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Proprioception: The Forgotten
Sixth Sense
Chapter: Proprioceptive Training in Neurological Diseases
Edited by: Defne Kaya
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eBooks
Proprioceptive Training in Neurological
Diseases
Cevher Savcun Demirci1, Fatma Avcu2, Ender Ayvat2, Muhammed Kılınç2
and Sibel Aksu Yıldırım2*
Kırıkkale University Faculty of Health Sciences, Department of Physiotherapy and
Rehabilitation, Turkey
1
Hacettepe University Faculty of Health Sciences, Department of Physiotherapy and
Rehabilitation, Turkey
2
*Corresponding author: Sibel Aksu Yıldırım, Pt. PhD, Professor, Hacettepe University
Faculty of Health Sciences, Department of Physiotherapy and Rehabilitation, Turkey,
E-mail: [email protected]
Abstract
The most important objective of neurological rehabilitation following nervous system
injury is the restoration of sensory-motor functions. A healthy sensory-motor function
requires normal flow of proprioceptive information from the periphery. Meanwhile
processing of proprioceptive signals can be hindered as in cerebral injury or stroke or
neurodegenerative diseases such as Parkinson’s disease. This is a significant obstacle for
neurorehabilitation. Clinically, proprioception is a very important factor for assessment
and treatment of the patients because these patients use proprioceptive information
insufficiently and proprioceptive sensory deficit prevents learning or re-learning of basic
functions such as postural control, protective reflexes, joint movements, balance, gait and
fine motor skills of the hand. Therefore, re-establishment of neural connections and more
specifically maintenance of these connections in proprioceptive-motor processes are needed
for restoration of motor control [1,2]. So evaluation and treatment of proprioception in
neurological disorders is very important and should not be ignored.
Keywords:
Approaches
Exercise; Multisensory Treatment; Proprioception Training; Sensory-Motor
Proprioceptive Training Methods
Proprioceptive System
Proprioception is the sense that allows us to perceive the position and movement of
the body in space. It contributes to all complex neuromuscular processes underlying the
balance and postural control. It is involved in all static and dynamic activities, helps the
body to be stable and oriented and contributes to all complex neuromuscular processes
underlying balance, gait and postural control [3]. Acting as a data system, it has a direct
effect on program generators at the spinal level. Sense of proprioception, which has a critical
role in motor learning and ability to adapt to new or changing environment, has extensive
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connections within the cortical-cerebellar conduction network. Proprioceptive input when
it reaches the supraspinal level from the periphery, in order to modulate more complex
processes of motor control, synapse with cerebellar, brain stem, subcortical and cortical
areas. When the stimulus reaches the reflex level, a rapid muscle response is elicited via
the reflex arch appropriate for the timing of the neuromuscular control. At higher levels,
afferent input synapse with the visual and vestibular inputs to facilitate automatic postural
control and locomotion. Proprioceptive data can influence the Central Nervous System
(CNS) functions at different levels and alter intensity and importance of the information at
all levels via many mechanisms. Proprioceptors are found in three peripheral anatomical
localizations: Muscle spindles, tendons and joints [4-7].
Muscle spindle
Muscle spindle is the most important receptor for the control of the movement. They are
involved in the maintenance of the modulation of the alpha motor neurons that innervate
extrafusal muscle fibers. This role is performed via the simultaneous modulation of gamma and
alpha motor neurons during functional activities. Afferents of the muscle spindle facilitates
the agonists and their synergists, while, at the same time inhibiting polysynaptically the
antagonists and their synergists. The information is conveyed to the ipsilateral cerebellum
and contralateral parietal lobe concurrently. In conclusion, muscle spindle plays a part in
the peripheral feed-back mechanism that conducts the stimuli periphery to various regions
of the CNS. These centers regulate the continuum of the neuro-excitation at the levels of the
brain stem and the spinal cord. Gamma innervation regulates the degree of internal tension
in the non-contractile part of the muscle spindle. Internal tension can be altered by the
external effect of gravity, positioning and therapeutic processes, thereby motor responses
can be modulated.
Main afferents of the spindle are length receptors and they detect the changes
in length that occur in the non-contractile part of the spindle. The change in length
occurs as a result of positioning, stretching or mechanical external force such as
internal mechanism caused by intrafusal muscle contraction. Spinal motor generators
and supraspinal activity affect the alpha and gamma motor neurons to modify muscle
contraction patterns. Due to this inherent internal sensitivity, it changes its length
when a therapeutic technique is applied and receptors sensitive to length start firing.
Another group of receptors respond to the speed of the tension rather than the length.
Techniques such as rapid stretching, vibration or taping cause rapid tension effect on
the spindle with a resultant stimulation of the receptor. As a therapeutic approach,
afferent input of the muscle spindle can permanently alter the existing programs by
affecting the cerebellum and basal ganglia. Even if neural plasticity is possible in the
spinal cord, the effect of muscle spindle on the spinal nervous system is short lived, with
very small long-term effects. Cerebellum is effective on the basal ganglia/frontal lobe
brain stem and they have the potential to alter existing motor patterns by modulating
interneurons in the spinal pattern generators.
