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Article history:
Received 6 November 2014
Received in revised form
18 December 2014
Accepted 15 January 2015
Keywords:
Assessment
Musculoskeletal disorder
Proprioception
Rehabilitation
* Corresponding author.
ijezon).
E-mail address: Ulrik.roijezon@ltu.se (U. Ro
http://dx.doi.org/10.1016/j.math.2015.01.008
1356-689X/ 2015 Elsevier Ltd. All rights reserved.
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
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assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
2
Table 1
Mechanoreceptors of the human body.
Mechanoreceptors
Type
Stimulation
Muscle-tendon unit
Muscle spindle
Muscle length
Velocity of change of muscle
length
Active muscle tension
Low and high load tension and
compression loads throughout
entire ROM
Joint
Fascia
Skin
Martin and Jessell (1991), Rothwell (1994), Yahia et al. (1992), Sojka et al. (1989),
Johansson et al. (1990), Needle et al. (2013).
2012). They are highly sensitive and their density varies widely
throughout the body, reecting different functional demands. The
sub-occipital muscles of the neck have an exceptionally high density of muscle spindles, thought to reect the cervical spine's
unique role in head and eye movement control (Liu et al., 2003).
Importantly the sensitivity of the muscle spindles can be adjusted
via innervation of the polar ends of the intrafusal muscle bers by
gamma motorneurons (Gordon and Ghez, 1991).
Joint proprioceptors have historically been considered limit
detectors, stimulated at the extremes of joint range-of-motion
(ROM) (Burgess and Clark, 1969). However it is now known that
joint proprioceptors provide input throughout a joint's entire ROM
under both low and high load conditions stimulating strong discharges from the muscle spindle and are thus vital for joint stability
(Sojka et al., 1989; Johansson et al., 1990; Needle et al., 2013).
1.2. Role of proprioceptors
Proprioceptive information is processed at the spinal level, brain
stem and higher cortical centers, as well as subcortical cerebral
nuclei and cerebellum (Bosco and Poppele, 2001; Amaral, 2013;
Lisberger and Thach, 2013; Pearson and Gordon, 2013). The information is mainly transferred, via several ascending pathways, to
the medulla and thalamus and then to somatosensory cortex
(conscious proprioception); or via the spinal nucleus to the cerebellum (unconscious proprioception) (Fig. 1). Cervical proprioceptive information is also transferred to the superior colliculus in the
midbrain which is thought to be the reex center for eye and head
movement co-ordination (Corneil et al., 2002). Cervical proprioceptors also have important central connections to the vestibular nuclei (Figs. 1 and 2) and are involved in reexes involving
head and eye movement control and balance (the cervico-ocular,
cervico-collic and the tonic neck reex) (Bronstein et al., 1991;
Gdowski and McCrea, 2000; Peterson, 2004). These work in
conjunction with other reexes acting on the neck and eye
musculature associated with the vestibular and visual systems
(Fig. 3).
The role of proprioception in sensorimotor control is multifold.
