Anatomy and Physiology
of Proprioception and
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M, LEBs%AR"%P9
PbD, A m C. BUZ SWRltBq PhDTa
Neuromuscular Research Laboratory
University of Pittsburgh
Developing or reestablishing proprioception and
neur~mu~cular
control is a critical component in
motor performance and rehabilitation. Proprioception can be
defined as a special variation of
sensory modality that encompasses the sensation of joint
movement (kinesthesia)and joint
position.
Proprioception involves integrating peripheral sensations
from afferent pathways while
neuromuscular control helps process these signals into coordinated
motor responses through efferent
pathways (Figure 1).
Both the afferent and efferent
pathways comprise the sensorymotor system. Basic science research has provided insight on the
sensory and motor characteristics
of structures that regulate proprioception and neuromuscular
control.
This paper gives an overview
of the sensory receptors that provide joint motion and position
awareness. It addresses the neu-
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ral pathways that integrate peripheral receptors and motor responses, and uses theoretical
models to describe the processing of sensory information for
neuromuscular control. The other
theme articles will discuss practical ways to improve neuromuscular control in injured athletes.
Peripheral receptors for proprioception, called mechanoreceptors,
are located in articular structures,
tendons, muscle, and skin. Mechanoreceptors are special nerve
endings that depolarize in response to tissue deformation.
Therefore, mechanical deformation of tissue is transduced into
neural signals (Grigg, 1994):
As tissue deformation increases, so does the frequency of
discharge and number of mechanoreceptors stimulated. These signals provide sensory information
on intrinsic and extrinsic joint
loads. Mechanoreceptors vary in
shape, location, and function and
can be classified according to their
responses to mechanical stimuli.
They are either slow-adapting
(SA)or quick-adapting (QA),and
either low-threshold or highthreshold.
QA mechanoreceptors decrease their discharge rate to extinction within millisecondsof the
onset of a continuous stimulus,
O 1998 Human Kinetics
September 1998
Descending pathways
Joint receptors
(stimuli: noxious
Muscle
(stimuli:
Muscle
\/
Muscle tone
Static sensitivi
Dynamic sensi ivity
SECONDARY MUSCLE
A FIGURE 1
Afferent and efferent pathways linking peripheral receptors with
muscle spindles and motor responses.
Reprinted from MedicalHypotheses, Vol. 35, H. Johansson & P. Sojka, "Pathophysiological
mechanisms involved in genesis and spread on muscular tension in occupational muscle
pain and in chronic musculoskeletal pain syndromes: A hypothesis," p p 196-203, 0 1991,
by permission of the publisher, churchill ~ivin~stone.
while SA mechanoreceptors continue to discharge. QA's are very
sensitive to changes in stimulation
and are therefore thought to mediate the sensation of joint motion,
while SA's are maximally stimulated at specific joint angles and
are thought to mediate the sensation of joint position.
Articular Mechanoreceptors
Four types of mechanoreceptors
are found in the knee joint: (a)
Pacinian corpuscles; (b) Ruffini
endings; (c) Golgi tendon organs;
and (d) free nerve endings.
Pacinian corpuscles are
low-threshold, QA located in
the medial meniscus, extra- and
intra-articular fat pad, cruciate,
September 1998
meniscofemoral, and collateral
ligaments. They are thought to
mediate the sensation of joint
motion.
Ruffini endings are lowthreshold, SA found in the
superficial layer of the cruciate,
meniscofemoral, and collateral
ligaments. Ruffini endings mediate the amplitude and velocity of
joint rotation and position.
Golgi tendon organ-like endings are high-threshold, SA found
in cruciate, collateral ligaments,
and menisci. These receptors remain silent when the joint is immobile but are stimulated at the
extremes of joint motion.
Free nerve endings are widely
. distributed throughout most ar-
ticular structures. During normal
conditions they are inactive, but
they become active when articular tissues are subjected to damaging mechanical deformation.
Free nerve endings are also sensitive to certain chemical by-products of the inflammatory process.
