80 Volume 37
•
Number 1
•
March 2002
Journal of Athletic Training 2002;37(1):80–84
q by the National Athletic Trainers’ Association, Inc
www.journalofathletictraining.org
The Sensorimotor System, Part II: The Role
of Proprioception in Motor Control and
Functional Joint Stability
Bryan L. Riemann; Scott M. Lephart
University of Pittsburgh, Pittsburgh, PA
Bryan L. Riemann, PhD, ATC, and Scott M. Lephart, PhD, ATC, contributed to conception and design and drafting, critical
revision, and final approval of the article.
Address correspondence to Bryan L. Riemann, PhD, ATC, Georgia Southern University, PO Box 8076, Statesboro, GA 30460–
8076. Address e-mail to briemann@gasou.edu.
Objective: To discuss the role of proprioception in motor
control and in activation of the dynamic restraints for functional
joint stability.
Data Sources: Information was drawn from an extensive
MEDLINE search of the scientific literature conducted in the
areas of proprioception, motor control, neuromuscular control,
and mechanisms of functional joint stability for the years 1970–
1999.
Data Synthesis: Proprioception is conveyed to all levels of
the central nervous system. It serves fundamental roles for op-
timal motor control and sensorimotor control over the dynamic
restraints.
Conclusions/Applications: Although controversy remains
over the precise contributions of specific mechanoreceptors,
proprioception as a whole is an essential component to con-
trolling activation of the dynamic restraints and motor control.
Enhanced muscle stiffness, of which muscle spindles are a cru-
cial element, is argued to be an important characteristic for dy-
namic joint stability. Articular mechanoreceptors are attributed
instrumental influence over gamma motor neuron activation,
and therefore, serve to indirectly influence muscle stiffness. In
addition, articular mechanoreceptors appear to influence higher
motor center control over the dynamic restraints. Further re-
search conducted in these areas will continue to assist in pro-
viding a scientific basis to the selection and development of
clinical procedures.
Key Words: neuromuscular, stability, motor control
T
his is Part II of a 2-part series discussing the current
understanding surrounding peripheral afferent infor-
mation acquisition, processing, and levels of motor con-
trol as they relate to functional joint stability. In Part I, the
sensorimotor system and the mechanisms responsible for pro-
prioception and neuromuscular control as they relate to func-
tional joint stability were addressed. The purpose of Part II is
to build upon and apply the concepts developed in the Part I.
Specifically, we will address the contribution of proprioception
in controlling the activation of the dynamic restraints and mo-
tor control.
The Role of Proprioception in Motor Control
Critical to effective motor control is accurate sensory in-
formation concerning both the external and internal environ-
mental conditions of the body.
1–4
During goal-directed behav-
ior, such as picking up a box while walking, provisions must
be made to adapt the motor program for walking to changes
occurring in the external environment (uneven ground) and
internal environment (change in center of mass because of the
additional load). These provisions are stimulated by sensory
triggers occurring in both feedback (mechanoreceptor detec-
tion of altered support surface) and feedforward (anticipating
center-of-mass change from previous experience) manners. Al-
though some of the afferent information may be redundant
across the 3 sensory sources (somatosensory, visual, vestibu-
lar), 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 in-
tegral role in the ability to modify internal models used with
feedforward control
5,6
that has been demonstrated to be only
partly compensated for by visual information.
7
The role of proprioceptive information in motor control can
be separated into 2 categories.
2
The first category involves the
role of proprioception with respect to the external environ-
ment. Motor programs often have to be adjusted to accom-
modate unexpected perturbations or changes in the external
environment. Although the source of this information is often
largely associated with visual input, there are many circum-
stances in which proprioceptive input is the quickest or the
most accurate, or both.
1
In the above example, modification
of the motor program for walking was required in response to
the uneven support surface. If the person’s vision was fixed
on the box to be picked up, he or she might not have visually
noted the uneven support surface. In addition to alterations in
the plantar cutaneous receptors, muscle and joint mechanore-
ceptors would have reported the degree of altered ankle joint
position and stimulated the motor program modification re-
quired. The planning of movements also requires attention to
environmental constraints.
8
This is especially true with respect
to the selection of strategies for the maintenance of postural
control.
9–11
For example, sensory detection of an unstable
handrail from peripheral signals (kinesthesia, changing joint

Journal of Athletic Training 81
positions) would alter the motor program used to avoid falling
on a slippery staircase. During the planning stages of a move-
ment, visual images are used to create a model of the envi-
ronment in which the movement will occur. Proprioception has
been described as essential during the movement execution to
update the feedforward commands derived from the visual im-
age.
