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Proprioception: The Forgotten Sixth Sense
Chapter: Posture, Kinesis and Proprioception
Edited by: Defne Kaya
Published Date: August, 2014
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Posture, Kinesis and Proprioception
Feryal Subasi*
Faculty of Health Sciences, Department of Physiotherapy & Rehabilitation, 26 Agustos
Campus, İstanbul, Turkey
*Corresponding author: Feryal Subasi, Faculty of Health Sciences, Department of
Physiotherapy & Rehabilitation, 26 Agustos Campus, İstanbul, Turkey, Tel: +90 216
578 0000/ 3216; Fax: +90 216 578 04 96; E-mail: [email protected]
Abstract
Proprioception refers to the sense of knowing where one’s body is in space and is
classically comprised of both static (i.e. joint position sense) and dynamic (i.e. kinaesthetic
movement sense) components. Following the early observations of Sherrington, muscle
spindles have been shown to provide essential proprioceptive feedback to the central nervous
system, mediating the conscious perception movement and limb position. Proprioception
is known to be a critical source of sensory feedback for the preservation of balance during
upright standing. It is generally accepted that human bipedal upright stance is achieved by
feedback mechanisms that generate an appropriate corrective torque based on body-sway
motion detected primarily by visual, vestibular, and proprioceptive sensory system. Thus,
proprioception largely contributes to postural regulation. When proprioceptive information
was altered (tendon vibration condition), postural behaviour was disturbed for each group.
It has been theorized that failure of stretched and damaged ligaments to provide adequate
neural feedback in an injured extremity may contribute to decreased mechanisms necessary
for maintenance for the balance or postural stability. The results of studies involving acute and
chronic sprains suggest that increased postural and/or balance instability may be related to
both neurological and biomechanical factors from somatosensory information of injured joint.
In the elderly, the involutions of the visual system, the vestibular system, the proprioceptive
system and the central processing mechanisms, induced by aging contribute to affect the
dynamic regulation of the sensorimotor integration and decrease the efficiency of postural
regulation. That’s why proprioceptive training program based on neuromuscular control may
ultimately lead to the development more effective neuro-rehabilitation strategies to enhance
the sensorimotor abilities.
Key Words
Kinesis; Neuromuscular Control; Posture; Postural Control; Proprioception
Historical Background of Proprioception
The somatosensory system conveys information about touch and proprioception. While
a touch is a straight forward sensation familiar to us, proprioception is a mysterious sense,
because we are largely unaware of it during activities of daily living. Only in certain conditions
does this sensation become conscious (e.g. kinaesthetic illusions during muscle vibration) [1Proprioception: The Forgotten Sixth Sense
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4]. However, the history of proprioception has been the subject of discussion for hundreds of
years, with ideas emerging, their rejection, and subsequent re-emergence as scientific progress
takes its tortuous path. In reading some of the 19th century accounts, the sophistication of
the ideas and clarity of expression are astonishing. An account of early speculations and the
rise of a proposal for a “sixth sense” are provided by Wade [5]. Aristotle firmly believed that
there were only five senses: sight, hearing, smell, taste, and touch. He specifically excluded
the existence of a sixth sense. Speculations about a muscle sense date back at least to the 17th
century [6]. William Harvey speculated about the fact that muscles which move the fingers lie
in the forearm. “Thus, it is perceived and so the fingers are felt to move, but truly we neither
perceive nor feel the movement of the muscles, which are in the elbow”. Discovery of the sixth
sense, the muscle sense, is attributed to Bell [1,5,7] . He posed the question, “Do muscles have
any other purpose to serve than merely to contract under the impulse of their motor nerves?”
He concluded, “We are sensible of the minuet changes of muscular exertion, by which we know
the position of the body and limbs, when there is no other means of knowledge open to us.”
