compared with the healthy individuals. Error in joint position sense was
higher in squatting position/ exercise than in leg- press position/ exercise in the PFPS
patients. They concluded that PFPS inhibits of the knee joint position sense. Considering
the results of joint position sense under different loading positions, leg-press positions/
exercises which is the position/ exercise of CKC were safer and favorable position/exercise
for the patients with PFPS [46].
Exercises that produce approximation of the glenohumeral joint and are characterized by
a fixed distal aspect of the extrem­ity are typically referred to as joint approximation or CKC
9
upper extremity exercises. The approximation of the joint surfaces and the multiple joint
loading inherent in CKC exer­cises are reported to increase mechanoreceptor stimulation
[16,47] and produce muscular cocontraction.
The presence of muscular co-contraction around the human shoulder is particularly
beneficial because of the important role that the musculature surrounding the scapulothoracic
joint plays in stabilizing and controlling movement of the shoulder [48,49].
Jan MH et al., have studied the effects of weight-bearing versus nonweight-bearing
exercise on function, walking speed, and position sense in participants with knee
osteoarthritis. Simple knee flexion and extension exercises (weight bearing and nonweightbearing exercises) performed over 8 weeks have resulted in significant improvement in
the knee function scale (WOMAC) and knee strength compared with the control group. They
found that nonweight- bearing exercise alone may be sufficient enough to improve function
and muscle strength. However weight bearing exercises have given additional benefit to
improve joint position sense, which may enhance complex walking tasks (walking on figure
of 8 route and spongy surface) [50]. In addition to weight bearing exercises, thus, joint
repositioning exercises can be used to enhance the conscious appreciation of propriception
[11].
Previously, CKC exercise has been shown to enhance proprioceptive performance [41].
Hurd et al., [51] and Hilberg et al., [52] also reported that CKC exercise alters muscle
activity, leading to normal quadriceps - hamstrings balance and increased joint reposition
acuity. CKC exercise is thought to enhance knee joint proprioception by increasing intraarticular pressure and thereby stimulating Ruffini nerve endings, which are sensitive to
changes in intracapsular fluid volume [53].
In another study on Closed Kinetic Chain (CKC) exercises versus Open Kinetic Chain
(OKC) exercise in the knee, it has been concluded that CKC procedure maximizes the
contribution of the muscle spindles, as more muscle spindles are activated during eccentric
work. CKC allows proprioceptive feedback from adjacent joints, namely the hip and ankle,
which could contribute to determine the position sense of the knee. CKC procedure requires
more eccentric knee extensor strength to control the movement than the OCK procedure,
thus recruiting more motor units, hence activating more muscle spindles. Additionally,
important afferent information could be added in CKC by Golgi tendon organs, which are
more activated in this procedure as a consequence of the increased tension generated by
the knee extensors [54].
Warm-up exercises and proprioception
Warm-ups and some exercises are found to improve proprioception to considerable
degrees [39,40,55].
Bartlett and Warren (2002) evaluated the effect of four minutes stretching and jogging onto
knee joint proprioception. The results demonstrated an improvement in joint repositioning
accuracy after movement intervention. They concluded that the warm-up exercises
increased the sensitivity of mechanoreceptors around the knee, thereby increasing joint
repositioning appreciation [55]. The warm-up effect might lead to an enhancement of reflex
neuromuscular mechanism, thus causing an improvement in joint position sense [40].
At the peripheral level, warm-up exercises may have positive impact on muscular
receptors function by improving the viscoelastic properties of muscular tissue, enhancing
oxygenation, increasing nerve-conduction rate, and increasing body temperature because
of vasodilatation. At the central the level, warm-up exercises may also contribute to better
position sense accuracy by changing corollary discharges, likely involved in position sense
and/or fusimotor commands and, then, muscle spindle sensitivity [54].
Some studies have reported improvements in the accuracy of knee position sense in
10
Open Kinetic Chain (OCK) after warm-up [55,56]. Hovewer, Magalhães et al., have found
the warm-up program has improved knee joint position sense only in Closed Kinetic Chain
(CKC). Knee joint position sense has been evaluated before and immediately after a warmup program through active repositioning in Open Kinetic Chain (OKC) and Closed Kinetic
Chain (CKC). The standardized warm-up program they have used in their study was 10
minutes long and comprised jogging, jumps, and stretching exercises. The stretching
exercises were applied to quadriceps, hamstring and gastrocnemius muscles. Jogging speed
was approximately 7 km/h. The warm-up program has enhanced knee joint position sense
only in CKC. Since no effects were detected in OKC, the evaluation of the effects of warmup on knee joint position sense using merely an OKC technique would underestimate the
valuable role of warm-up [54].
Stretching exercises and proprioception
It is known that passive muscle stretching may change the electrical and mechanical
properties of the muscle slow muscle lengthening of a muscle-tendon unit (contrary to
fast muscle stretching) decreases spinal reflex excitability, reducing muscle stiffness and
increasing joint range of motion [57,58]. Indeed, the importance of the muscle spindles in
neuromuscular function is well known, being responsible for conveying information regarding
muscle length and rate changes in length [3]. According to this, changes in muscle spindle
sensitivity due to stretching are expected, leading to alterations in sensory information with
an impact on the Joint Position Sense (JPS) and the Threshold To Detect Passive Movement
(TTDPM) [59]. Although, the sensory-motor system is a complex mechanism involving higher
centers of the nervous system to ensure the generation of the correct patterns of muscle
activity [60], it is reasonable to think that the changes in the sensory receptors, for example
from muscle receptors, should lead to a decrement in the joint proprioceptive acuity.
Bjorkland et al., had observed no effect on the sense of shoulder position after a bout
of stretching of the agonist and antagonist muscles of the shoulder complex. Larsen et al.,
[61] also found no differences in the sense of knee position after stretching quadriceps and
hamstring muscles.
Torres et al., has studied to determine if an acute bout of static stretching of the quadriceps
muscle, affects the sense of joint position, the threshold to detect passive movement, and
the sense of force. Thirty young, healthy men had been randomly divided into two groups.