5,6
The second category of roles proprioceptive information
plays in motor control is in the planning and modification of
internally generated motor commands.
2
Before and during a
motor command, the motor control system must consider the
current and changing positions of the joints involved to ac-
count for the complex mechanical interactions within the com-
ponents of the musculoskeletal system.
2
Proprioception best
provides the needed segmental movement and position infor-
mation to the motor control system.
1,2
In the situation of a
single joint moving through a 108 arc of motion, the precise
muscle force required to perform the task depends upon the
joint angle. As one can surmise, the task of determining how
much tension in a muscle is required for a movement becomes
extremely complex and important with movements involving
several joints.
2,4,12
Accompanying each angular change in
joint position are changes in the mechanical advantages as-
sociated with all the muscles that traverse the joint. Many tasks
involve a sequence of overlapping joint movements. The mo-
tor control system must consider the multiple motions occur-
ring as both a direct function of muscle activation and indi-
rectly from intersegmental dynamics (movement of one joint
inducing movement of another). Proprioception provides much
of the information required to solve all these movement prob-
lems.
2,4,7,12,13
Role of Proprioception in Sensorimotor Control of
Functional Joint Stability
Motor control for even simple tasks is a plastic process
3
that undergoes constant review and modification based upon
the integration and analysis of sensory input, efferent motor
commands, and resultant movements. Proprioceptive infor-
mation stemming from joint and muscle receptors, as previ-
ously demonstrated, plays an integral role in this process. Un-
derlying the execution of all motor tasks are particular events,
often very subtle, that are aimed at preparing, maintaining, and
restoring stability of both the entire body (postural stability)
and the segments (joint stability). With respect to joint stabil-
ity, these actions represent neuromuscular control. Propriocep-
tive information, first recognized and described by Sherring-
ton
14
almost 100 years ago, is essential to maintaining both
types of stability. Because articular mechanoreceptors are be-
lieved to become disrupted in conjunction with joint injury,
this section will focus on the role articular mechanoreceptors
serve in sensorimotor control over functional joint stability. A
discussion of the contribution of articular receptors to postural
control has recently been published.
15
Since the work of Palmer,
16
one of the major tenets con-
cerning the role of joint afferents in functional joint stability
has been direct reflexive activation of alpha motor neurons (a
MNs).
17–19
This belief, however, is not uncontested
20–22
and
represents one of the biggest ongoing debates within the sen-
sorimotor system. Direct evidence supporting the existence of
ligament-muscle reflexes has largely arisen though direct elec-
tric and mechanical stimulation of the knee, ankle, and shoul-
der ligaments or capsule (or both).
19,23–26
Similar to the use
of electric stimulation on afferent nerve fibers to document
cortical projections, the applicability of these findings to nor-
mal physiologic function remains speculative and uncertain.
27
Specific to the mechanical stimuli, the loading required to elic-
it a-MN responses has been criticized as exceeding normal
physiologic loads.
22,28,29
Even assuming that the ligament-
muscle reflex exists, one must question its effectiveness in
contributing to joint protection because of the latency
times
22,29,30
and weak response magnitudes,
31
especially in
comparison with reflexes stimulated from muscle spindles.
28
Despite the controversial basic science and empirical support,
in vivo human studies involving ankle and knee joint pertur-
bations in conjunction with electromyography have been con-
ducted and have produced varying results.
17,18,32–40
For ex-
ample, at the ankle, the number of investigations
demonstrating increased latencies with mechanically or func-
tionally unstable joints (or both)
32–35
is matched by just as
many studies failing to elicit differences.
36–40
Several factors
must be considered with respect to the conclusions that can be
drawn from this experimental model. These are reviewed in a
subsequent paper describing sensorimotor measurement tech-
niques.
41
In contrast with the seemingly controversial activation of a
MNs, joint afferents are more unanimously credited with elic-
iting similar effects on gamma motor neurons (g
MNs).
21,22,29,42,43
Interestingly, and in opposition to what
many have claimed, Freeman and Wyke
43
attributed increases
in muscle activity in response to joint mechanoreceptor stim-
ulation to activation of g MNs, not a MNs. Since their study,
many investigations have demonstrated reflexive action of
joint afferents on g MNs through electric stimulation
44
and
tissue traction using force levels below those associated with
tissue damage and nociception.