Various therapeutic approaches that adopt sensory stimulation of muscle
spindle
Positioning: It is based on reducing the effects of gravity on alpha motor neuron and
consequently inhibiting muscle tone. Relaxation achieved by this technique is not permanent
and unless motor learning or central program adaptation is actualized it is reversible.
Hence, modifications in a number of systems are required for this treatment to be effective.
The effects of muscle tone on autogenic inhibition, reciprocal innervation, labyrinthic or
somatosensory effects and cerebellar regulation can be benefitted. It should be kept in mind
that active participation of the patient is required for the changes in the CNS to occur and
motor learning to take place [8].
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Manuel techniques
Resistance: It is generally used to stimulate intrafusal and extrafusal muscle contraction.
Resistance can be applied mechanically or manually, using the body weight or the effect of
gravity, allowing smooth and coordinated movement. More motor units fire when resistance
is applied against a movement. Resistance activates muscle spindle (Ia and II endings)
and golgi tendon organ (Ib ending) and makes them sensitive to changes in velocity and
length. Input to the spinal neurons and upper centers trigger a response in the form of
facilitation or increase in muscle contractions. While agonist and synergistic muscles are
facilitated antagonist muscles are inhibited. Extrafusal muscle fibers undergo hypertrophy
and kinesthetic awareness increase [9].
Resistance applied for isometric contraction is more stimulating than that applied for
isotonic contraction. When the isometric resistance is increased or maintained, more motor
units participate in the contraction and the force of the extrafusal contraction is enhanced.
Eccentric isometric contraction has been defined as the elongation of muscle fiber with
resistance. Eccentric contraction provides faster increase in strength though all types of
contractions increase strength. Resistance is an important clinical treatment and its use is
recommended in treatment programs [8] (Figure 1).
Figure 1: Application of resistance.
Tapping: Tapping stimulates intrafusal and extrafusal muscle fibers by giving the muscle
spindle a quick stretch. Physiotherapists use three different types of “tapping”. Tapping
on the tendon is not exactly a discriminative stimulus. Clinicians use this technique to
examine the stretch sensitivity of a muscle (patellar reflex). Normal response is a brisk
muscle contraction. Because of the magnitude of the stimulus and its direct effect on
alpha motor neuron, it is not possible to teach a patient how to control or grade muscle
contraction effectively. Tapping the muscle belly elicits a lower intensity response and is
more satisfactory. It can be used, for instance, to maintain the weight carrying position.
“Reverse tapping” is a less frequently employed technique but can be used. The limb is
positioned so that the gravity promotes stretch rather than the physiotherapist exerting a
manual or the patient exerting an active stretch. When the muscle responds, the therapist
taps lightly or moves the limb passively to the position where the muscle is shortened. For
instance, patient bears weight on extended elbow and tries to fully extend the elbow while
the therapist taps the triceps muscle. In the meantime gravity rapidly stretches the triceps
muscle. Timing is critical in this technique. If not applied just on time, for instance, if the
elbow is tapped towards extension, when the flexor muscles’ motor neurons are sensitive,
then the flexor muscles contract. If the therapist taps following stretch to the extensor
muscles, then the flexor muscles would be dampened and motor response of the extensor
muscles would increase [8-10].
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Stretch-pressure: The target area of this technique is its belly. Since this technique can
increase the muscle tone, it is not used in hypertonic muscles. It is applied to an antagonist
muscle to inhibit hypertonic muscle. Generally, it is not a rapid stimulus and the stimulus
is maintained for 5-10 seconds [8].
Stretch-release: In this technique, fingers are placed over the belly of large muscles
and the fingers are then abducted to stretch the skin and underlying muscle. The stretch is
performed firmly so that the soft tissue will deform temporarily. By this way, the cutaneous
receptors and Ia afferent fibers would be stimulated, which results in facilitation of the
target muscle [8].
Manual pressure: Manuel pressure has a facilitatory effect when applied as a brisk
stretch or friction-like massage. In conjunction with volitional effort, it contributes to motor
learning [8].
Mechanical stimulations
Electrical stimulation: It is a technique used to achieve muscle contraction by eliciting
action potential in the motor branches of peripheral nerves [11]. Since electrical stimulation
is a method of inducing facilitation of muscle spindle, it is used as an adjunct to treatment.
Studies showed that combination of electrical stimulation with active movement was more
effective in improving function [12]. Studies especially in stroke patients highlighted the
beneficial effects of functional electrical stimulation on gait [13-16]. It is believed by some
authors that utilization of electrical stimulation as a sensory stimulus would be less effective
due to the absence of sensory receptors for electrical current and absence of somatosensory
cortical representation of such a stimulus [8].
Vibration: Vibration applied to the tendon stimulates the primary ending of the muscle
spindle, elicits reflex muscle contractions that would help improve muscle functions [17]. The
effects of vibration on muscle spindle depend on the vibration parameters. High frequency
vibration (100-300 Hz) applied to the muscle or tendon elicits a reflex response termed
tonic vibratory reaction. Tension within the muscle increases slowly and progressively for
30-60 seconds and makes a plateau throughout the duration of the stimulus. The effect of
vibration can be increased by combining it with resistance, positioning and visually directed
movement [8].