Bell also speculated about whether the signals were of central or peripheral origin. The idea of
a muscle sense was debated repeatedly during the 19th century. German physiologists talked
about the “Muskelsinn” What was meant here was not a sensation originating in the muscles
themselves, but in the brain. It was also referred to as a “sensation of innervation”. The idea was
that whenever we willed a movement, this gave rise centrally to sensations of muscular activity
[1]. The Scottish physiologist Charles Bell was first to identify the fundamental anatomical
basis for sense/perception and movement: ‘Between the brain and the muscles there is a circle
of nerves;one nerve [ventral roots] conveys the influence from the brain to the muscle, another
[dorsal roots] gives the sense of the condition of the muscle to the brain’. Bell included within
this muscular sense the senses of position and movement, and other senses evoked by mucle
contraction [5,7]. However, the term “proprioception” first used by Sherrington at the start of
twentieth century, is generally used to describe the unconscious perception of movement and
spatial orientation arising from stimuli within the body [8,9]. Traditionally, however, the term
proprioceptors has been restricted to receptors concerned with conscious sensations [1], and
these include the senses of limb position and movement, the sense of tension or force, the
sense of effort, and the sense of balance. On the other hand, Kinaesthesia, a term introduced
by Bastian, is used here to refer to sensations of limb position and movement [1].
Definition of Proprioception
Proprioception is a component of the somatosensory system which plays an important
role in normal human performance. Its main aim is to provide afferent information on the
position and movements of a joint [10,11]. Proprioception is the flow of signals arising from
the receptors of muscles, tendons, joint capsules, and the skin, and can be also defined as
‘a special type of sensitivity that informs about the sensations of the deep organs and of the
relationship between muscles and joints, generate afferent information that is crucial to the
effective and safe performance of motor tasks’ [6,8,9].
It includes ‘conscious’ and ‘unconscious’ components, an important sensory system,
not only allows people to detect the position and motion of limbs, but also provides the
sensation of force generation. Therefore, a person can regulate force output properly [9,1214]. Proprioceptors precisely measure physical properties, such as muscle length, tendon
tension, joint angle or deep pressure [6]. It provides information on the physics of the body, the
momentary distribution and dynamics of masses, forces acting on the limbs and their highly
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nonlinear interactions. The maps derived from these complex calculations not only guide body
movement, they also (together with touch) sense the size and shape of objects and measure the
geometry of external space. Weight-one’s own and that of objects is measured independently
by pressure sensors and muscular tension.
Based upon neurophysiological studies, convention has identified four components of
proprioception:
(1) The kinaesthetic sense or kinaesthesia (i.e. sense of position and movement sense).
(2) Sense of tension and force.
(3) Sense of balance.
(4) Sense of effort or heaviness.
Clinically, most attention is focused on the kinaesthetic sense, namely that of position and
movement [8].
The process of proprioception is unfortunately impaired from injury and disease. For
example, knee and ankle ligament injuries have been shown to reduce proprioception
[4,15-17]. These situations are true for both osteoarthritis and rheumatoid arthritis. With
deficient proprioception, a person may also exhibit muscular weakness [14]. At the knee joint,
proprioception is mediated by feedback from specialized receptors located in intra-articular
tissues, such as ligaments and capsules, and also from those receptors located in extraarticular tissues, such as tendons and muscles [16,18]. Neuropathies, most notably diabetic
neuropathy, can cause also significant loss of proprioception [19]. Proprioception has also
shown decrease with age [1,13,19,20]. If the CNS is denied sensory in flow from the active limb
for example, by deafferentation a profound impairment of the accuracy of all but the fastest,
ballistic movements inevitably ensue [11]. Despite the lack of research on compensatory
stepping in Parkinson Disease (PD) subject, research on voluntary movement suggests that
PD subjects may exhibit hypometria because they overestimate the length of their movement
due to abnormally integrated proprioceptive input [21]. On the other hand person with low
back pain seem to have altered proprioceptive sensitivity due to less refined position sense of
the lower back [22].
With deficient proprioception, a person may exhibit muscular weakness [9]. The level of
muscle activation, whether it is preparatory or reactive, greatly modifies its stiffness properties.
