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Update on proprioception: considerations for dance education

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 Original Article

Update on Proprioception
Considerations for Dance Education
Glenna Batson, P.T., D.Sc., M.A.

Abstract the Latin “proprius,” meaning “one’s and agility exercises) for prevention
Proprioception is a topic of interest within own,” for sensory information derived and rehabilitation of lower extrem-
the larger scope of dance pedagogy, sci- from neural receptors embedded in ity injuries.3,7 Once characterized by
ence, and rehabilitation. As the science joints, muscles, and tendons.1 These simple exercises of position sense (e.g.,
of proprioception changes, approaches to specialized sensory (“afferent”) nerve timed standing on one leg with eyes
proprioceptive training also change. Thus, endings are stimulated by body mo- closed), proprioceptive exercises now
proprioceptive training in dance medicine tion and position, providing the body are embedded in expanded balance
has expanded to include balance protocols. with an awareness of itself and of its protocols.8-10 A key principle in balance
A key concept within these protocols for
location in space. Today, considerable testing and training is perturbation,
treatment of lower extremity injuries is
perturbation. Perturbation training is discrepancies persist as to the exact in which graded, controlled forces are
designed to evoke focal neuromuscular usage and meaning of proprioception applied across injured joints to selec-
control at injured joint sites, as well as more and its kindred term kinesthesia. 2 tively “destabilize” them while avoid-
global postural responses for overall balance As a sensory system, proprioception ing further risk of injury.9,11 Careful,
and coordination. This article provides an includes conscious and non-conscious selective destabilization is designed to
update on the science of proprioception inter- and extra-personal sensations of evoke timely, reflexive neuromuscular
within the framework of postural control static position and movement within responses.9 Additionally, destabilization
and balance. Specific practices from reha- the context of a specific environment strategies activate higher neural cen-
bilitation that integrate balance exercises and task.3,4 Static position sense in- ters so that postural synergies are also
into proprioceptive training are considered. corporates body orientation and body evoked. In these synergies, large groups
Further research is needed to test the ef-
part relationships, while movement of muscles respond quickly throughout
ficacy and utility of these exercises within
the context of the dance studio. sense incorporates neuromuscular the whole body to maintain balance
and mechanical feedback about the (center of mass over the base of sup-
rate, amplitude, direction, and force port).12 Perturbation challenges have

P
roprioception is the sense of of movement.3 Proprioception also been shown in rehabilitation to im-
body motion—the ability to contributes to complex neuromuscular prove balance after lower extremity
feel the body moving in space. processes that underlie postural control injury, implying that improvements
Despite centuries of scientific interest, and balance, allowing the body to in proprioception may be an indirect
the role of proprioception in the orga- remain oriented and stable in all activi- benefit.13 What follows is a review of
nization and execution of movement ties, static and dynamic.5,6 the current science of proprioception,
remains conjectural. In 1906, neuro- Proprioception “drills” are part of presented with a view to considering
physiologist Sir Charles Sherrington comprehensive neuromuscular training the potential merits of proprioceptive
coined the term proprioception from (along with flexibility, strengthening, exercises in dance training.
Although beyond the scope of
this review, readers might consider
Glenna Batson, P.T., D.Sc., M.A., is an Associate Professor in the Program in proprioception not only through the
Physical Therapy, Winston-Salem State University, Winston-Salem, North Carolina. lens of science, but also through phe-
Correspondence: Glenna Batson, P.T., D.Sc., M.A., Winston-Salem State University, nomenology and somatic education,
601 Martin Luther King Jr. Drive, Winston-Salem, North Carolina 27110; especially in view of the evolving sci-
[email protected]. ence of embodiment.14 Because body