Tenomscalar -Mechanorecepl.ovs
Muscle spindles, SA mechanoreceptors located in skeletal muscle,
are sensitive to length and rate of
length changes. They have the distinction of being innervated by
gamma motor nerves. Increased
signals from the gamma motor
nerves do not initiate muscle eontraction but they do heighten the
sensitivity of muscle spindles to
stretch. When stimulated, muscle
spindles convey information
about joint motion and position
caused by or due to changes in
muscle length. They can also elicit
a reflex contraction of the agonist
muscles. This is the mechanism,
known as the stretch reflex,
whereby muscle spindles have
the capacity to mediate muscle
activity.
Golgi tendon organs are SA
mechanoreceptors found near the
musculotendinousjunction; they
function by monitoring muscle
tension. When stimulated by high
muscle tension, they cause reflexive inhibition (relaxation) of the
involved muscle.
Cutaneous Mechanoreceptors
The primary role of skin afferents
is to enhance the effects of other
proprioceptive inputs. We know,
for example, that receptors located in the dorsal skin of the
wrist and fingers can provide information on wrist and finger
movements. The contribution of
cutaneous mechanoreceptors to
joint motion and position sense
continues to be explored.
The ProBesslonalJollranall for ASBhIeSic Tmliners amd Tlhemgplas
7
Sensory information from articular, tenomuscular, and cutaneous
receptors is encoded for the central nervous system (CNS) by
populations rather than individual mechanoreceptors. This
property of peripheral receptors
is referred to as ensemble coding
(Johansson et al., 1991).
Since different types of mechanoreceptors have distinct response profiles to the same type
of stimulus (joint motion or
forces), this allows more discrete
sensory information concerning
mechanical stimuli to be transmitted to the CNS. Increases in the
number and diversity of receptors
that are stimulated enhances the
information about mechanical
events occurring in muscles and
joints (Johansson et al., 1991).
These coded signals follow
afferent pathways to three levels
of motor control: the cerebral
cortex, brain stem, and spinal
reflexes (Lephart et al., 1997) (see
Figure 2).
Ascending pathways to the
cerebral cortex provide the con-
scious appreciation of joint position (proprioception) and joint
motion (kinesthesia)that are used
for motor programming. Pathways leading to the brain stem are
responsible for long-loop reflexes
such as postural responses. Reflex
pathways in the spinal cord link
peripheral receptors with motor
nerves and muscle spindles by
way of interneurons. The stretch
reflex arc directly links muscle
spindles with motor nerves.
Johansson et al. contend that
the afferent pathways from
joint receptors do not exert much
direct influence on skeletal
motor nerves, but they do have
more potent effects on muscle
spindles through the gamma
motor nerves.
A relatively small tensile load
on the cmciate ligaments significantly heightens gamma motor
nerve activity, while it takes loads
near ligament failure to elicit activity in larger motor nerves innervating muscle. Therefore,
loads placed on articular receptors will modify the sensitivity of
the muscle spindle system by way
of gamma motor nerves.
Cutaneous receptors and
GTOs can also influence muscle
spindles through gamma motor
nerves and have previously been
associated with protective reflexes. Muscle spindles in turn
regulate muscle activity through
the stretch reflex.
What is the effect of all this
afferent activity? How does it all
come together?
This sophisticated reflex
network between peripheral receptors and muscle spindles is
described by the final common
input theory which suggests that
muscle spindles integrate information from peripheral receptors
and transmit a final modified
signal to the CNS (Johansson et
al., 1991).
This feedback loop is responsible for maintaining muscle tone
at rest and continuously modifying muscle stiffness during dynamic activities via the stretch
reflex. These reflex pathways have
also been implicated in the origin
and spread of muscle tension that
results in chronic musculoskeletal
pain syndromes (Johansson et al.,
1991).
MECHANORECEPTORS
CONTROL
*joint
* muscle
* skin
I MUSCLE I
Vestibular receptors
balance
A FIGURE 2
Neummuscular control pathways and three levels of motor control.
Fmm S.M. Lephart and TJ. Henry, "The physiological basis for open and closed kinetic chain rehabilitation for the upper elmemity."
Journal of Sport Rehabilitation, 5(1), pp. 71-87. @ 1996 by Human Kinetics.
8
Athletic B$lerapy Today
September 1998
The (efferent) motor response of
muscles "transforming neural information into physical energy" is
termed neuromuscular control
(Kandell et al., 1991).Contemporary theories emphasize the significance of preprogramming
muscle activity in anticipation
of joint movements and loads
through practice and repeated
movements.