From the mechanical perspective, muscle stiffness is the ratio in change of force to the change
in length. Muscles that are stiffer resist stretching episodes more effectively. And more provide
dynamic restraint to joint displacement [2,3]. But, high stiffness decreases electromechanical
delay or would not permit the fast joint motions necessary for physical activity [3]. Chronic
overloading to muscle and tendon may result in connective tissue proliferation thus
desensitizing Golgi Tendon Organs (GTOs) and increasing muscle spindle activity [3].
Neurological Proprioception Mechanisms
The components of proprioception: Proprioception denotes the process by which
information about the position and movement of body parts is related to the central nervous
system [3,9]. Sherrington’s contributions are fundamental due to the classification of sensitivity
[9].
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a. Exteroceptive sensation: This is external surface sensation. It includes touch,
pressure, pain, and hot and cold temperatures, which are globally known as general
exteroceptive sensations; it also includes other more specialized sensations such as
sight, hearing and smell, which together form special exteroceptive sensation.
b. Proprioceptive sensation: This covers a series of impressions on the functional state of
the joints and muscles. If the individual is aware of these impressions, this is conscious
proprioceptive sensation (awareness of passive and active movements, and the attitude or
position of a somatic part of the body, kinaesthesia; If he or she is unaware of them, this
is called unconscious proprioceptive sensation (relating to balance, tone and muscular
coordination). There is also a special proprioceptive sensation, called labyrinthine.
c. Interoceptive sensation: This is found in the viscera and vessels (pain, oppression,
etc.) and is of a general nature; it can be divided in areas such as gustatory and olfactory
(Table1).
Receptors
Location
Function
Superficial somatic sensations
(extroceptive)
Pacinian corpuscles
Merkel’s disks
Meissner corpuscles
Krause bulbs
Ruffini corpuscles
Free nerve endings
Rapid adaptations, touch, vibration,
Slow adaptations, tactile sensations, pressure
Rapid adaptations, tactile sensations
Temperature receptors
Rapid adaptation, sustained pressure
Nociception, tactile stimuli endings
Profound somatic sensation
( proprioceptors)
Golgi receptors
Ruffini corpuscles
Pacinian Corpuscles
Krause’s free endings
Muscle receptors
Pacinian corpuscles
Kühne’s spindles
Golgi organs
Free nerve endings
Deep sensations
Table 1: Sensory receptor organs [9].
Signals from this sensory orchestra are sent by afferent nerves through the spinal cord to
the somatosensory, motor and parietal cortices of the brain, where they continuously feed and
update dynamic sensory-motor maps of the body [6]. The current (but not universal) view is
that kinaesthetic sense is provided predominantly by muscle spindle with some contribution
from skin and joint receptors; the sensations of force is provided by GTOs; and the sense of
balance is provided by the vestibular system. Sense of effort, which should be distinguished
from the peripheral sense of force, is thought to be central [8]. Following the early observations
of Sherrington, muscle spindles have been shown to provide essential feedback to the central
nervous system, mediating the conscious perception of movement and limb position as the
principal proprioceptors [8,13,18]. Proprioceptive messages undergo a two-fold processing at
different levels in the CNS: cognitive processing, which is responsible for the body’s awareness
of its position and movements and contributes to spatial orientation ability as well as the
ability to locate and reach objects in extra-personal space, and sensorimotor processing, which
operates via reflex and automatic loops and has decisive effects on the regulation of posture
and movement as well as participating in their central programming [23]. While conscious
proprioception is essential for proper joint function in sports, activities of daily living, and
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occupational tasks, unconscious proprioception modulates muscle function and initiates reflex
stabilization. Much effort has been dedicated to elucidate the mechanical function of articular
structures and the corresponding mechanical deficits which occur secondary to disruption of
these structures [24]. Therefore, the using of proprioceptive mechanisms helps to correct or
perfect motor abilities and conscious proprioceptive perception provides awareness of posture
and recognition of the body schema, allowing for their eventual correction [9]. Muscular
weakness, proprioceptive deficits and range of motion deficits [25] may challenge a person’s
ability to maintain their Centre of Gravity (COG) within the Base of Support (BOS) or in other
words cause them to lose their balance [26].