Some side effects of vibration have been highlighted. Frequencies over 200 Hz can cause
lesions on the skin. Discomfort and sometimes pain have been reported with vibrations over
150 Hz. Therefore, it is recommended that the frequency be kept between 100-125 Hz. Many
battery-operated hand vibrators have a frequency in the range 50-90 Hz. A frequency less
than 75 Hz can cause inhibitory effect in a normal muscle.
Another type of application, namely whole body application involves delivering vibrations
to a large area. While standing on a platform vibrating at a frequency between 1-50 Hz,
vibrations from the sole of the foot stimulate the muscles and tendons as well as joint
proprioceptors [18]. Johansson et al., found a strong relation between stimulation of the
joint mechanoreceptors and stimulation of gamma efferents (spindle becoming responsive),
resulting in stiffness in muscles and joint stability [19]. This is important in understanding
how whole body vibration improves proprioception.
A study by El-Tamawy et al., showed that vibration, when applied while walking on the
treadmill, had positive effects on angular displacement in the joints and spatio-temporal
parameters of gait in Parkinson’s disease patients. External stimuli contribute to the sensorymotor integration that requires processing and organization of proprioception. They cause
improvement in cortico-spinal excitability and increase in the tonic activity of the plantar
muscles [20]. Ghoseiri et al., showed that vibration applied to the lumbar region in sync with
stepping increased walking velocity and stability in Parkinson’s disease patients [21].
4
Müller et al., argued that muscle vibration applied on the left forearm improved slowed
cognitive processes due to traumatic cerebral injury [22]. Karnath et al., demonstrated that
vibration applied to the neck decreased contralateral neglect in patients with right-sided
hemispheric lesion [23].
The study by Avanzino et al., on the other hand, showed that maintaining the dynamic
proprioceptive inputs by muscle vibration in an immobilized arm could prevent hemispheric
unbalance due to short-term limb disuse [24].
Tendon organ
Golgi tendon organ is a special kind of receptor localized at the proximal and distal
musculotendinous junctions. Together with muscle spindles, it plays a key role in
proprioception [25,26].
The most important role of Golgi tendon organ is to monitor the muscle stretch as a
result of contraction of the extrafusal muscle fibers. Research showed that the tendon
organ is very sensitive to stretch and, working together with muscle spindle, it adjusts the
muscle tone and adaptability of the extrafusal muscle fiber by conducting the demands of
environmental circumstances to higher centers. The basic difference between Golgi tendon
organ and muscle spindle is that muscle spindle is sensitive to length while Golgi tendon
organ is sensitive to force and speed. Their effects at the spinal level are the opposite.
Muscle spindle regulates reciprocal inhibition whereas golgi tendon organ is involved in
autogenic inhibition [26,27].
Inhibitory pressure: Is stimulation in the form of a long-term pressure on the tendons. It
activates muscle receptors and tactile receptors and elicits an inhibitory response. Pressure
can be applied manually or using body weight, mechanically or using inhibitory splints.
It has been argued that deep pressure exerts its effects by stimulating rapidly adapting
Pacinian corpuscles. There are studies demonstrated that these receptors are involved
in regulation of vasomotor reflexes, modulation of pain and that they are related to the
inhibitory effects of other sensory systems in the CNS [28-30].
Combination of pressure (manual), environmental needs (low) and parasympathetic
activity (slow, easy breathing) indicates that many systems should work side-by-side in
order to elucidate the best motor response. Real world requires one, whether under stress
or not, to give a normal response to various environmental conditions. Hence, a therapist
should include as many different environmental conditions as possible and change the
stimuli frequently to enhance the adaptation capacity of the patient [8].
Joint
Joints yields information on body position and movements to the cerebellum, cortical
sensory areas and motor nuclei [31]. Complex joints contain more receptors and produce a
signal even with small angulations. Joint mechanoreceptors conduct the afferent information
they receive to the anterior horn cells for a rapid control of the periarticular muscles. On
the other hand, the information is transferred to the supraspinal centers via spinocerebellar
and dorsolateral tracts. Proprioceptive and somatosensory integration of the movement is
undertaken in the cerebellum and unconscious control is achieved while the conscious
control is handled by the cortex [32].
Four major joint receptors have been defined in the literature. Anatomically, these
receptors are localized on the joint capsule and ligaments [5,33]. Joint receptors have
different thresholds for angulation and velocity of the joint movements. They not only play
a role in the origination of the information but also in the cortical sensory mapping within
the somatosensory area 3a. These stimuli project onto various cortical fields related to body
perception and motor control of the body. On the other hand, if there is no overlap between
sensory information and targeted movement, then the motor movement is modified or the
plan is changed to achieve the aim [34].
5
Joint receptors are quite useful in various treatment techniques and exert very powerful
effects on motor systems [8].
Combined proprioceptive input techniques
Thanks to their combined effects, these techniques are used for multiple data input.
Some of these combined approaches include Jamming; ballistic movements; total body
positioning; PNF patterns; stretching; range; rotation and shaking; postexitatory inhibition;
heavy work patterns; Feldenkrais and manual therapy [8].