The Stretching Group undergone stretching of the dominant quadriceps muscle, which
comprised ten passive stretches lasting 30 seconds each. None of the measurements has
revealed any significant change between both groups in each assessment moment or between
moments within the groups. They demonstrated that static quadriceps muscle stretching
has no effect on the sense of knee joint position, threshold to detect passive movement, and
force sense, suggesting that stretching does not have appreciable effect on the spindle firing
characteristics and tendon organs activation. Consequently, stretching does not suggest
having sufficient influence on the muscle receptors functioning, which could compromise
joint proprioception. However, the authors belived that stretching exercise might have
fundamental effects on muscle receptors, which could mean that sensory information
conveyed by other receptors is sufficient to maintain normal levels of proprioception [62].
Concentric / eccentric exercises and proprioception
A muscle performs an eccentric contraction when it is used as a brake to slow down motion
of the body and in the process is lengthened while actively contracting. This compares with
the more common, concentric contraction where the contracting muscle shortens. Eccentric
exercise is a major component in downhill walking, descending the stairs, step-down, skiing
and horse riding (Figure 4). Activities which largely involve concentric contractions are
cycling, swimming and rowing. During eccentric exercise contracting muscles are forcibly
lengthened, to act as a brake to control motion of the body. A consequence of eccentric
exercise is damage to muscle fibres [10,63].
11
Figure 4: Eccentric Exercise (Step-down).
Unaccustomed eccentric exercise typically leads to myofibrillar damage, disturbance of
the extracellular matrix and an inflammatory reaction [53,63,64]. The sensation of pain
and muscle stiffness normally begins several hours after unaccustomed eccentric exercise,
reaches a peak 24–48 hours after and may even persist for several days [53,64]. This
phenomenon – Delayed-Onset Muscular Soreness (DOMS) – is associated with prolonged
muscle force loss, reduction of joint range of motion, a sensation of unsteady limbs and
clumsiness in precision movements [10,63,65,66], and impaired proprioception [63,67].
Brockett et al., have stated that both elbow joint position sense and force sense are
disturbed over a number of days by eccentric exercise. The direction of the errors suggests
that receptors responsible for position sense have become less sensitive. Errors in force
estimation suggest subjects perceived the eccentrically exercised muscle to be generating
more force than it really was. It is argued that this is not due to central mechanisms and
a sensitisation of tendon organs is postulated [10]. It has been reported that following the
damage there is disturbance to proprioception, in particular, the senses of force and limb
position [10,63].
By contrast to eccentric exercise, concentric exercise is followed by fatigue, with little
or no evidence of damage [68,69]. Fortier et al., have studied to determine which type of
repetitive muscle contractions induces a greater acute impairment of elbow position sense.
Eleven male subjects have randomly performed 9 sets of 10 voluntary isometric, concentric,
or eccentric contractions on three separate sessions, and a pre- and post-exercise Maximal
Voluntary İsometric Contraction (iMVC). Immediately after the concentric exercise task,
subjects have made significant position matching errors (- 2.6 degrees) by adopting a
more extended position with the indicator arm. The results showed that concentric muscle
contractions impaired position sense to a greater extent compared to isometric and eccentric
contractions and, the authors have concluded that high-intensity concentric exercise
protocol impaired position sense to a greater extent compared to the other types of muscle
contractions [70].
Several studies have shown that immediately after either eccentric or concentric exercise,
the size of errors observed during position- and force-matching tasks increases significantly
[71,72]. Furthermore, these studies show that the degree of matching errors is associated
with the degree of force reduction due to either muscle fatigue or Delayed-Onset Muscular
Soreness (DOMS). Although proprioception can be impaired following both eccentric and
concentric exercise, it appears to be affected more following eccentric exercise [72,73].
This is presumably due to the greater reduction in force following eccentric compared to
concentric exercise [73,74]. After eccentric exercise, the impairment in force lasts for 24–48
12
hours [16,75] and significant matching errors are still observed after 24 hours [72]. Since
maximal force is reduced after exercise, the effort required to support the limb increases,
altering the sense of effort [71] resulting in reduced joint position accuracy. The majority
of studies examining the effects of exercise on proprioception have examined the upper
extremities in non-weight bearing positions [63,73,76].
The mechanism for the reduction in spindle discharge has been proposed to involve a
reflex inhibition of fusimotor neurones by small muscle afferents excited by the metabolic
products of the exercise. It has considered for these findings is that contractures in the
muscle fibres damaged by the eccentric contractions and responsible for the reduced joint
angle will activate some tendon organs. If the tendon organ output of the muscle rises
because of the higher resting tension, this may lead to the perception of a higher level
of force in the muscle than is actually generated and that would produce the observed
tension mismatch. Both joint position sense and force sense are disturbed over a number
of days by eccentric exercise. The direction of the errors suggests that receptors responsible
for position sense have become less sensitive. Errors in force estimation suggest subjects
perceived the eccentrically exercised muscle to be generating more force than it really is. It
is argued that this is not due to central mechanisms and a sensitisation of tendon organs
is postulated. As conclusion, when intensive enough, eccentric exercises typically lead to
impaired sense of position [10,66].
Vila-Chã et al., observed a reduction in maximal knee extension force both immediately
and 24 hours after eccentric exercise. Eccentric exercise of the quadriceps impaired
proprioception of the knee both immediately after and 24 hous after exercise when tested
in a non-weight bearing position. In contrast, eccentric exercise did not affect knee
proprioception when tested in a weight bearing position [77].
Recent studies have shown that immediately after concentric exercise – where no
disruption of muscle spindles is expected - the sense of joint position is also impaired
[73]. Thus the disturbance in proprioception may be attributed to alterations in central
commands rather than to abnormal function of the muscle receptors [76].
To summarise, after a series of eccentric contractions there are large force matching
errors due to three causes:
1. The greater effort required to achieve a given force, as a result of fatigue and muscle
damage.
2. There is an increase in central neural drive, presumably accompanied by an increase
in effort, which lasts for up to 48 hours.