21,22,42,45,46
Increased g-MN ac-
tivation, which may occur from input arising from cutaneous
or muscle sources as well as descending supraspinal com-
mands, serves to heighten muscle spindle sensitivity. What
does increased muscle spindle sensitivity have in connection
with sensorimotor control of functional joint stability? The an-
swer to this question will become evident in the following
discussion of stiffness.
Muscle stiffness is defined as the ratio of change in force
per change in length.
29,47,48
In contrast to muscle stiffness,
which refers specifically to the stiffness properties exhibited
by tenomuscular tissues, joint stiffness involves the contribu-
tions of all of the structures located within and over the joint
(muscles, tendons, skin, subcutaneous tissue, fascia, ligaments,
joint capsule, and cartilage).
49–51
Several studies have been
conducted in attempts to quantify the contributions of each
structure to joint stiffness. These studies generally indicate that
the muscle and joint ligamentous and capsular structures tra-
versing the joint contribute equally in passive modes.
50,51
The constituents of muscle stiffness can be categorized into
intrinsic and extrinsic (reflex) components.
52
Many of the el-
ements comprising muscle tissue and connecting noncontrac-
tile tissues (tendon, fascia) contain high amounts of collagen
and, therefore, exhibit the properties of elasticity and viscosity
when stretched. In addition, the intrinsic component encom-
passes the number of actin-myosin cross-bridges (level of
muscle activation) existing at an instant,
29,53
as well as the
factors of both single muscle fibers (ie, sarcomere length-ten-
sion and force-velocity relationships) and whole muscles (ie,
arrangement of muscle fibers within a muscle).
54
The levels
of activation existing within a muscle at a given instant are a

82 Volume 37
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function of both preceding reflexes and descending influences
on the a-MN pool.
29
The extrinsic contribution of muscle stiffness arises from
the increased reflexive neural activation of the muscle. This is
largely determined by the excitability of the motorneuron
pool,
29
which in itself is largely dependent upon the sensitivity
of primary muscle spindle afferents eliciting autogenetic and
heterogenetic reflexes, as well as descending neural com-
mands. Superimposed on these constituents are a number of
interacting factors involving the whole muscle-joint complex,
such as joint kinematics (ie, angle, velocity), attachment sites
(ie, exact location of muscle insertions), and tissue transitions
(ie, muscle, tendon, bone).
54
From a theoretic perspective, increased muscle stiffness and,
therefore, enhanced joint stiffness, appears to be a beneficial
characteristic for augmented functional joint stability. First,
stiffer muscles should potentially resist sudden joint displace-
ments more effectively.
29,47,55,56
Although not all destabilizing
forces may be entirely countered, many could potentially be
lessened in magnitude, thereby reducing the incidence of joint
subluxation and injury. This may be essential in maintaining
functional stability when mechanical stability is deficient and
may assist in explaining the moderate correlation between
hamstring muscle stiffness and functional ability in anterior
cruciate ligament (ACL)-deficient individuals found by
McNair et al.
47
Directly, voluntary muscle contraction of a
muscle group has been demonstrated to increase joint stiff-
ness.
56,57
Cocontraction of antagonistic muscles is believed to
further enhance joint stiffness by increasing the compression
between the articular surfaces.
29,56,57
Second, intrinsically stiffer muscles enhance the potential
capacities of the extrinsic component. Stiffer muscles as a re-
sult of increased activation are also believed to transmit loads
to muscle spindles more readily, thereby reducing some of the
lag time associated with initiation of reflexive activity.
58,59
Some of the physical events contributing to electromechanical
delay, such as the time interval between muscle activation and
onset of segmental acceleration,
60
are reduced in muscles with
higher activation levels. Thus, not only is the initial resistance
to joint displacement superior through heightened intrinsic
stiffness, but the ability to recruit an improved reflexive re-
sponse is also enhanced.
Higher motor control centers have been credited with com-
pensating for static stabilizer deficiency losses through altered
movement and muscle activation patterns.
61–63
Similar to the
spinal reflexes discussed, both direct and indirect evidence
suggests that joint and ligmentous mechanoreceptors are im-
portant for supraspinal sensorimotor control over dynamic
joint stability. In humans, the difficulty surrounding this aspect
of the sensorimotor system arises from the inability to easily
induce isolated experimental manipulations to one or more tar-
get structures without eliciting numerous confounding factors.
Thus, researchers most often attempt to retrospectively mea-
sure patients with different conditions and speculate concern-
ing whether elicited changes or adaptations result from damage
to static stabilizers, neural elements, or both. Direct evidence
supporting the role of articular receptors in sensorimotor con-
trol of dynamic joint stability can only be obtained from ani-
mal studies after experimentally induced deafferentation. An
exorbitant amount of retrospective human research has docu-
mented alterations in movement and muscle activation patterns
in mechanically and functionally unstable joints, so we will
only review several of the common themes supporting the role
of articular receptors to higher motor control centers.