Traction: The joint receptors are stimulated by manually distracting the joint surfaces.
Slow and gradual traction can be used to increase mobility, relieve muscle spasms and
reduce pain [9].
Approximation: The joint receptors are stimulated by manual or mechanical compression
of the joint surfaces. It increases joint awareness, facilitates postural extensor system
and helps to stabilize joints. It is usually applied during extensor patterns and by adding
pressure down the limb [9]. Moreover, jamming, when used as an approximation technique,
is a procedure in which weight is applied to the wrist or ankle of the patient. It can be done
by the patient him/herself and it activates co-contraction of the muscles around the joint
and inhibits spasticity. This tecnique can be combined with functional training to support
functional outcomes and achieve better somatosensory response [8].
Ballistic movements: These are the movements performed with maximal velocity and
acceleration. It is characterized by high firing ratio, short contraction time and high force
generation. Ballistic movements or pendular exercises are effective due to their combined
proprioceptive effects and cause specific neuromuscular adaptations. Ballistic movements
are a part of the pattern generators in the spinal system and are more complex than reflex
responses. Supraspinal influence over programmed activity has a role to enhance the
efficacy of this treatment [8,35,36].
Proprioceptive neuromuscular facilitation pattern: Based on the normal development
of human movements, this method is used with the aim of improving motor performance.
It facilitates neuromuscular responses by stimulating the proprioceptors. This approach is
widely used in many orthopedic or neurological diseases but research on this method has
focused largely on its efficiency in lower motor neuron lesions. This method is helpful in the
rehabilitation of patients with spasticity or paresis since it facilitates muscle lengthening
by increasing the inhibitory mechanisms and increases muscle strength by facilitating the
excitatory mechanisms [37-39] (Figures 2 and 3).
Figure 2: PNF application in flexor pattern.
6
Figure 3: PNF application in extansor pattern.
Rood: This method involves the relations between somatic, autonomic and psychological
factors and the roles of these relations on motor behavior. The treatment aims to improve
normal patterns by activating the movement and postural responses. Movement is
accomplished from the most basic to the most complex patterns. Sensory stimulus is the
fundamental approach; techniques such as tactile stimuli with brushing and ice, mild
stretching of the muscle and compression on the joints should be used [40].
Feldenkrais: It is an approach, which argues that increase in the kinesthetic and
proprioceptive awareness of functional movements will result in increased function, reduced
pain, comfort in movements and satisfaction. Feldenkrais concept involves stretching of
the relaxed muscle, distraction and compression of the joint for sensory awareness. Both
techniques are combinations of proprioceptive techniques. It is applied to one body part and
then moved to other body segments. Body schema awareness is enhanced by this technique.
By observing the technique, volitional control can be achieved by the patients [41].
Manual therapy: These approaches can be utilized whenever a pathological condition
affects joint mobility and functional problems ensue. Immobility in the joints reduces the
adaptation potential of the peripheral nerve due to changes in nerve bed. Problems in the
neural elasticity eventually affect the functions of the connective tissue. Consequently, the
control of motor system over musculoskeletal component is altered [42,43]. Even for this
reason alone, manual techniques constitute an important option.
Patients with functional restriction due to pain usually present to the physiotherapist for
musculoskeletal assessment. A subjective and observatory assessment should be carried
out, physical assessment should be structured in such a way that somatic and radicular
symptoms could be differentiated and the involvement of the peripheral nervous system
could be established [43]. Increased muscle tone in peripheral injury is usually believed
to be a protective mechanism of the tissue against inflammation. It is possible that this
increase in muscle tone is a result of reduced presynaptic activity of afferents of the flexor
reflex arch through supraspinal mechanisms. The same mechanisms can trigger CNS injury
as well. The difference between an orthopedic and neurological case is the triggering of
CNS injury. Following central lesions, motor generators are usually not spared and this
results in hypotonia. Hypotonia, in turn, results in peripheral instability, tension in the
peripheral tissues and potential peripheral injury. Both in orthopedic and neurological
cases, peripheral injury appear first, followed by peripheral instability due to hypotonia. The
response of CNS to instability is similar: muscle tone increases when presynaptic inhibition
is suppressed. As a result of suppressed presynaptic inhibition on afferent input, activity of
the spinal generator increases. In an isolated musculoskeletal problem in the presence of
7
intact CNS, the motor system has the capacity to adapt, can control the spinal generators
and increased muscle tone directly related to the problem can be isolated. In cases with
CNS involvement flexibility of the motor system is lost, the control over the central system
generators disappear and synergistic patterns with high tone can develop. In both cases, the
peripheral system should be assessed and treatment should be given, if necessary. Tension
tests can yield inappropriate responses in the neural tissues. In order to prevent inducing
further pain, movements of the neural tissues are limited and muscle tone increases
secondary to painful provocation of nociceptors of the sensitized neural tissue. Pain further
increases muscle tone and hinders passive movement [44]. Painless movement indicates
the sensitivity of CNS to large-caliber myelinated fibers and their functions. Restriction
of the joint movements that could cause pain beyond the threshold, nociceptors, muscles
and joints play roles in the attention and protection of the CNS. Inflammation of the neural
tissues renders the nociceptors hypersensitive [43].