35
36 Volume 13, Number 2, 2009 • Journal of Dance Medicine & Science

perception and attunement function as nerve endings).23 Proprioceptive nerve loading to the spinal cord through re-
both process and product in dance, the endings are activated when tissue de- flex arcs that trigger rapid response of
phenomenological perspective of the forms by way of static positioning or the muscles to contract for timely neu-
“lived body” helps avoid reductionist movement, either actual (physically romuscular coordination.26,27 At higher
thinking in which proprioception is executed or passively manipulated) or levels of integration (e.g., brainstem)
viewed only as a neurophysiological imagined. Stimulus modalities include afferent neurons synapse with visual
construct.15 Montero argues that we pressure, stretch or rate of change of and vestibular input throughout the
don’t have proprioception, we “pro- muscle length, muscular tension and neuraxis to facilitate automatic postural
prioceive.”16 Reynolds expands on relaxation, as well as vibration and control and locomotion. Continual
the role of kinesthesia, stating that other less clearly defined sources.23,24 processing of sensory input at the non-
dancers refine kinesthetic sensation to Transduction of neural signals provides conscious level between neurons in the
convey the subtle nuances of move- a sense of localized position as well as spinal cord, cerebellum, and brainstem
ment texture, as well as to transcend movement, signaling the amount and underscores the more automatic as-
the conventions of bodily habit.17 Our velocity of joint loading and the degree pects of balance in both pedestrian and
familiar and confident selves are bound of muscle length and force. Theoreti- skilled movement.6,20,21 Integration of
up with habitual, normative effort.17 cally, stimulating joint mechanorecep- sensory input in the somato-sensory
Embedded within the proprioceptive tors increases gamma motor activity, cortex (S1, S2, S3, and association
sense are sensations of muscle tonus resulting in an increase in the sensitivity areas) aids in elaboration of the body
and perceptions of heaviness and effort of muscle spindles in those muscles image and body schema.6,28 Flexible
(or effortlessness).18,19 Proprioception surrounding the joint.24 Increased and adaptive body “maps” within the
not only helps us know where we are, spindle sensitivity fosters a higher state motor program offer a conscious and
but also defines perceived effort within of “readiness” of the muscle to respond non-conscious sense of body owner-
environmental and task contexts.3 The to perturbing forces.24 ship (of body parts and their locations)
“task” of dancing involves kinesthetic Although it is not practical to con- and agency (control of body action).28
exploration of various movement ef- sider each individual receptor’s isolated With the developments in technol-
forts in which the boundaries of self-to- contribution to motor programming, ogy and sensory neurophysiology in the
self and self-to-audience are stretched, Table 1 illustrates the classical schema late 1980s and 1990s the focus of re-
and the normative, habitual ways of of neurons. The Roman numerals refer search has shifted from the relative con-
deliberately using energy are altered.16 to the afferent nerves’ diameters, the tribution of any one receptor to a more
size of which influences conduction ve- dynamical systems-based approach.29,30
Neurophysiology: A Brief locity, the level of threshold firing, and Scientists have replaced a strict division
Glimpse the adaptive properties (how quickly or between afferent (incoming) and effer-
Proprioceptive input derives from a slowly the nerves respond to deforma- ent (outgoing) neural processing with
number of peripheral sensory end tion resulting in reflex neuromuscular an integrated, multimodal perspective
organs embedded in muscles, tendons, responses). Nerve detection thresholds, in which perception and action are
and articular joint complexes, includ- for example, usually are lowered (more intimately coupled and inseparable.29-31
ing ligaments, fascia, and skin.20,21 The rapidly responsive) in conditioned Explanations of physiological function
term “somatosensory” better captures muscles2 and raised (slower to respond) of sensory phenomena alone do not
the scope of these combined stimuli in fatigued muscles.25 sufficiently explain how these receptor
(musculotendinous, joint, and cuta- Proprioceptive or “kinesthetic” properties lead to improved behavior or
neous) coming from the body itself awareness results from complex media- function, making it difficult for danc-
and its responses to the environment.4 tion of input distributed throughout ers to glean practical information from
Somatosensory input combines with all levels of the central nervous system the receptor level to use for training.
visual and vestibular information to (reflex, brainstem, and higher subcorti- Instead, proprioception can be viewed
support balance, accounting for 70% cal and cortical levels).23,26 Peripheral within the larger context of interacting
of postural control in quiet upright input from these sensory nerve endings constraints on postural control and
standing.22 Receptors from muscles, enters into the spinal cord, mediating balance.29 Maintaining balance within
tendons, and joints proper are called reflex spinal control at various spinal an ever-changing environment requires
“mechanoreceptors.” Mechanorecep- segments. As input ascends to supraspi- rapid postural responses to perturba-
tors fire in response to mechanical nal levels, synapses occur throughout tions, both internal (self-induced) and
stimuli coming from static position the neuraxis, including the cerebellum, external (gravitational, inertial, and so
(body orientation) or movement brainstem, subcortical (e.g., basal gan- forth). Examples of internal perturba-
(force, speed, amplitude, and direc- glia and thalamus), and cortical (e.g., tions include purposely lifting your
tion). Traditionally, these receptors are sensorimotor and association) areas, arms in a port de bras or automatically
classified as muscle spindles (Ia and II to mediate more complex levels of reaching for a drink while engaged
fibers), Golgi tendon organs (GTOs) motor control.21 At the reflex level, for in reading. External perturbations
and joint afferents (GTOs, Ruffini example, knee sensory receptors convey typically involve slipping or tripping.32
endings, Pacinian corpuscles, and free non-conscious information about joint These responses are both anticipatory
 Journal of Dance Medicine & Science • Volume 13, Number 2, 2009 37