Neuroanatomical Components of Proprioception System
The signals are transmitted to the spinal cord via afferent (sensory) pathways. The
efferent (motor) response to sensory information is termed neuromuscular control [3,27].
Input from peripheral receptors ascends through the dorsal column in the spinal cord and
subsequently arrives in the medulla. They represent one of the subconscious functions of
the proprioceptive system [7,28]. A second ascending system and the anterolateral system,
mainly deal with thermal and noxious stimuli, but also relay some pressure information [28].
Another destination is cerebellar regions, which are so important for (subconscious) regulation
of postures, balance, and movement in general [7]. At the head of the hierarchy is the cerebral
cortex, with two relief stations: the somatosensory area and motor areas, through which a
trans cortical loop of variable gain and relatively slow execution is established. For the afferent
nerves, there are two ways in which sensations reach the cerebral cortex to become conscious,
they are the lemniscal system that carries precise time and space information, and the indirect
extralemniscal system, with imprecise space and time characteristics. For efferent nerves,
there is the pyramidal path, a prolongation of the pyramidal neurones of the motor cortex
that is directly and indirectly projected the motor neurones of the anterior horn of medulla, to
voluntary motor function [9].
Posture, Postural Control and Proprioception
The Posture Committee of American Academy of Orthopedic Surgeons, 1947 define posture
as: the relative arrangements of parts of the body. Good posture is that state of muscular
and skeletal balance which protects the supporting structures of the body against injury or
progressive deformity irrespective of the attitude (erect, lying, squatting and stooping) in which
are working or resting. Under such conditions the muscles will function most efficiently and
optimum positions are afforded the thoracic and abdominal organs. The position of one point
(segment) affects other segments and the overall posture [25,29]. A basic condition for correct
posture is minimal stress, therefore, if a certain position increases stress, the postural body
adaptation is incorrect [25,30,31].
While balance is the more commonly used term, postural stability is a broader term which
involves the alignment of joint segments in an effort to maintain the COG within an optimal
range of the maximum Limits of Stability (LOS) [26]. To achieve balance, both dynamic and
inert structures are responsible for postural stability [32]. The vertical orientation of the
body in the upright standing position is also maintained by a dynamic interplay of vision,
proprioception, haptic contact cues, efferent control and internal models [15,22] Theoretically
balance has been also static and dynamic, while static balance is the body’s ability to keep
COG in the base of support; dynamic balance is the active movement of centre of pressure
during standing, walking or execution of sport skills [33,34].
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Good posture is a state of musculoskeletal balance that protects the supporting structures
of the body against injury or progressive deformity. This musculoskeletal balance is important
not only at rest but also with dynamic activity [32]. Good posture is also a good habit that
contributes to the well–being of the individual. The structure and function of the body provide
the potential for attaining and maintaining good posture. Conversely, poor posture is a bad
habit and, unfortunately is all too common. Postural faults have their origin in the misuse
of the capacities provided by body, not in the structure and function of the normal body. In
other words, correct posture is the position in which minimum stress will be applied to each
joint [25,31]. Any position that increases the stress to the joint may be called faulty posture.
If the individual has strong and flexible muscles, faulty postures may not affect the joints
because of the individual ability to change position readily, so that the stresses do not become
excessive. If the joints are stiff or too mobile and the muscles are weak, the posture cannot
be easily altered to the correct alignment and the result can be some form of pathology. The
pathology may be due to the cumulative effects of repeated small stresses over a period of time
or constant abnormal stresses over a shorter period of time [31].
Muscle proprioceptive messages provide the main information necessary for coding
postural configurations and body movements as well as for exerting both reflex and automatic
controls on these configurations and movements [23]. Postural muscles are hungry for signals:
Instability and gravity feed them through proprioception. The reduction of motor experiences
(hypokinesis) can lead to a progressive proprioceptive and postural deficit with functional
joint instabilities, impaired capacity of equilibrium and increased risk of fall. This situation is
responsible for the choice of more and more simplified motor tasks and a further worsening of
hypokinesis [12].