Treatment should be modified according to the degree of immobility, intensity of pain and
the area of irritability. Taking the tension in the peripheral nervous system into account, not
only the joints but also the affected neural dynamics should be targeted. Motor responses can
be modulated by the effects of manual therapeutic approaches on proprioceptive system [30].
Exteroceptive/Cutaneal System
Somatosensory system is generally divided into 2 groups: The first system is
phylogenetically older and non-specific while the second system is newer and functionspecific. To date, systems are classified as lemniscal and spinothalamic systems.
Spinothalamic system: Conducts predominantly protective stimuli.
Lemniscal system: Conducts the discriminative properties of somatic senses, including
exteroceptive and proprioceptive information.
Understanding the anatomy and physiology of the sensory systems is fundamental
in formulating treatment options. Afferent information reach the lemniscal system via a
peripheral or cranial nerve. These interneurons are large-calibre. Therefore signals are
conducted very fast. The most striking feature of this system is somatotopic organization.
There is a spatial topographic representation in the ascending fibers in the dorsal column
and a synaptic organization in the thalamus. This high-order organization enables
differentiation of specific proprioception and tactile senses. Lemniscal system conducts
kinesthetic information such as conscious proprioception, touch, pressure, localization,
quality and spatial attributes of a mechanical stimulus [5,45,46].
The ascending stimuli of the spinothalamic system either terminate in the reticular
formation or establish collateral connections. These fibers ascend to synapse with the
neurons of the non-specific (medial) thalamus, after which are distributed to almost every
region of the cerebral cortex. Other collaterals project to the autonomic nervous system, limbic
system and brain stem [5,33]. There is an alarm system against noxious stimuli due to the
connections of the spinothalamic system with the reticular formation and autonomic nervous
system. This system conducts pain, light (crude) touch, sexual and noxious senses [5].
Categorizing spinothalamic and lemniscal systems as two separate systems can be
misleading and lead the reader to think that these systems can be activated separately.
Both systems react to many sensory stimuli, for instance to crude touch, concurrently.
Lemniscal system carries both exteroseptive and interoseptive information. On the other
hand, it is possible to overload a system with selective stimulus given slowly or rapidly [47].
Poggio and Mountcastle [48] argued that the lemniscal system had an inhibitory effect on
the spinothalamic system. Many techniques targeting sensory treatment act on activating
the lemniscal system or establishing the balance between two systems.
8
On the other hand, facial region innervated by the trigeminal nerve projects to the third
somatosensory area, which is closely related to the parasympathetic system. If the protective
system becomes hypersensitive, general sympathetic hyperactivity, inadequate control or
suppression of the external stimuli and attention deficits can be observed. It renders the
lemniscal system functional by desensitizing the tactile sensation with various methods or
reducing matching [47].
Treatment alternatives that use exteroceptive system
The function of this system is to equip the nervous system with information related
to the outside world. CNS adapts behavior according to this information. Even though
many protective responses are elicited in the motor system, these responses can be altered,
modulated or terminated secondary to chemical, emotional, motivational etc stimuli. In
contrast to other therapeutic approaches, the function of the exteroceptive input system is
not reflexive but informative and adaptive [8].
Cold application: Short-duration, high intensity cold application is rubbing ice on the
swollen regions of the muscle for 3-5 seconds with mild pressure. This method causes
activation of both the exteroceptors and proprioceptors and, consequently the cortex for a
short time but it is not related to motor learning. Cold application, at the same time, may alert
the reticular formation, autonomic nervous system and limbic system via its connections.
Cold applications should be avoided on the facial region, forehead or behind the ears, and
in patients with angina pectoris or coronary artery disease due to the connections of these
regions to the reticular formation and autonomic nervous system [8].
Long-duration cold application reduces firing of the neurons and muscle spindles by
activating the thermoreceptors. The aim is to reduce the conduction of afferent and efferent
stimuli. It inhibits muscle tone and painful muscle spasms. During the application, there
is a decrease in the metabolic rate of the tissue. Application needs to be performed under
observation due to the possibility of any autonomic side effect and it should be avoided in
patients with sensory impairment, autonomic instability and vascular disorders [8,9].
Neutral warmth: It activates the thermoreceptors in the parasympathetic areas of the
autonomic nervous system. It reduces the muscle tone, relaxes and alleviates pain. Like cold
application, neutral warmth can alter the status of central pattern generators by influencing
afferent input directly or indirectly. In the absence of an active participation, neuroplastic
adaptations do not occur in the CNS. Johnstone pressure splints is a fine example of
neutral warmth application and can be combined with functional activities [9,49]. Moreover,
maintaining the stimuli for sometime results in effective inhibition by preventing conduction
of other stimuli. Armutlu et al., examined the effects of neuromuscular rehabilitation and
Johnstone pressure splints on balance and coordination in MS patients and found that
patients using pressure splints, compared to the controls, showed improved cortical onset
P37 peak amplitude, one of the components of somatosensory evoked potential, and singlelimb stance time was longer [50].