Table 1 Sensory Receptors for Proprioception

Firing
Threshold & Adaptive
Deformation Properties &
Receptor Axon Size Class Shape Location Source Effect
Musculotendinous
Muscle Spindles Large Ia Fusiform “Bag” Scattered Low, quick Velocity-sensitive
Intrafusal Fibers myelinated* distribution, stretch and rapid changes in
3-10 fibers in maintained muscle length†
parallel with 1 (tonic) stretch
extrafusal muscle
fiber‡
Medium II Fusiform In parallel with Higher than Ia Slow-adapting,
myelinated “Chain” extrafusal muscle Tonic stretch static or sustained
fibers‡ muscle lengths
Golgi tendon Large myelinated Ib Capsular In series with 1 Low, < 1gm Accurate sampling
organs (GTOs) GTO per 10-20 tendon of active muscle
collagen fibers of tension, active tension and
tendon contraction velocity of change
mainly of tension, less
responsive to passive
stretch
Joint Afferents
GTOs Ib Joint ligaments Low, Similar Slow-adapting
to GTOs in
tendons, signal
tension changes
Pacinian Corpuscle Medium II Onion-shaped, Deep layer joint Very low, Rapidly-adapting,
myelinated concentric layers capusules movement, not high sensitivity to
constant joint vibration & tissue
position displacement
Ruffini Endings Medium III Spindle-shaped Deep layers Higher than I, Slow-adapting§
myelinated capsular in skin, joint extremes of joint
capsules, range, passive
ligaments, more than active
tendons
Free Nerve Endings Small, IV Branching, non- Superficial layers Variable, Tissue damage,
myelinated (Adelta capsular of skin, joint highly context- coarse touch, pain||
& C) capsule dependent
*Neural diameter (large, small) and myelination is significant in conduction velocity. The larger, myelinated fibers conduct faster. †Intrafusal fibers
do not add appreciably to the force of muscle contraction, but change in their tension level via the gamma motor system and impact significantly
on their sensitivity to muscle length changes.23 ‡The ratio of muscle spindles to muscle fibers varies with the type of muscle. Larger muscles that
generate coarser movements (e.g., superficial back muscles) have fewer spindles compared with extraocular muscles or intrinsics of the hand that
require greater sensitivity and accuracy for precise movements of the hand and for manipulation, respectively.23 §While not much is understood
about joint afferents (which also occur in skin), Pacinian and Ruffini afferents presumably respond to tracking of motion and position (of fingers),
while Merkel cell afferents and Meissner corpuscles (which appear only in skin) are more responsive to shape and pattern detail, as evidenced in
research on Braille readers’ finger afferents, providing “stereognosis.” ||Note that with any abnormal (repetitive, continuous, overly-forceful) input,
any receptor can become a “nociceptor” and signal pain.