Effective motor control is accurate sensory information concerning both the external and
internal environmental conditions of the body. During goal-directed behaviour, such as picking
up a box while walking, provisions must be made to adapt the motor program for walking
to change occurring in the external environment (uneven ground) and internal environment
(change in the centre of mass because of the additional load). These provisions are stimulated
by sensory triggers occurring in both feedback (mechanoreceptor detection of altered support
surface) and feed forward (anticipating centre-of-mass change from previous experience)
manners. Although some of the afferent information may be redundant across the 3 sensory
sources (somatosensory, visual, vestibular), specific unique roles are associated with each
source that may not be entirely compensated for by the other sensory sources. For example,
proprioceptive information plays an integral role in the ability to modify internal models used
with feed forward control that has been demonstrated to be only partly compensated for by
visual information [2].
Postural control is a particularly complex system that involves the integration of various
sensory and motor components [8,18,35]. Maintenance of postural control includes the
integration in the vestibular nuclei of sensor neural information of three types, vestibular,
visual and somesthetic, to generate a context-specific motor response which leads to control
antigravity activity and gaze [36]. It is controlled from the afferent side and involves the central
processing of peripheral sensory input from vestibular, visual, and proprioceptive pathways,
whereas the efferent side involves the precise recruitment of specific (and varying) populations
of motor units [18]. Figure 1 summarizes how to effect of absence of load on postural muscles
and bones.
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Absence of Load +
Instability
Proprioceptive flow
Muscle tone, Muscle
trophism
Mechanical Load Mechanical Load
(compression) ( traction)
Bone Modelling
Figure 1: Functional and structural consequences of the absence of load and instability on postural muscles and bearing bones
[12].
However, most daily activities such as walking, climbing stairs, or throwing a ball require
static foot placement with controlled balance shift. So, balance should be considered both
a dynamic and static process. Balance movements also involve motions of ankle motions of
ankle, knee, and hip joints, which are controlled by the coordinated actions along the kinetic
chain [26].
The ability to select and reweight alternative orientation references adaptively in conflictual
demanding situations is considered as one of the main issues for postural control. Recent
models of postural control have proposed the controls of self-motion and self-orientation to
depend on how the Central Nervous System (CNS) internally reconstructs, from sense data,
the physics (kinematics and kinetics) of our own movements and of those of the environment
with which we interact [35].
The lack of variability in posture and movement might lead to abnormal mapping of the
sensory cortex, which in turn may lead to further altered postural and motor control [37]. The
body schema, in brief, is the internal, dynamic representation of the spatial and biomechanical
properties of one’s body, and is derived from multiple sensory and motor inputs that interact
with motor systems in the generation of actions [38]. Figure 2 shows how proprioception
can negatively influence and how impaired proprioception may affect postural strategy and
internal representation of the body leading to decreased variability, undue loading and pain.
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Peripheral
Proprioceptive
impairment
Decreased Back
muscle endurance
Decreased inspiratory
muscle endurance
Altered sympathetic
activation
Central
Altered postural strategy
Stiffening
Fear
Passive
Altered
IRoBO/frames
Decreased postural strategy variability
Undue loading
Pain
Recurrence
Figure 2: Proprioceptive impairment leading to decreased postural strategy variability, and pain [37].