Vestibular System
Vestibular apparatus is a mechanoreceptor [5]. Peripheral proprioceptive receptors give
information to the CNS regarding the position of the body in space while the vestibular
system gives information about the position of the head in space and its linear acceleration.
The vestibular system has a critical role in motor functions due to its close connections
and interactions with audio, visual, proprioceptive and motor systems [31]. In case of an
injury to one of these systems, body tries to educate other systems and heal itself. The most
prominent functions of the vestibular system are regulating the muscle tone and ocular
movements, keeping the object in focus while the head or the object is moving, modulating
spatial orientation as well as orientations of the head and body. It also supports learning
and emotional development [51].
9
Proprioception and Exercise
The effects of exercise in proprioceptive training can be explained in brief: Exercise
does not change the number of mechanoreceptors but induces morphological adaptations
in muscle spindle. Intrafusal muscle fibers can exhibit some metabolic changes and the
latency of stretch reflex response decreases while its amplitude increases. At central level,
regular physical activity and exercise can alter proprioception by increasing muscle spindles
and inducing plastic changes in the CNS. During physical activity, there is an increase in
the muscle spindle output and cortical planning of the sense of proprioception becomes
facilitated. This eventually increases the output of the muscle spindle, which possibly
results in plastic changes in the CNS, including increase in the strength of the synaptic
connections, changes in the number of connections between neurons and structural changes
in its organization. Plastic changes in the cortex can eventually modify the cortical map of
the human body and improve joint proprioception by increasing the cortical representations
of the joints [52,53].
Recovery of the sense of proprioception is achieved by the help of motor control on
different levels of the CNS: reflex spinal level, brain stem level (balance and correction
responses) and cortical level [54,55]. Reflex level is not sufficient for full motor control.
Just like using contract-relax technique, one of the PNF techniques or manual techniques
such as tendon pressure to relax the muscle, the utilization of reflex stimulation to regain
flexibility will not yield permanent results [56]. For a comprehensive training, ball and disk
exercises, plyometric exercise, trampoline exercises, pilates exercises, rapid movement with
change of velocity or direction and hopping and jumping should be implemented in the
treatment. Perception and interpretation of the senses can be made difficult by using a
number of floor surfaces, getting the eyes closed and giving additional tasks [57]. Aksu et
al., gave patients with ataxia due to posterior column degeneration a treatment program
comprising of proprioceptive neuromuscular facilitation techniques, Johnstone pressure
splints, balance and gait training. As a result, they showed that balance and proprioception
training comprising neurophysiological approaches had beneficial effects on static and
dynamic balance and functional level [58].
Additional tasks during the execution of a basic task disrupt static and dynamic balance,
reduce motor performance and gait disturbance. This is evident especially in neurological
disorders and results in restrictions in daily life, increased risk of falling and decreased
independence. This should be considered in treatment [59].
Combined multisensory approaches
Despite the fact that all approaches have the potential of being multisensory, they either
focus on a single sensory system or use two or more input modality in autonomic motor
programming. Physiotherapists who analyze the combined input that affect the patients’
performance and the effects of autonomic responses determine the aims for expected
treatment outcome by problem solving. Classification of multisensory input is extensive and,
therefore, this section includes some examples to support the clinicians in classifying new
intervention approaches. Clinical decisions, techniques and approaches need to be modified
as the patient shows progression. These decisions should be based on understanding and
integrating the neurophysiological mechanisms, impact of the environment, motor learning
and motor control approaches, as well as the objectives, needs and motivation of the patient.
In this section, combined multisensory approaches as rolling of the hand, touch
bombardment, gentle shaking, withdrawal with resistance, tapping and head and body
movements in space for the purpose of regaining functional control will be discussed.
Rolling of the hand approach can induce a proprioceptive reaction in the joints and
muscles. It consists of and effectively combines tactile and proprioceptive stimuli to facilitate
central pattern generators responsible of extensor motor neurons innervating the hand and
10
finger muscles. At the same time, this technique also triggers spinal generator patterns that
block the existing neural network (Figure 4).
Figure 4: Rolling of the hand.
Another example of proprioceptive-tactile treatment is touch bombardment. The aim
of this approach is to bombard the tactile system with continuous input for light touch
sensory adaptation or desensitization. Deep pressure involves simultaneous stimulation
proprioceptive input and conscious awareness. Proprioceptive discrimination and tactilepressure sensitivity are of paramount importance for high-level tactile discrimination and
stereognosis.
Gentle shaking technique depends on a combination of vestibular system, muscle
spindle and tendons. This technique activates the deep joint receptors at the levels of C1-C3, the
vestibular mechanism which is connected with the cerebellum and the motor nuclei of the brain
stem and the muscle spindles in the neck. Total body inhibition can occur if this technique is
carried out slowly and without interruption in a rhythmical movement. If the pattern is irregular
and rapid, facilitation of the spinal motor generators could be observed [8].