3. There is the influence of Delayed-Onset Muscular Soreness (DOMS) which does not
begin to exert a significant effect until 24 hours after the exercise and which lasts for at
least four days [63].
The fatigue and damage from eccentric exercise led to a change in the effort-force
relationship and this produced the position errors. If the fatigue from exercise changes the
relationship between force and effort, and both position sense and force sense use effort
cues, it comes as no surprise that there is a significant disturbance of proprioception after
strenuous exercise [63]. Since it is known that eccentric exercise is associated with damage
to muscle fibres, it is postulated that this leads to a disturbance of muscle receptors, the
muscle spindles and tendon organs [10].
Plyometric exercises and proprioception
Plyometric exercises describes it as activities of maximal or submaximal effort that
involves stretch-shortening cycle. More demonstrating definition would be the activity where
involved muscle of the joint, first undergoes eccentric contraction immediately followed by
13
forceful concentric one [78].
There are very few studies investigated the effect of plyometric exercise on proprioception.
The proprioception following plyometric training was firstly investigated by Kathleen Swanik.
The results indicate great benefits in proprioception values in female swimmers undergone
plyometric training, compared to the athletes who followed regular training activities [79,80].
In one of the few studies on proprioception and plyometrics, Chan and Can have aimed
to compare the effects of plyometric training versus general strength training on shoulder
proprioception. 30 young, sedentary healthy university students have been recruited to
the study as general strengthening group and plyometric group. Assessments included
strength with hand-held dynamometer (kg), Joint Position Sense (JPS) in open space
measuring accuracy of flexion, abduction angle replication in degrees. JPS of shoulder
rotation was tested in 30˚ internal and external rotation as well as 90% of maximal external
rotation. Kinesthesia was measured as Threshold Till Passive Movement Detection (TTPMD)
in degrees at 30˚ internal and external, and 80˚ external rotation. Following 6 weeks of
trainings, 2 times per week the final testing was carried out. General strength group showed
significantly improved JPS in 30˚ external rotation, whereas plyometric group showed
increased JPS at 30˚ internal rotation and 90% of maximal external rotation. No changes
were observed in TTPMD in general strength group. Plyometric group improved TTPMD in
all angles, 30˚ internal rotation, 30˚ external rotation, and 80˚ external rotation. At the
end of the study, plyometric exercises and general strength exercises have been found to
provide similar increases in shoulder muscle strength in healthy individuals. Despite lack of
differences between the groups in proprioception measurements, plyometric exercises have
seemed to be more effective “relative to initial assessment” in increasing proprioception [81].
Incorporation of plyometric exercises in the last stages of rehabilitation may give additional
benefits, although there is still lack of evidence on efficacy of plyometric exercises on
proprioception due to having very few studies.
İsokinetic exercises and proprioception
For many years, isokinetic exercise is used to strengthen muscles after sport injuries
and to increase muscle performance in healthy athletes. However, there is very few studies
which evaluated the isokinetic exercise intervention in patients with propriceptice deficits.
Marks (1994) utilized 20 reciprocal concentric and eccentric isokinetic quadriceps
exercises as the fatigue exercise. He found a decline in knee joint positioning accuracy after
the intervention in subjects. He stated that since the exercise was performed dynamically at
high speed with no pause, it could maximize the firing of Type 1a muscle spindle afferents.
It has been concluded that exercise-induced contractile fatigue could introduce bias into the
encoding of positional information in a healthy knee [82].
Ribeiro et al., (2007) also found a significant decrease in knee joint position sense after
maximal knee isokinetic contractions at 120°/s on elderly. They concluded that local fatigue
protocol with isokinetic exercises would confound muscle spindle sensibility, thus inducing
errors in joint position sense [83].
Hazneci et al., (2005) have studied to demonstrate the impairment of knee joint position
sense in individuals with patellofemoral pain syndrome and to investigate the effects of
isokinetic exercise on knee joint position sense and muscle strength. A total of 24 male
patients complaining of anterior knee pain caused by overexertion and 24 male healthy
individuals without symptoms have been included for this investigation. Isokinetic exercise
protocol was carried out at angular velocities of 60 degrees/sec and 180 degrees/sec. These
sessions have been repeated three times per week and lasted for 6 wks. At the beginning
and after 6 weeks of knee passive joint position sense, quadriceps and hamstring muscle
strength and pain assessments have been performed. After the isokinetic exercise, passive
reproduction of knee joint position sense for 40 degrees of flexion and 50 degrees of extension
14
in addition to flexion peak torque, extension peak torque, flexion total work, extension
total work and pain score have improved significantly in the patellofemoral pain syndrome
group.They concluded that isokinetic exercises have positive effects on passive position
sense of knee joints, increasing the muscular strength and work capacity. These findings
show that using the present isokinetic exercise in rehabilitation protocols of patients with
patellofemoral pain syndrome not only improves the knee joint stabilization but also the
proprioceptive acuity [19].
Sekir at al., (2007) have investigated the effects of isokinetic exercise on strength, joint
position sense and functionality in recreational athletes with functional ankle instability.
Strength, proprioception and balance have been evaluated by using isokinetic muscle
strength measurement, ankle joint position sense and one leg standing test on 24 recreational
athletes with unilateral functional instability. Isokinetic peak torque of the ankle invertor
and evertor muscles were assessed eccentrically and concentrically at test speeds of 120˚/
s. Isokinetic exercise protocol was carried out at an angular velocity of 120˚/ s. The exercise
session was repeated three times a week and lasted after 6 weeks. At the end of the study,
they have found the isokinetic exercise program used in this study had a positive effect on
these parameters [84]. Regarding all these studies, isokinetic exercise training can have
positive effects on proprioceptive acuity.
Proprioceptive exercises and proprioception
Proprioception is a specialized variation of the sensory modality and encompasses
the sensations of joint movement (kinesthesia) and joint position (joint reposition sense).