Sensory feedback from previous movement experiences is
used in advance to preprogram
muscle activationpatterns. This is
described as feed-forward neuromuscular control. These centrally
generated motor commands
are responsible for preparatory
muscle activity and high-velocity
movements.
Preparatory muscle activity
serves several functions that contribute to muscle performance.
Muscle activity increases the stiffness properties of muscle and improves the stretch sensitivity of
the muscle spindle system by
co-activating the gamma motor
nerves that innervate the muscle
spindles. Increased muscle stiffness improves the transmission of
force between muscle and bone by
reducing the time it takes to develop tension (Wilson et al., 1994).
Heightened stretch sensitivity
improves the reactive capabilities
of muscle by providing additional
sensory feedback and superimposing stretch reflexes onto
descending motor commands.
Sensory information about the
movement is then used to evaluate the results and help arrange
future muscle activation strategies.
Feedback neuromuscular control
is characterized by numerous reSeptember 1998
flex pathways that continuously
adjust ongoing muscle activity.Information from joint, muscle, and
skin receptors reflexively coordinates muscle activity to complete
a movement.
This feedback process results
in long conduction delays, however, and is best equipped for
maintaining posture and regulating slow movements. The efficacy
of reflex-mediated neuromuscular control is therefore related to
the level of preparatory muscle
stiffness and muscle spindle sensitivity.
Both feed-forward and feedback neuromuscular control can
be enhanced if the sensory and
motor pathways are repeatedly
stimulated through practice. Each
time a signal passes through a sequence of nerve fibers, the pathways become more capable of
transmitting the same signal.
When these pathways are "facilitated" regularly, memory of that
signal is created and can be recalled to program future movements.
Therefore, repetition enhances
both the memory of a task for
preprogrammed motor control
and reflex pathways for reactive
neuromuscular control (Lephart
et al., 1997).
Summary
Peripheral mechanoreceptors
encode mechanical stimuli into
neural signals, providing both
conscious and unconscious
appreciation of joint motion and
position. Ensemble coding refers
to transmission of sensory information by populations rather
than individual peripheral receptors.
Muscle spindles have received special consideration for
The hdesslsnal JsurnaB far Aglnlaic Teasiners an
their capacity to integrate peripheral afferent information into a
"final common input" and reflexively modifying muscle activity.
The efferent response to peripheral afferent information is termed
neuromuscular control.
Feed-forward and feedback
neuromuscular control utilize
sensory information for preparatory and reactive muscle activity.
Repetitive stimulation of sensory
pathways forms memories of
specific motor tasks that can elicit
reflexive muscle activity or be
recalled to preprogram muscle
activation patterns.
Grigg, P. (1994). Peripheral neural mechanisms
inproprioception. Journal of Sport Rehabilitation, 3,l-17.
Johansson, H., Sjolander, P., & Sojka, P. (1991).
A sensory role for the cruciate ligaments.
Clinical Orthopaedics,268,161-178.
Kandell, E.R., Schwartz, J.H., & Jessell, T.M.
(1991). Principles of neural science (3rd ed.).
Norwalk, CT:Appleton & Lange.
Lephart, S.M., Pincivero, D.M., Giraldo, J.L.,
& Fu, F.H. (1997). The role of proprioception in the management and rehabilitation
of athletic injuries. American Journal of
Sports Medicine, 25,-130-137.
Wilson, G.J., Murphy, A.J., & Pryor, J.F. (1994).
Musculotendinous stiffness: Its relationship to eccentric, isometric, and concentric performance. Journal of Applied Physiology, 76,2714-2727.
rn
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Scoff M. Lephart is an associate professor of
education and orthopaedic surgery, and director of the Neuromuscular Research Laboratory
at the University of Pittsburgh, where he is the
coordinator of graduate sports medicine education.
C. Buz Swanik is an associate professor in the
School of Education and is graduate athletic
training curriculum coordinator at West Virginia University. He received his PhD from the
University of Pittsb&gh.
Tanarat Boonriong was a research fellow at
the Neuromuscular Research Laboratory and
Department of Orthopaedic Surgery at the
University of Pittsburgh. He has recently returned to his home in Thailand, where he is a
practicing orthopaedic surgeon.