and reactive, and occur much faster execution (feedforward) as well as to how to self-correct seamlessly for errors
than the fastest voluntary movements.33 correct for velocity and timing errors in space, time, or effort as they move,
A neuromotor state of “readiness” acts (feedback). A simple example is that but also how to anticipate effort values
to prime postural response synergies as you descend a staircase your foot in advance of the onset and execution
both in anticipation and in response “knows” there is a step below it, how of movement. Training these rapidly
to modifications in the motor pro- far it is located below the descending adaptive postural responses requires a
gram or the environment.33 Integrated body, and how much control is needed specialized approach in which perturba-
proprioceptive input at all levels of the to descend without losing your balance, tion plays a key role (discussed below).
nervous system functions to organize even with eyes closed. This information Proprioceptive responsiveness is
body stability ahead of movement is vital to dancers who learn not only readily altered, adapting to a number
38 Volume 13, Number 2, 2009 • Journal of Dance Medicine & Science

of factors including postural habit, over other populations or under all

Further, because of its intimate re-
conditioning, and movement training. conditions. Researchers suggest that: 1. lationship to balance, proprioception
Factors leading to diminished (hypo- ballet training alone without concur- underscores our sense of safety and
tonic) or inappropriately exaggerated rent additional coordination training confidence in daily navigation. Thus,
(hypertonic) proprioceptive responses does not lead to improvements in ankle the psycho-physical impact of small
include: 1. prolonged periods where joint position sense or positive post- proprioceptive deficits is important to
muscles are held in shortened (i.e., rehabilitation measures of balance49; 2. consider after injury. Although surgi-
unloaded or un-stretched positions) trained dancers exhibit perceptual and cal and rehabilitation outcomes may
or in overly stretched lengths, as is balance errors in posturography testing have been successfully met after lower
commonly seen in habitual postural with EMG50; 3. dancers perform less extremity injury, if proprioception is
malalignment34; 2. prolonged or repeti- well on balance outcome measures insufficiently restored, or if the athlete
tive maximum voluntary contractions compared to judo practitioners 51; feels insecure and unstable on the joint,
without sufficient rest between repeti- and 4. professional dancers perform full performance is compromised, and
tions25; 3. musculoskeletal injury and less well on platform posturography there is a higher risk of reinjury.3,59
surgical interventions, especially with testing during eyes-closed conditions Severely impaired or absent proprio-
inadequate or incomplete rehabilita- that demand increased propriocep- ception negatively affects not only the
tion19; and 4. joint degeneration or tive strategies for balance as the base quality of the individual’s motor con-
other neuromuscular disease.35 The of support is narrowed and vision trol, but also the way that individual
sensitivity of proprioceptors also is is occluded.52 While proprioceptive perceives and interprets the behavior of
altered throughout the lifespan by training is routine in dance rehabilita- others.61 Deafferentation studies have
a variety of other factors, including tion, few reports exist on the effects shown that people who lose the ability
gender,36 development,37 menstrua- of targeted proprioception exercises to feel their bodies accurately through
tion and other hormonal fluctuations on dance technique, except perhaps illness must rely largely on vision and
during key growth periods,38 nutrition with children.53 Even a simple exercise cognition to carry out the simplest
and weight loss or gain,39 vitamin B6 such as balancing in passé relevé with movements.62
toxicity and exposure to industrial pol- eyes closed is rarely performed in adult Proprioceptive training is believed
lutants,40 steroid use and bodybuild- dance training. to be beneficial in preventing lower
ing,41 declines associated with aging extremity injuries, as well as reducing
or prolonged immobility at any age,35 Injury recovery time and adding protection
emotional stress,42 and even shifting For a dancer, a simple ankle sprain is against re-injury.7,59,63 Known benefits
attentional states.43 a whole body injury. A proprioceptive of proprioceptive training after knee
deficit, however minimal, compromis- and ankle injury in athletes include
Proprioception: A Dancer’s es finely tuned postural control, jeop- improved postural stability (balance),56
Advantage? ardizing balance and increasing injury flexibility,64 joint position sense, sta-
A healthy, responsive proprioceptive risk.54-56 Undetected proprioceptive bilization, and faster muscle reaction
system appears integral to the way deficits can predispose the dancer to time,60 and ultimately a decreased
dancers monitor themselves, learn, injury, delay rehabilitation, or pose the incidence of re-injury. Whether pro-
and self-correct, implying a potential risk of re-injury.3,19 Results from testing prioception itself actually improves
advantage in motor planning, motor proprioception in athletes with recur- with training is controversial.13 Adap-
control, and postural stability.44 Pre- rent ankle sprains, for example, show tations occurring during rehabilitation
sumably, professional dance training them to have less ankle joint position through perturbation training are
strengthens the accuracy of proprio- sense than non-injured athletes,57 and thought to be mediated by changes
ceptive inputs and shifts sensorimotor diminished perception of inversion and in feedforward processes, affecting the
dominance from vision to a more eversion movements as compared to speed of anticipatory reactions dur-
internally-based system of reference.45 controls.58 Undetected proprioceptive ing fast movements, with concurrent
This would suggest that dancers de- deficits can lead to both peripheral and proprioceptive feedback being less
velop an augmented inner body sense central alterations in function, such as important.3,13
compared to non-dancers, or that joint laxity and instability, malalign- Proprioception should be an im-
those persons who are what Howard ment, localized weakness, diminished portant part of the dancer’s fitness pro-
Gardner calls “kinesthetic thinkers” muscle reaction time, and altered body file.65 It should be routinely screened
gravitate toward careers in dance.46 schema and central motor program- in dance, with deficits recorded,
Dancers demonstrate increased ac- ming.7,59,60 Poorly rehabilitated injuries proprioceptive training initiated,
curacy of position-matching when may interfere, for example, with the and progress tracked; especially, the
tested against gymnasts and untrained strength of the reflex arc, leading to al- screening should be repeated peri-
controls, both in static47 and dynamic tered joint stability and motor control, odically if there is a history of injury.
testing.48 Results from research on bal- as has been reported in cases of knee Traditional screenings for deficits in
ance, however, indicate that dancers and ankle joint injury, post-surgery, proprioception include tests in which
do not necessarily have an advantage and traumatic osteoarthritis.3,7,19 subjects detect the threshold of pas-
 Journal of Dance Medicine & Science • Volume 13, Number 2, 2009 39