Thus, it contributes to motor programming for neuromuscular control and contributes to
muscle reflexes for dynamic joint stability [3,5,15,16]. It is believed that joint proprioception
in lower extremity like ankle proprioception is critical to the balance of the human body
during functional activities such as standing, walking and running. Thus balance activites
are commonly used or recommended as proprioceptive exercises. However, it must be
remembered that balance, i.e., maintenance of the centre of mass within one’s base of
support, is subserved by the somatosensory, vestibular, and visual systems with the primary
system in adults being the sensorimotor system (Figures 5 and 6). If the client’s balance has
been diminished as a results of injury and/or surgery, varied levels of balance activities and
challenges can be included strengthening of the leg muscles [5].
Figure 5: Proprioceptive Exercise (using Wobble Board).
15
Figure 6: Proprioceptive Exercise (using trombolin).
The effectiveness of 4–8 weeks of wobble board training on proprioception, postural
control and perceived stability on functional instability after ankle injuries has been well
documented [85-87]. Lee and Lin have examined the effects of 12-week biomechanical
ankle platform system training on static postural stability and ankle reposition sense in
subjects with unilateral functional ankle instability. The active and passive reposition
senses have been assessed using an isokinetic dynamometer. The mean radius of the
center of pressure excursion has been recorded during single-leg standing with a force
platform. The mean radius of center of pressure on unilateral standing and the absolute
error from pre-selected ankle angle in the functional ankle instability limb have been
significantly reduced after 12 weeks of training. They concluded that these improvements
in postural stability appear to reflect improved neuromuscular ability along with
enhanced functional joint stability, as ankle proprioception also demonstrated the same
positive improvements after training [88].
According to one of the meta-analysis in the literature, proprioceptive exercises may
reduce subjective instability, and improve functional outcomes when included as part
of the rehabilitation of people following ankle ligament injury. However, there was no
consensus on the advantages of including proprioceptive training for the assessment of
swelling, postural sway, joint position sense or recurrent injury rates [89].
Coşkun and Can (2008) have investigated the effects of proprioceptive exercises on
joint position sense, muscle strength and functional level in patients with chronic low
back pain. They recruited 30 patients with chronic low back pain to the study and
divided into two similar groups. Group 1 had only stabilization exercises while Group
2 had proprioception exercises in addition to stabilization exercises. All the patients in
both groups have been treated for 6 weeks, 3 days per week. Active and passive joint
position sense and isometric muscle strength have been measured using Biodex System
Pro 3 Izokinetic System. Peak torque and mean peak torque values have increased in
both groups. However, aquity of passive and active joint position sense were better in the
proprioception group (Group 2) after the treatment. They conclude that proprioception
exercises has beneficial effects for increasing joint position sense in patients with chronic
low back pain. Thus, proprioception exercises can be used to enhance joint position
16
sense in rehabilitation of chronic low back patients. This will also give additional
positive effect to increase the efficacy of stabilization exercsies for low back pain [90].
In the study of Erdem and Can, joint position sense of the wrist joint have been
studied after application of various physical therapy and rehabilitation interventions. 60
healthy individuals have been divided into 4 equal groups as strengthening exercises group,
proprioceptive exercises group, vibration group and control group. Their Joint Position
Sense (JPS) have been tested before and after 3 week’s rehabilitation period. Records of JPS
have been compared with and within the groups. Improvement in joint position accuity in
the wrist joint have mostly seen in the proprioceptive exercises group comparing with the
other groups. This significant difference in the joint position sence has been found at 30˚ of
wrist flexion [91].
A systematic review studied by Cooper et al has investigated the effect of proprioceptive
and balance exercises on people with an injured or reconstructed anterior cruciate ligament.
They showed some evidence for proprioceptive and balance exercises improve outcomes.
İmprovements have been found in joint position sense and proprioception in addition to
muscle strength, knee functions, and hoop testing [92].
As a conclusion, propriceptive exercises have to be inserted in exercise program of the
injured athletes or individuals. Propriceptive exercises are also important for the older
individuals or other individuals who have propriceptive deficits or loss of joint position
sense and kinesthetic sensitivity. Proprioceptive exercises play major role for providing or
restoring dynamic stability and neromuscular control resulted with enhanced propriceptive
inputs.
Stable based (tilt-board, wobble-board, etc) and unstable based equipments (slingboard, Profitter, Euro-glide), gymnasium balls, tromboline or various spring systems as well
sophisticated proprioception and balance devices (KAT, BAPS, etc) can be used for improving
proprioception. Walking or other exercises or on soft cushions or beds, grounds with different
sorts of slopes or softness can be used to stimulate proprioceptors. Proprioceptive exercises
can be initiated using stable bases, then be progressed to the unstable bases exercises.
Late term of rehabilitation, perturbations such as multidirectional resistance to the
board or unexpected body or limb perturbations can also add to sensory inputs utilized by
the neuromuscular system, ultimately contributing to limb and joint stability.
Proprioceptive Neuromuscular Facilitation (PNF)
The Proprioceptive Neuromuscular Facilitation (PNF) approach is holistic, integrating
sensory, motor, and psychological aspects of rehabilitation. It incorparates reflex activies from
the spinal levels and upward, either inhibiting or facilitating them as appropriate [11]. PNF
exercise is characterized by stretching the involved musculature through rhythmic joint actions
and maximal (manual) resistance (Figure 7). Based on the theoretical principles of PNF, such
exercises are designed to enhance the response of neuromuscular mechanisms by stimulating
the proprioceptors. It is also believed that PNF stretch techniques reduce reflexive components
that stimulate muscular contraction and thereby enhance joint range of motion [93-95].
Stretching the musculature in multiple directions provides various stimuli to proprioceptors
and enhances performance through increased muscle strength [96] and improved muscle coordination [97]. Rhytmic stabilization exercises in PNF techniques can be included early in the
reactive neuromuscular training program to enhance neuromuscular coordination in response
to unexpected joint translation [11]. There is some evidence that PNF is associated with the
presence of neurogenic excitatory impulses to the antagonist motor neuron pool [94], but the
effect of PNF on proprioception has not been studied in the literature yet.
17
Figure 7: Proprioceptive Neuromuscular Facilitation.