To plan appropriate motor commands, the CNS needs an updated
body schema of the biomechanical and spatial properties of the
body parts, supplied largely by proprioceptors (Maravita et al.,
2003). Proprioception is important also after movement for comparison of actual movement with intended movement, as well as
the predicted movement supplied by the efference copy (corollary
discharge). This is suggested to have importance for motor learning
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
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assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
Fig. 1. Ascending pathways relating to proprioception. A) Dorsal column Medial lemniscus pathway to Cerebral Cortex for conscious proprioception. Proprioceptive information is
transmitted via the dorsal column which is formed by axons of the dorsal root ganglia. These travel to the medulla to synapse in one of the dorsal column nuclei e the gracile nucleus
(lower body) or cuneate nucleus (upper body and arm). These bers then sweep ventrally and medially to cross the midline to form the medial lemniscus which projects to the ventral
posterior lateral (VPL) nucleus of the thalamus and then projects to the relevant somatosensory area of the cerebral cortex. Lower limb axons of the dorsal spinocerebellar tract (B) also
branch to the nucleus z which then joins the medial lemniscus and projects information from the lower limb to the cerebral cortex. Input from the face, teeth and head enter the brain
stem at the level of the pons and synapse in several brain stem nuclei including the mesencephalic nucleus, main sensory nucleus and the spinal nuclei of the trigeminal nerve. Some
bers also ascend to join the spinotrigeminal tract with input from the upper cervical spine. From the reticular formation they join the trigeminothalamic tract to the ventral posterior
medial (VPM) thalamic nucleus and this is relayed to the relevant area of the somatosensory cerebral cortex. Input from the cervical spine is also projected via the spinotectal tract to the
superior colliculus which is located in the midbrain and is a reex center for co-ordination between the visual system and the neck. B) Spinocerebellar pathway to the Cerebellum for
unconscious proprioception. For the trunk and lower part of the leg, dorsal root ganglion cells synapse in the dorsal nuclei then on to the gracilis funiculus to form the dorsal spinocerebellar tract which enters the cerebellum via the inferior cerebellar peduncle. The ventral spinocerebellar tract also supplies input from the lower limb to the cerebellum via the
superior cerebellar peduncle. For the upper limb, dorsal root ganglia from the cervical spine ascend in the cuneate fasciculus to the external cuneate nucleus forming the cuneocerebellar tract and enter the cerebellum via the inferior cerebellar peduncle. Proprioceptive input from the face and head projects to the spinal trigeminal nucleus plus the main sensory
nucleus to form the trigeminocerebellar tract and ascends to the cerebellum via the inferior peduncles. Information is also projected from the mesencephalic nucleus to the cerebellum
via the superior cerebellar peduncle (Rothwell, 1994; Bosco and Poppele, 2001; Amaral, 2013; Pearson and Gordon, 2013; Lisberger and Thach, 2013).
In cervical pain disorders oculomotor and eyeehead coordination tests are often included as non-specic proprioception
tests due to the neurophysiological connections between cervical
proprioceptors and visual and vestibular organs (Treleaven, 2008).
3. Causes of altered proprioception
Disturbed proprioception has been found to be associated with
several musculoskeletal disorders and/or experimental conditions
following pain, effusion and trauma as well as fatigue.
3.1. Pain
Abundant research has reported disturbed proprioception in
acute and chronic musculoskeletal pain disorders at the cervical
lander et al., 2008; Kristjansson and
(Treleaven et al., 2003; Sjo
Oddsdottir, 2010) and lumbar (Lee et al., 2010; Williamson and
Marshall, 2014) spine, as well as upper (Juul-Kristensen et al.,
2008; Anderson and Wee, 2011) and lower (Sharma et al., 2003;
Salahzadeh et al., 2013) extremities. In the presence of pain,
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
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assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
Fig. 2. Ascending and descending pathways and connections to the vestibular and visual systems relevant for proprioception.
3.2. Effusion
3.4. Fatigue
The term joint effusion refers to swelling within a joint capsule,
common after acute extremity joint injury, potentially persisting
for extended periods of time (Frobell et al., 2009). Joint effusions
Fig. 3. Proprioceptive reex activity relating to balance and head and eye movement control.
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
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assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
Table 2
The role of proprioception in sensorimotor control for feedback (reactive) control, feed-forward (preparatory) control and regulation of muscle stiffness is summarized below.
These control systems are used to achieve specic functional roles of movement acuity, joint stability, co-ordination and balance, and in the case of cervical proprioception,
head and eye movement control.
Role
Source of
proprioceptor
input to CNS
CNS processing
level
CNS processing
characteristics
Feedback
Sensorimotor
Control
Muscle spindle
Spinal cord
Monosynaptic reex
Golgi tendon
organ
Spinal cord
Polysynaptic reexes
Muscle, tendon,
joint, fascia
Cerebral cortex
and subcortical
Polysynaptic reexes
Muscle, tendon,
joint, fascia
Cerebral cortex
and subcortical
Voluntary reaction
Feed-forward
Sensorimotor
Control
Muscle, tendon,
joint, fascia
Muscle, tendon,
joint, fascia
Cerebral cortex
and subcortical
Cerebellum
Regulation of
Muscle Stiffness
Muscle spindle
Spinal cord
Preparatory motor
commands
Copy of motor
command (efference
copy, or corollary
discharge) based on
past events.