Fourth approach as withdrawal with resistance is an effective way to reduce hypertonicity,
especially in the lower limb. Withdrawal can be elicited by thumbnail, a sharp object, a piece
of ice or plantar light touch stimulus. The withdrawal pattern directly affects alpha motor
neurons that innervate the muscles, which respond in the flexor pattern and concurrently
suppresses alpha motor neurons innervating the antagonistic muscles. If the antagonistic
muscles are hypertonic, hypertonicity is dampened in the neuronal pool of the alpha motor
neurons.
Adaptation of the touch system to continuing pressure forces, resistance and deep
pressure improves the proprioceptive system by a complex adaptation process and a
complex interaction ensues between all motor systems.
Physiotherapists strategically take systematic desensitization into account to integrate
it with the touch system. When the patients are allowed to stimulate themselves, they can
increase the stimulation as much as they can tolerate. In that respect, patients have the
power to control their environment. They can practice adaptation in various conditions.
If the patient feels that the environment is overwhelming, they can develop techniques to
reduce the input from within their own systems by controlling the external world.
Gradual exposure to intense stimulation increases the excitability threshold of the
mechanoreceptors in the skin. Patients benefit from that since it also allows the patient be
able to control the stimulation and realize the objective of the treatment. Moreover, vibration
applied through a folded towel provides proprioceptive input to dampen the sensitivity of the
touch system [60] (Figure 5).
11
Figure 5: Enhancing sensory perception.
Tapping method can be used in patients with peripheral orthopedic muscle imbalance,
pain and neurological disorders with the same potential. Even though the efficacy of taping
method could not be proven in any study, whether it be peripheral instability or CNS
dysfunction, the concept and idea remains the same.
In the inner range, tapping hypotonic groups of muscles effectively reduces the
mechanical pull on the groups of muscles and joints and prevents compensatory stabilization
resulting from the need of the CNS. If hypertonia is the result of peripheral instability,
tapping a hypertonic muscle in the inner range would stabilize the peripheral system and,
consequently, eliminate the need for the CNS to develop hypertonic pattern.
Proprioceptive and vestibular input is the most frequently used combined techniques
of the physiotherapists. So the last approach is head and body movements in space. As a
matter of fact, patient success in nearly all therapeutic tasks depends on coordinated input
of these two sensory modalities.
If the head movement in space takes place without eliminating the surrounding, vestibular
and proprioceptive receptors will be activated to inform the CNS. Direction of the movement
and gravity affects the joints, tendons and muscles. Responses of certain body parts vary
according to the degree of flexibility within the motor system. Bed mobility, transfers, mat
activities and gait involve these two modalities. Despite the fact that all these functional
movements can be performed without feedback mechanisms, the CNS cannot effectively
adapt to the environmental changes without the input to these system. For that reason
alone, if any daily life activity is the impetus for treatment, then examining the integration
of the systems and the effects of combined input becomes of paramount importance [61].
Utilization of large exercise balls (Bobath balls) in treatment is classified under
proprioceptive-vestibular input category. Moreover, trampoline, balance board or similar
apparatus activates the CNS of the patient with large amount of vestibular-proprioceptive
input. Trampoline and balance board are generally used to increase balance reactions, help
the patient to adapt to the position in space and verticality and increase postural muscle
tone (Figures 6 and 7).
Figure 6: Examples of exercises with exercise ball in sitting position.
12
Figure 7: Examples of exercises with exercise ball in bed.
Each one of these techniques can be performed as a viable treatment approach vestibularproprioceptive stimulation.
Holistic treatment techniques based on multisensory input
Two advanced therapeutic interventions that have been developed and accepted in the
last decade are body weight supported treadmill training and constraint-induced movement
treatment. Before the patient is considered functionally independent, he/she should be able
to perform functional activities in their natural environment such as ambulation at home
and be able to eat using the necessary limb. Robots, which constitute the third advanced
therapeutic intervention, offer the therapist and the patients a new and advanced technology
to be aware of the patients’ capacities [8].
Body weight supported treadmill training: In the last decade, BWSTT (Figure 8) has
been accepted by those who are involved in rehabilitation as an alternative therapeutic
approach to give the patients gait training following CNS injuries.
Figure 8: Body weight supported treadmill training.
A treadmill that supports the body weight and pulls the center of gravity anteriorly
would meet the following needs of the CNS by eliminating the environment:
13
1.
Controls and triggers the postural system, which is effective and essential.
2.
Introduces the power required to execute upright ambulation
3.
Controls the stepping strategies to prevent falls.
4. Possesses a cognitive interphase with various motor programs required to perform
the functional activity.
There are studies in the literature that employed body weight supported treadmill
training in patients with incomplete spinal injury [62], Parkinson’s disease [63] and after
[64,65]. Hasse et al., conducted a study on 7 non-ambulatory stroke patients and showed
that body weight supported treadmill training was effective in improving gait and speed of
walking [66].
Miyai et al., [67] showed that, compared to traditional physical therapy, body weight
supported treadmill training had long-term beneficial effects on short-step gait. Further,
improvements in ADL, motor performance and ambulation far exceed those achieved by
traditional physical therapy approaches [68,69].