Tai chi exercises and proprioception
Tai Chi is a traditional Chinese martial arts form comprised almost entirely of movement
control task and an ancient exercise used for all age groups. Tai Chi Chuan (TCC) was
originally developed as a martial arts form, but has been used for centuries in China as
an exercise by the elderly. It is a mind-body, low-intensity exercise practiced by slow,
controlled dimensional movements. The movements engage continuous body and trunk
rotation, flexion/extension of the hips and knees, postural alignment, and the coordination
of the arms. It involves a sequence of fluid, continuous, rhythmical, and graceful movements.
In general, from a physical benefit perspective, Tai Chi has been shown to enhance an
individuals’s physical capacity, general health, well being, respiratory function, balance,
coordination, and gracefullness. It can enhance muscle toning, thereby building strength
and flexibility rather than muscle mass, improve circulation, alleviate pain, improve energy
as well as stamina, and provide the individual with a sense of body control [98].
There has been growing interest in using Tai Chi training characterized by slow and
graceful movements, to improve postural balance and prevent falls in older people. During
the performance of Tai Chi, the shifting of one’s body weight, rotations, and standing on a
single leg are repeatedly practiced. All of these actions require accurate joint control, muscle
coordination, and good balance performance [24,28,99-101].
In 2001, Wong et al., compared the sway amplitude of elderly Tai Chi practitioners with
an active elderly group, when standing under 6 combinations of conditions: visual (eyes
open, eyes closed, sway-referenced) and support surface (fixed, sway-referenced). They
found that the Tai Chi practitioners swayed significantly less than did the control group
in the more challenged conditions, when the somatosensory input was ofset by absent or
conflicting visual input. However, it is not known whether the improvement is comparable
to that realized in young, healthy subjects standing under similar conditions [102].
Tsang et al., have studied to investigate the effects of long-term Tai Chi practice on
balance control when healthy elderly Tai Chi practitioners stood under reduced or conflicting
somatosensory, visual, and vestibular conditions, as compared with healthy elderly non–
Tai Chi practitioners and also with young subjects. They have revealed that the Tai Chi
practitioners had significantly better balance control than the non–Tai Chi subjects in the
visual and vestibular ratios, but not in the somatosensory ratio. Furthermore, there were no
18
significant differences in any of these 3 sensory ratios (somatosensory, visual, and vestibular
conditions) when the Tai Chi practitioners were compared with those of the young, healthy
subjects [100].
Tai Chi is also a mind–body exercise that emphasizes exact joint position and limb
positioning [5,99]. Of particular interest, Tai Chi also appears to improve kinesthetic sense,
which could indirectly improve movement quality and thus neuromuscular coordination
[98].
Tsang and Hui-Chan have shown that older Tai Chi practitioners have better knee joint
proprioceptive acuity, as evidenced by the fact that they make smaller absolute angle errors
in passive knee joint repositioning than control subjects similar in age, sex, and physical
activity level [28]. As similarly, Fong and Ng [101] have found Tai Chi practitioners achieved
less knee joint repositioning error than controls using an active repositioning test. It is
believed that a similar enhancement of joint position sense may also apply to the trunk,
because Tai Chi theory recognizes the importance of trunk movement in daily activities and
practitioners are required to use the trunk to lead the four limbs.
Tsang et al., have studied trunk propriception in older Tai Chi sword practitioners using
active trunk repositioning test acuity. They have revealed that Tai Chi sword practitioners
had developed better position sense in trunk rotation but not in trunk flexion than healthy
older subjects [99].
Xu et al., have shown that kinesthetic awareness was greater in elderly Tai Chi
practitioners compared to sedentary older adults. They have found that knee proprioception
of older swimmers/runners was not different from their non-exercised counterparts and it is
inferior than proprioception of Tai Chi practitioners. They have also demonstrated a similar
effect for upper limb static position sense where physically active older adults performed as
well as young individuals [24]. Therefore it can be concluded that ‘‘usual’’ exercise and not
only exercise that puts a great emphasis on the awareness of joint position and direction,
such as Tai Chi, is effective to preserve joint proprioception.
References
1. Cavanaugh JT, Mox RJ (2002) Balance and postoperative lower extremity joint reconstruction. Orthop Phys
Ther Clin N Am 11: 75-97.
2. Guyton AC, Hall JE (2006) The Nervous System: C. Motor and Integrative Neurophysiology. In: Textbook of
Medical Physiology. Elsevier, Saunders, Philadelphia, USA.
3. Riemann BL, Lephart SM (2002) The sensorimotor system, part I: the physiologic basis of functional joint
stability. J Athl Train 37: 71-79.
4. Billek-Sawhney B, Perry S (2006) Coordination and Proprioception. In F Huber, CW Wells (eds.). Therapeutic
Exercise. Elsevier, Philadelphia, USA.
5. Ogard WK (2006) Training for proprioception and kinesthesia. In J Nyland (ed.). Clinical Decisions in
Therapeutic Exercises. Pearson Prentice Hall, Pearson Education Inc., New Jersey, USA.
6. Wright ML, Adamo DE, Brown SH (2011) Age-related declines in the detection of passive wrist movement.
Neurosci Lett 500: 108-112.
7. Wingert JR, Welder C2, Foo P3 (2014) Age-related hip proprioception declines: effects on postural sway and
dynamic balance. Arch Phys Med Rehabil 95: 253-261.
8. Hurley MV (1997) The effects of joint damage on muscle function, proprioception and rehabilitation. Man Ther
2: 11-17.
9. Skinner HB, Wyatt MP, Hodgdon JA, Conard DW, Barrack RL (1986) Effect of fatigue on joint position sense
of the knee. J Orthop Res 4: 112-118.
10. Brockett C, Warren N, Gregory JE, Morgan DL, Proske U (1997) A comparison of the effects of concentric
versus eccentric exercise on force and position sense at the human elbow joint. Brain Res 771: 251-258.
19
11. Voight ML CG (2007) Impaired neuromuscular control: Reactive neuromuscular training. In HB Voight ML,
Prentice WE (eds.). Musculoskelatal Interventions, Techniques for Therapeutic Exercises. McGraw-Hill
Companies, Inc, NewYork, USA.