With knee injuries, for example, persons sustaining an ACL
rupture develop an adaptive motor pattern that involves in-
creased hamstrings activation before joint loading
64–67
and
maintaining the knee in a more flexed position during the ac-
ceptance of the load.
61,68,69
Both of these alterations are be-
lieved to prevent anterior tibial translation in the absence of
the ACL. The increase in hamstrings activity occurs before
joint loading in a feedforward control manner. This suggests
that the motor program for the activity was changed and in-
directly supports the idea of motor control change above a
reflexive level.
The alterations in muscle activation sequences appear to oc-
cur not only at the involved joint but also at distal and prox-
imal joints, further supporting the idea of higher motor chang-
es. With respect to alterations in proximal joint positioning and
activation, evidence has been found in subjects sustaining
ACL rupture
61
and ankle injury.
38,70
Increased activation of
musculature acting on the ankle and lower leg (anterior tibialis
and soleus) has been demonstrated in ACL-deficient sub-
jects.
65
After ankle injury, several investigators
71–73
have re-
ported use of postural control strategies that rely more heavily
on proximal joint (hip) muscle activation. Collectively, all of
these investigations support the premise of higher center motor
control changes after orthopaedic injury. Again, the stimulus
for these changes remains debatable: afferent changes from the
articular receptors, loss of mechanical stability, or both.
Freeman and Wyke
74
pioneered direct evidence supporting
the importance of articular receptors in sensorimotor control
over joint stability by surgically resecting the posterior or me-
dial articular nerves of cats. Since both of these nerves convey
afferent information predominantly from the knee joint, the
surgical procedure caused the deafferentation of the joint with-
out disrupting mechanical stability. After the surgery, in ad-
dition to spinal-level motor alterations, the animals displayed
changes in supraspinal motor programs controlling voluntary
movements. Further, postural control adjustments that were
initiated from visual and vestibular sources were also altered.
The authors hypothesized that the alterations developed sec-
ondary to the loss of local input concerning stresses on the
knee joint capsule. When accompanied by mechanical stability
disruptions, the adaptations in movement programs developed
after injury may help prevent damage to secondary restraints
and arthropathy.
28
O’Connor et al,
75
using dogs, reported that
although joint deafferentation alone was not enough to induce
joint degeneration, when combined with ACL transection, se-
vere degenerative changes became more quickly evident than
after ligament transection alone.
Thus, it appears that proprioception is fundamental for sen-
sorimotor control over joint stability, with articular receptors
providing unique, subtle roles. With respect to stiffness, mus-
cle spindles with higher g-MN drive enhance both the feed-
forward and feedback controls of the dynamic restraint mech-
anism through direct regulation of muscle activation levels.
Since g-MN activation is largely influenced by peripheral af-
ferent input, the adequacy and accuracy of the input become
important considerations. Given the sensitivity of joint and lig-
ament receptors through ranges of joint motion and their po-
tent influences on g-MN activity, it becomes quite likely that
this indirect mechanism may outweigh the importance of the
controversial direct a-MN reflexes. At higher motor levels,
joint receptors may play essential roles in the development of

Journal of Athletic Training 83
motor program adaptations to compensate for losses in me-
chanical stability. Figure 4 in Part I summarizes the role of
articular receptors in sensorimotor control of functional sta-
bility. Further research is needed in all of these areas to fully
elucidate the precise mechanisms by which joint receptors con-
tribute.
CONCLUSIONS
Proprioception is conveyed to all levels of the central ner-
vous system, where it provides a unique sensory component
to optimize motor control. Additionally, proprioceptive infor-
mation is necessary for neuromuscular control of the dynamic
restraints. Joint receptors, which are often damaged to some
degree during articular injury, appear to be an important com-
ponent to proprioception. While their role in eliciting direct
muscular reflexes remains controversial, their role in influenc-
ing the g MNs and supraspinal motor programs appears to be
more substantial. Further research concerning the role of ar-
ticular mechanoreceptors in promoting g-MN activation and
supraspinal motor control is needed. Supraspinal control over
the dynamic restaints may be the area that has the most rele-
vance to the development of preventive and rehabilitative
strategies. Intervening at supraspinal levels may provide the
key to promoting increased dynamic stability from a prepa-
ratory perspective, rather than the debatable reactive perspec-
tive.
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