The main systems that contribute to the properties of the body schema include: (a)
proprioceptive and somatosensory systems, (b) vestibular system, (c) visual system, and (d)
movement systems and an efference copy-that is, the neural copy of a movement command
that is sent to the parietal cortex to be mapped onto the body schema to generate expected
sensory outcomes, and to the premotor cortex in preparation for rapid corrective adjustment
of movements when errors between the expected and actual sensory outcomes are detected
[38]. The body image is also a cognitive representation of the body that is based on stored
knowledge and experience and is thought to underlie perceptual judgements. In addition,
there is the body schema that is dependent on ongoing proprioceptive input, operates largely
unconsciously, and is concerned with body movements. Areas of cerebral cortex attributed
to these functions are the parietal cortex for immediate guidance of action while conscious
perception and memory may be associated with the insula. Complex movements require a lot
more energy to execute than simpler ones. By comparison, a normal subject can forget about
their body in daily routines. It takes care of itself. In simplistic terms, this is because the body
schema functions to control posture and movement unconsciously, without the intervention
of a body image [1].
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Proprioceptive Training
The importance of proprioception to injury prevention and rehabilitation is generally
accepted. Impaired proprioception has been associated with an increased risk for joint damage,
athletic injury, and falls. In addition, decreased joint proprioception is also thought to influence
the progressive joint deterioration associated with osteoarthritis, rheumatoid arthritis [19]. In
patients with musculoskeletal impairments such as spasmodic torticollis (i.e., a pathological
condition whereby torsion of the cervical spine due to neck muscle spasm occurs) changes
in the reference system used in the control of body orientation have been demonstrated [22].
Even without pathologies, ageing is believed to adversely affect balance, particularly by
producing changes at every level of postural control. Several studies showed that, at neuro
sensorial afferences level, ageing is characterized by a decreased vestibular excitability due
to a lower number of cells in the utriculus and sacculus maculae and in the semi-circular
canals [36]. It has been also demonstrated in several studies that the risk for falling in the
elderly population correlates with postural sway, a variable that is determined in large part of
proprioception [19]. The regular practice of proprioceptive activities allows retaining an excellent
response to somatosensory input. On the other hand, the research of the declines in balance
in the elderly implied when postural muscles are vibrated and the CNS uses these signals for
postural control; the kinaesthetic illusions will cause excessive corrective displacement of the
centre of mass to avoid falling. Based on the results, during standing vibration of triceps, surae
muscles can give the illusion of forward leaning and therefore, the subject will compensate
with a backwards shift of the centre of mass, even to the point of falling [39].
Deficient neuromuscular of motion during athletic tasks may predispose athletes to low
back injuries as well as injuries of lower extremity. These results suggest that the patients
with chronic or acute ankle sprain had increased postural sway and /or balance instability
[17,26]. Many studies suggested also that ligamentous injury to the knee has proven to affect
the ability of subjects to accurately detect position [26]. Thus, it was proposed that for balance
corrections ankle inputs trigger responses in stretched lower leg muscles. Bloem et al., have
also noted that lower leg propriocepsis serves to trigger postural responses in ankle and helps
to shape other responses within postural strategy [40].
Proprioceptive exercise seeks to improve joint and limb position sense. These exercises
are typically used after an injury has occurred to the joint that has resulted in a deficit in
proprioception [19] . The objective of proprioceptive training is to restore the neurosensory
properties of injured capsule ligamentous structures, and enhance the sensitivity of uninvolved
peripheral afferents. Closed chain exercises, which can accomplish joint compression, are
believed to maximally stimulate articular receptors. Applying elastic bandage or orthotic
interventions can provide additional proprioceptive and kinaesthetic information by stimulating
cutaneous receptors [26]. Postural control may rely upon the proper use and function of sensory
afferences, but could also depend on the muscular strength of lower limb. Based on results of
the research, it can be concluded that good proprioception is important for promoting dynamic
joint and functional stability in sports (standing, walking and running) and in daily activities
living. Lower leg proprioception may be considered the trigger for postural responses.
However, there are a lot of studies showing that the proprioception process is disrupted
from injury, disease, aging and it was also explained that disturbances in proprioception
process influence postural control the reseraches on neuromuscular control improving the
ability to withstand postural disturbance through a better use of the sensory information is
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relativeley few. Due to the lack of the sufficient clinical data based on specific proprioceptive
training programs or the role of proprioceptive inputs to the control of posture there are a lot
of questions need to be explained.
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