12. Rymer WZ, D’Almeida A (1980) Joint position sense: the effects of muscle contraction. Brain 103: 1-22.
13. Dietz V, Duysens J (2000) Significance of load receptor input during locomotion: a review. Gait Posture 11:
102-110.
14. Ribeiro F, Oliveira J (2010) Effect of physical exercise and age on knee joint position sense. Arch Gerontol
Geriatr 51: 64-67.
15. Lephart SM, Pincivero DM, Giraldo JL, Fu FH (1997) The role of proprioception in the management and
rehabilitation of athletic injuries. Am J Sports Med 25: 130-137.
16. Lephart SMRBL, Fu FH (2000) Introduction to the sensorimotor system. In FFH Lephart SM (ed.). Proprioception
and Neuromuscular Control in Joint Stability. Human Kinetics, Champaign, IL, USA.
17. Lane RE (1969) Physiotherapy in the treatment of balance problems. Physiotherapy 55: 415-420.
18. van der Esch M, Steultjens M, Knol DL, Dinant H, Dekker J (2006) Joint laxity and the relationship between
muscle strength and functional ability in patients with osteoarthritis of the knee. Arthritis Rheum 55: 953-959.
19. Hazneci B, Yildiz Y, Sekir U, Aydin T, Kalyon TA (2005) Efficacy of isokinetic exercise on joint position sense
and muscle strength in patellofemoral pain syndrome. American journal of physical medicine & rehabilitation /
Association of Academic Physiatrists 84: 521-527.
20. Leanderson J, Eriksson E, Nilsson C, Wykman A (1996) Proprioception in classical ballet dancers. A prospective
study of the influence of an ankle sprain on proprioception in the ankle joint. Am J Sports Med 24: 370-374.
21. Erden Z, Otman S (2002) Effects of rehabilitation on functional activity and proprioceptive sense in patients
with Total Knee Prothesis In Institute of Health Sciences, Physical Therapy and Rehabilitation. Hacettepe
University, Ankara.
22. Erdem EU, Can F (2007) The relationship between joint position sense, muscle strength and functional
level in cervical spondylosis. In Institute of Health Sciences, Physical Therapy and Rehabilitation. Hacettepe
University, Ankara.
23. van der Esch M, Steultjens M, Harlaar J, Knol D, Lems W, et al. (2007) Joint proprioception, muscle strength,
and functional ability in patients with osteoarthritis of the knee. Arthritis Rheum 57: 787-793.
24. Xu D, Hong Y, Li J, Chan K (2004) Effect of tai chi exercise on proprioception of ankle and knee joints in old
people. Br J Sports Med 38: 50-54.
25. Stewart AL, Grossman M, Bera N, Gillis DE, Sperber N, et al. (2006) Multilevel perspectives on diffusing a
physical activity promotion program to reach diverse older adults. J Aging Phys Act 14: 270-287.
26. Li JX, Xu DQ, Hong Y (2008) Tai Chi exercise and proprioception behavior in old people. Med Sport Sci 52: 77-86.
27. Petrella RJ, Lattanzio PJ, Nelson MG (1997) Effect of age and activity on knee joint proprioception. American
journal of physical medicine & rehabilitation / Association of Academic Physiatrists 76: 235-41.
28. Tsang WW, Hui-Chan CW (2003) Effects of tai chi on joint proprioception and stability limits in elderly subjects.
Med Sci Sports Exerc 35: 1962-1971.
29. Tsang WW, Hui-Chan CW (2004) Effects of exercise on joint sense and balance in elderly men: Tai Chi versus
golf. Med Sci Sports Exerc 36: 658-667.
30. Ashton-Miller JA, Wojtys EM, Huston LJ, Fry-Welch D (2001) Can proprioception really be improved by
exercises? Knee Surg Sports Traumatol Arthrosc 9: 128-136.
31. ML V (2002) The balance component of orthopedic rehabilitation. Ortop Phys Ther Clin N Am 11: 17-29.
32. Sharpe MH, Miles TS (1993) Position sense at the elbow after fatiguing contractions. Exp Brain Res 94: 179-182.
33. Tripp BL, Yochem EM, Uhl TL (2007) Recovery of upper extremity sensorimotor system acuity in baseball
athletes after a throwing-fatigue protocol. J Athl Train 42: 452-457.
34. Euzet JP, GY (1995) Relationships between position sense and physical practice. J Hum Mov Stud 28: 149-173.
35. Hewett TE, Paterno MV, Myer GD (2002) Strategies for enhancing proprioception and neuromuscular control
of the knee. Clin Orthop Relat Res : 76-94.
20
36. Schmitt H, Kuni B, Sabo D (2005) Influence of professional dance training on peak torque and proprioception
at the ankle. Clin J Sport Med 15: 331-339.
37. Hutton RS, Atwater SW (1992) Acute and chronic adaptations of muscle proprioceptors in response to
increased use. Sports Med 14: 406-421.
38. Lephart SM, Pincivero DM, Rozzi SL (1998) Proprioception of the ankle and knee. Sports Med 25: 149-155.
39. Friemert B, Bach C, Schwarz W, Gerngross H, Schmidt R (2006) Benefits of active motion for joint position
sense. Knee Surg Sports Traumatol Arthrosc 14: 564-570.
40. Ju YY, Wang CW, Cheng HY (2010) Effects of active fatiguing movement versus passive repetitive movement
on knee proprioception. Clin Biomech (Bristol, Avon) 25: 708-712.
41. Lin DH, Lin YF, Chai HM, Han YC, Jan MH (2007) Comparison of proprioceptive functions between computerized
proprioception facilitation exercise and closed kinetic chain exercise in patients with knee osteoarthritis. Clin
Rheumatol 26: 520-528.
42. Docherty CL, Moore JH, Arnold BL (1998) Effects of strength training on strength development and joint
position sense in functionally unstable ankles. J Athl Train 33: 310-314.
43. Bouët V, Gahéry Y (2000) Muscular exercise improves knee position sense in humans. Neurosci Lett 289:
143-146.