Monosynaptic
Golgi tendon
organ
Spinal cord
Polysynaptic
Joint
Spinal cord
Polysynaptic
Muscle, tendon,
joint
Brainstem (and
cerebrum and
cerebellum)
Polysynaptic
(Johansson et al., 1990; Rothwell, 1994; Bosco and Poppele, 2001; Amaral, 2013; Pearson and Gordon, 2013) Lisberger and Thach (2013).
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
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assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
Fig. 4. Calculation of constant error (CE), variable error (VE) and absolute error (AE) in 2-dimensional (A) and 1-dimensional (B) assessments of joint position sense. CE, VE and AE
display different aspects of the ability to reproduce a predetermined target. CE is the deviation from the target where each value is described by a positive (overshoot) or negative
(undershoot) number. CE gives an indication of accuracy as an average magnitude of the movements, and an indication of any systematic error, i.e., whether the person is generally
overshooting or undershooting the target. VE is the variance, or consistency, of the values regardless of how accurate (close to the target) the measures are and provides an estimate
of precision. AE is the absolute difference from the target regardless of direction and gives an indication of the accuracy as overall amplitude of the error without consideration of
error direction (Schmidt and Lee, 2011).
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
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assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
from injured structures to the CNS has been associated with the
onset and progression of peripheral joint OA (Segal et al., 2010) in
humans. This has also been demonstrated in animals where selective ligament and mechanoreceptor resection resulted in a rapid
onset and progression of OA (O'Connor et al., 1985; O'Connor et al.,
1992).
Poor proprioception may also contribute to increased injury risk
(Zazulak et al., 2007) and training directed towards improving
proprioception has been associated with reduced injury risk
(Hupperets et al., 2010). Thus interventions targeting proprioception is relevant both in prevention and rehabilitation of musculoskeletal disorders.
Training methods with the specic aim to improve proprioception commonly involve specic acuity tasks targeting JPS, kinesthesia or sense of force, or some kind of unstable dynamic system
to train balance, co-ordination and dynamic stability and simultaneously train multiple components of the sensorimotor control
system (Lephart et al., 1997). Common to these exercise tasks is that
they involve learning motor skills, explicit or implicit. In relation to
Doyons and colleague's model on sequential learning vs motor
adaptations (Doyon and Benali, 2005; Doyon et al., 2009), explicit
tasks targeting precise movements may have similarities with
motor sequential learning which primarily involves the corticostriatal (basal ganglia) system (conscious and unconscious proprioception); while implicit tasks, involving an unstable system, primarily involves the cortico-cerebellar system (unconscious
proprioception) through motor adaptation due to the inherently
changing (unstable) environment.
Training explicit motor skills, such as precise repositioning
tasks, have shown to have a preferential effect on the reorganization within the motor cortex of the CNS, when compared to muscle
performance training (performed without involvement of motor
skill) of the same body part (Jensen et al., 2005; Adkins et al., 2006).
These plastic changes include increases in protein synthesis, synaptogenesis and map reorganization and are closely related to
improved task performance (Jensen et al., 2005; Adkins et al.,
2006).
Implicit motor skills training, such as with an unstable surface or
object, involves some degree of uncertainty and, therefore,
continuous sensory input, CNS processing, and motor actions and
reactions to adjust motor commands (Taube et al., 2008; Franklin
and Wolpert, 2011). Neurophysiological studies have demonstrated central adaptations at multiple levels due to exercises using
unstable surfaces, including increased cerebellar and subcortical
activity in combination with reduced spinal reex excitability and
cortical activity, and that these adaptations are task specic (Taube
et al., 2008).
A common nding during initial unstable task training is
increased co-activation of agonists and antagonists (Burdet et al.,
2001; Franklin et al., 2003; Cimadoro et al., 2013), related to the
ijezon U, et al., Proprioception in musculoskeletal rehabilitation. Part 1: Basic science and principles of
Please cite this article in press as: Ro
assessment and clinical interventions, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.008
Acknowledgement
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