Constraint-Induced Movement Treatment (CIMT): CIMT (Figure 9) is the treatment of
patients with motor system limitations and involves immobilization of the unaffected arm
to achieve significant motor tasks with the affected arm [70,71]. The focus of CIMT is to
shape the behavior to improve functional use of the affected upper limb. CIMT is based on
the impairment in hand and arm function after a stroke due to alterations in the cortical
representation of the upper limb in the primary sensory cortex, which results in learned
non-use. Learned non-use develops in the early stages after a stroke when the patient grows
a confidence in the unaffected limb and compensates the difficulty by using the affected
limb. This compensation prevents the functional healing of the affected limb [72].
Figure 9: CIMT in activities of daily living.
It has been shown that CIMT is a treatment used effectively in patients with chronic stroke
who has sufficient motor control and would benefit from exercise [73-85], patients who suffered
brain injury [86-88], pediatric patients with hemiplegic cerebral palsy [89-92] and Parkinson’s
disease patients [93,94]. CIMT approach is being used successfully for the rehabilitation of
lower limb in patients with stroke, incomplete spinal cord injury and pelvic fracture. CIMT can
be beneficial in various chronic disorders such as phantom limb pain and aphasia [77].
Even though there are many studies on the beneficial effects of CIMT [73-75], small
sample size, heterogeneity among the patient groups, duration and intensity of the treatment
14
and assessment criteria emerge as the limitations of these studies.
The neurophysiological mechanisms underlying CIMT are based on overcoming learned
non-use and plastic reorganization [95,96]. It has been confirmed that CIMT improves usedependent cortical reorganization in patients with post-stroke paresis of the upper limb [97100]. However, there are questions as to whether the improved motor function of the upper
limb after CIMT is a result of the reduction in learned non-use or of overcoming a sense
of increased effort during movement [101]. Neuroimaging studies such as transcutaneal
magnetic stimulation and functional MRI, elektro-encephalography [101,102] provided us
with the evidence of neuroplasticity and cortical changes with CIMT [78,98,103,104]. These
studies showed that intensive CIMT practice in chronic stroke patients caused cortical
reorganization in the region involved in the voluntary movement of the affected limb [72,105].
Robotics
One of the advanced approaches most popular among clinical community in recent years
is the robotics technology used to regain control of functional movements. Robots are used
for the purpose of achieving an increase in movement patterns both in upper and lower
limbs (Figure 10). It allows safe, intensive and target-oriented rehabilitation in all kinds of
motor disorders, ranging from mild to severe, due to neurological diseases [106]. Robotic
rehabilitation of gait yields successful results in other gait parameters such as speed of
walking and endurance, balance, motor gain in the lower limb, symmetry, step length
and double stance phase [107-109]. While the rehabilitation of the lower limb focuses on
ambulation [110,111] that of the upper limb focuses on the functions of the shoulder, elbow
and wrist during reaching out [112-115]. It is the contribution of robotic devices on the
recovery of functional ambulation that is studied most in patients with spinal cord injury
[110,111] whereas recovery of the upper limb functional movements have been analyzed in
patients with stroke [112-117].
Figure 10: Robotic rehabilitation for upper and lower limbs.
In patients with neurological trauma, robotic devices function as a therapeutic tool and
orthosis, which supports target-oriented training programs based on functional movements
and motor control output [118]. Thanks to its advantages in terms of controllable assistance
or resistance during movement, good repeatability, objective and quantifiable measures of
performance and high motivation through the use of interactive biofeedback, they have the
potential to increase the intensity of rehabilitation [16].
Sensory discriminative retraining
It is based on the principles of intervention strategies and neuroplasticity for the retraining
of sense discrimination. As we all know, motor and sensory systems are connected. Therefore,
even though the focus is on increasing the sensitivity of the somatosensory system and its
ability to respond, ultimate goal is to achieve a good motor control.
15
Somatosensory degradation present in some people can cause locomotion problems
(such as focal hand dystonia) [34]. There is a close relation between all high level perceptive
and locomotor functions. Brain, in order to accurately assess the interactions between
the body and environment, should establish a relation between sensory input and motor
output. Therefore, sensory impairments result in serious problems with motor control [33].
Prevention of abnormal movements and stretch is important so as to be able to implement
effective sensory discrimination training. If abnormal movement patterns are continuously
repeated, person learns this, resulting in negative learning.
Deep receptors should be included in retraining. Although deep receptors are located in
the 3a region, they provide input for proprioception and kinesthesia through deep pressure,
tapping, weight bearing, and muscle tension. These receptors, at the same time, provide
information to the sensory-motor feedback loop that guides the increased contraction and
coordinated movement. Deep receptors also contribute to object recognition (size, shape,
attributes) as well. They also help with static and dynamic joint position and sense of
location, improvement of motor control and control of joint movements.
Sometimes it is challenging to implement retraining of the sense without eliciting
abnormal motor responses. This is an indication for utilization of imagery rather than
physical practice. Imagery refers to creating representations of objects or completion of a
task by without physically using the objects. Therefore, sensory discrimination programs
utilize visual imagery such as playing a musical instrument, motor imagery or mental
rehearsal in sequential tasks to help restore sense [119].
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