44. Lee HM, Cheng CK, Liau JJ (2009) Correlation between proprioception, muscle strength, knee laxity, and
dynamic standing balance in patients with chronic anterior cruciate ligament deficiency. Knee 16: 387-391.
45. Wong YM, Ng G (2010) Resistance training alters the sensorimotor control of vasti muscles. Journal of
electromyography and kinesiology : official journal of the International Society of Electrophysiological
Kinesiology 20: 180-184.
46. Numanoglu EA, Erden Z (2013) Evaluation of the joint position sense of the knee under different mechanical
loads among individuals with the patellofemoral pain syndrome. In Institute of Health Sciences, Physical
Therapy and Rehabilitation. Hacettepe University, Ankara, Turkey.
47. Palmitier RA, An KN, Scott SG, Chao EY (1991) Kinetic chain exercise in knee rehabilitation. Sports Med 11:
402-413.
48. Kibler WB LB, Bruce R (1995) Current concepts in shoulder rehabilitation. Adv Oper Orthop 3: 249–297.
49. Kibler WB (1998) The role of the scapula in athletic shoulder function. Am J Sports Med 26: 325-337.
50. Jan MH, Lin CH, Lin YF, Lin JJ, Lin DH (2009) Effects of weight-bearing versus nonweight-bearing exercise on
function, walking speed, and position sense in participants with knee osteoarthritis: a randomized controlled
trial. Arch Phys Med Rehabil 90: 897-904.
51. Hurd WJ, Chmielewski TL, Snyder-Mackler L (2006) Perturbation-enhanced neuromuscular training alters
muscle activity in female athletes. Knee surgery, sports traumatology, arthroscopy : official journal of the
ESSKA 14: 60-69.
52. Hilberg T, Herbsleb M, Puta C, Gabriel HH, Schramm W (2003) Physical training increases isometric muscular
strength and proprioceptive performance in haemophilic subjects. Haemophilia : the official journal of the
World Federation of Hemophilia 9: 86-93.
53. Armstrong RB (1984) Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med
Sci Sports Exerc 16: 529-538.
54. Magalhaes T, Ribeiro F, Pinheiro A, Oliveira J (2010) Warming-up before sporting activity improves knee
position sense. Physical therapy in sport : official journal of the Association of Chartered Physiotherapists in
Sports Medicine 11: 86-90.
55. Bartlett MJ, Warren PJ (2002) Effect of warming up on knee proprioception before sporting activity. Br J Sports
Med 36: 132-134.
56. Subasi SS, Gelecek N, Aksakoglu G (2008) Effects of different warm-up periods on knee proprioception and
balance in healthy young individuals. J Sport Rehabil 17: 186-205.
57. Avela J, Kyröläinen H, Komi PV (1999) Altered reflex sensitivity after repeated and prolonged passive muscle
stretching. J Appl Physiol (1985) 86: 1283-1291.
21
58. Guissard N, Duchateau J (2006) Neural aspects of muscle stretching. Exerc Sport Sci Rev 34: 154-158.
59. Björklund M, Djupsjöbacka M, Crenshaw AG (2006) Acute muscle stretching and shoulder position sense. J
Athl Train 41: 270-274.
60. Riemann BL, Lephart SM (2002) The Sensorimotor System, Part II: The Role of Proprioception in Motor
Control and Functional Joint Stability. J Athl Train 37: 80-84.
61. Larsen R, Lund H, Christensen R, Røgind H, Danneskiold-Samsøe B, et al. (2005) Effect of static stretching of
quadriceps and hamstring muscles on knee joint position sense. Br J Sports Med 39: 43-46.
62. Torres R, Duarte JA, Cabri JM (2012) An Acute Bout of Quadriceps Muscle Stretching has no Influence on
Knee Joint Proprioception. J Hum Kinet 34: 33-39.
63. Proske U, Gregory JE, Morgan DL, Percival P, Weerakkody NS, et al. (2004) Force matching errors following
eccentric exercise. Hum Mov Sci 23: 365-378.
64. Jones DA, Newham DJ, Clarkson PM (1987) Skeletal muscle stiffness and pain following eccentric exercise of
the elbow flexors. Pain 30: 233-242.
65. Paschalis V, Nikolaidis MG, Giakas G, Jamurtas AZ, Pappas A, et al. (2007) The effect of eccentric exercise on
position sense and joint reaction angle of the lower limbs. Muscle Nerve 35: 496-503.
66. Saxton JM, Clarkson PM, James R, Miles M, Westerfer M, et al. (1995) Neuromuscular dysfunction following
eccentric exercise. Med Sci Sports Exerc 27: 1185-1193.
67. Proske U, Allen TJ (2005) Damage to skeletal muscle from eccentric exercise. Exerc Sport Sci Rev 33: 98-104.
68. Newham DJ, Mills KR, Quigley BM, Edwards RH (1983) Pain and fatigue after concentric and eccentric muscle
contractions. Clin Sci (Lond) 64: 55-62.
69. Newham DJ, MG, Mills KR, Edwards RH (1983) Ultrastructural changes after concentric and eccentric
contractions of human muscle. Journal of Neurological Science 61: 109-122.
70. Fortier S, Basset FA, Billaut F, Behm D, Teasdale N (2010) Which type of repetitive muscle contractions
induces a greater acute impairment of position sense? Journal of electromyography and kinesiology : official
journal of the International Society of Electrophysiological Kinesiology 20: 298-304.
71. Walsh LD, Allen TJ, Gandevia SC, Proske U (2006) Effect of eccentric exercise on position sense at the human
forearm in different postures. J Appl Physiol (1985) 100: 1109-1116.
72. Givoni NJ, Pham T, Allen TJ, Proske U (2007) The effect of quadriceps muscle fatigue on position matching at
the knee. J Physiol 584: 111-119.
73. Walsh LD, Hesse CW, Morgan DL, Proske U (2004) Human forearm position sense after fatigue of elbow flexor
muscles. J Physiol 558: 705-715.
74. Winter JA, Allen TJ, Proske U (2005) Muscle spindle signals combine with the sense of effort to indicate limb
position. J Physiol 568: 1035-1046.
75. Proske U, Morgan DL (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs,
adaptation and clinical applications. J Physiol 537: 333-345.
76. Allen TJ, Ansems GE, Proske U (2007) Effects of muscle conditioning on position sense at the human forearm
during loading or fatigue of elbow flexors and the role of the sense of effort. J Physiol 580.
77. Vila-Cha C, Riis S, Lund D, Moller A, Farina D, et al. (2011) Effect of unaccustomed eccentric exercise on
proprioception of the knee in weight and non-weight bearing tasks. Journal of electromyography and kinesiology
: official journal of the International Society of Electrophysiological Kinesiology 21: 141-147.
78. Chmielewski TL, Myer GD, Kauffman D, Tillman SM (2006) Plyometric exercise in the rehabilitation of athletes:
physiological responses and clinical application. J Orthop Sports Phys Ther 36: 308-319.
79. Swanik KA, Lephart SM, Swanik CB, Lephart SP, Stone DA, et al. (2002) The effects of shoulder plyometric
training on proprioception and selected muscle performance characteristics. Journal of shoulder and elbow
surgery / American Shoulder and Elbow Surgeons 11: 579-586.
80. Swanik KA, Lephart SM, Swanik CB, Lephart SP, Stone DA, et al. (2002) The effects of shoulder plyometric training
on proprioception and selected muscle performance characteristics. J Shoulder Elbow Surg 11: 579-586.
22
81. Chan D, Can F (2009) The effects of plyometric versus strength training exercise program on shoulder
proprioception. In Institute of Health Science, Physical Therapy and Rehabilitation Program. Hacettepe
University, Ankara, Turkey.
82. Marks R (1994) Effect of exercise-induced fatigue on position sense of the knee. Aust J Physiother 40: 175-181.
83. Ribeiro F, Mota J, Oliveira J (2007) Effect of exercise-induced fatigue on position sense of the knee in the
elderly. Eur J Appl Physiol 99: 379-385.
84. Sekir U, Yildiz Y, Hazneci B, Ors F, Aydin T (2007) Effect of isokinetic training on strength, functionality and
proprioception in athletes with functional ankle instability. Knee surgery, sports traumatology, arthroscopy :
official journal of the ESSKA 15: 654-664.
85. Rozzi SL, Lephart SM, Sterner R, Kuligowski L (1999) Balance training for persons with functionally unstable
ankles. J Orthop Sports Phys Ther 29: 478-486.
86. Bernier JN, Perrin DH (1998) Effect of coordination training on proprioception of the functionally unstable
ankle. J Orthop Sports Phys Ther 27: 264-275.
87. Hughes T, Rochester P (2008) The effects of proprioceptive exercise and taping on proprioception in subjects
with functional ankle instability: a review of the literature. Physical therapy in sport : official journal of the
Association of Chartered Physiotherapists in Sports Medicine 9: 136-147.
88. Lee AJ, Lin WH (2008) Twelve-week biomechanical ankle platform system training on postural stability and
ankle proprioception in subjects with unilateral functional ankle instability. Clin Biomech (Bristol, Avon) 23:
1065-1072.
89. Postle K, Pak D, Smith TO (2012) Effectiveness of proprioceptive exercises for ankle ligament injury in adults:
a systematic literature and meta-analysis. Man Ther 17: 285-291.
90. Coskun G, Can F (2008) Effects of proprioceptive exercises on muscle strength and functinal level in
rehabilitation of chronic low back pain. In Institute of Health Sciences, Physical Therapy and Rehabilitation.
Hacettepe University, Ankara, Turkey.
91. Erdem EU, Can F (2013) The comparative study on efficiency of different physiotherapeutic approaches in
wrist proprioception. In Institute of Health Sciences, Physical Therapy and Rehabilitation. Hacettepe University,
Ankara, Turkey.
92. Cooper RL, Taylor NF, Feller JA (2005) A systematic review of the effect of proprioceptive and balance
exercises on people with an injured or reconstructed anterior cruciate ligament. Research in sports medicine
(Print) 13: 163-178.
93. Kofotolis ND VI, Vamvakoudis E, Papanikolaou A, Mandroukas K. (2005) Proprioceptive neuromuscular
facilitation training induced alterations in muscle fibre type and cross sectional area. British journal of sports
medicine 39: 11-14.
94. Kofotolis ND KE (2007) Cross-training effects of a proprioceptive neuromuscular facilitation exercise
programme on knee musculature. Physical Therapy in Sport 8: 109-116.
95. Knott MV, D. E. (1968) Proprioceptive neuromuscular facilitation: Patterns and techniques. Harper & Row.
96. Kofotolis N, Kellis E (2006) Effects of two 4-week proprioceptive neuromuscular facilitation programs on
muscle endurance, flexibility, and functional performance in women with chronic low back pain. Phys Ther 86:
1001-1012.
97. Nelson AG CR, McGown CM, Penrose KW (1986) Proprioceptive neuromuscular facilitation versus weight
training for enhancement of muscular strength and athletic performance. Journal of Orthopaedic and Sports
Physical Therapy 7: 250-253.
98. Kraemer TJ (2006) Complementary and alternative approaches to movement and exercise. In: J Nyland (ed.).
Clinical Decisions in Therapeutic Exercises. Pearson Education Inc., Pearson Prentice Hall, New Jersey, USA.
99. Tsang WWN FS, Lui F, Hui-Chan CWY (2009) Trunk position sense in older Tai Chi sword practitioner. Hong
Kong Physiother J 27: 55-60.
100.Tsang WW, Wong VS, Fu SN, Hui-Chan CW (2004) Tai Chi improves standing balance control under reduced
or conflicting sensory conditions. Arch Phys Med Rehabil 85: 129-137.
23
101.Fong SM, Ng GY (2006) The effects on sensorimotor performance and balance with Tai Chi training. Arch
Phys Med Rehabil 87: 82-87.
102.Wong AM, Lin YC, Chou SW, Tang FT, Wong PY (2001) Coordination exercise and postural stability in elderly
people: Effect of Tai Chi Chuan. Arch Phys Med Rehabil 82: 608-612.
24