sive joint movement. For static joint and visual surround to quantify lim- Exploiting reflex stimulation to gain
position sense and joint movement, its of stability and discrimination of flexibility, as in PNF contract-relax
the examiner passively moves a digit sensory organization.59 Dance-specific stretching or through self-employed
or limb while the subject, with eyes balance batteries need to be developed manual therapeutic procedures (e.g.,
closed, mimics with the opposite limb and validated that also test dancers in pressing on a tendon to relax a muscle),
or verbally describes the movement traditional foot positions (parallel, first, does not appear to have lasting value
direction. Problems with this type of second, demi-pointe, and pointe). for motor re-programming.68
screen include sensitivity; the dance Comprehensive approaches to bal-
population may be too functionally Rehabilitation ance training can include a combina-
advanced for this simple measure to Once assessed, comprehensive reha- tion of wobble board protocols, Pilates
detect differences.66 Second, although bilitation of lower extremity injuries reformer training, therapeutic ball and
relatively easy to execute, these tests are includes balance training and proprio- disk exercises, plyometric training, or
difficult to interpret if there are subtle ceptive exercises along with strengthen- mini-trampoline exercises. Employ-
deficits that may emerge under more ing, flexibility exercises, and sport- or ing sudden alterations in direction
active conditions of motor execution dance-specific movements.19 Rehabili- and speed of movement, along with
with and without injury.3 For example, tation of proprioception includes a impulsive loading, as in hopping,
the timing and amplitude with which spectrum of interventions that use: 1. jumping, and plyometrics, helps to
the peroneal muscles fire under static modalities, manual therapy, and other achieve these goals. By adding eyes-
conditions does not reflect their re- receptive body therapies and passive closed conditions, variable surfaces
sponsiveness during at-risk conditions maneuvers; 2. bracing and taping; and and multitasking, sensing, perceiv-
for injury (e.g., the landing phase of 3. perturbation training, a progres- ing, and interpreting sensory input
walking, running, or jumping).13 Fi- sion of static and dynamic exercises to is challenged. Single leg stance with
nally, these screens are inadequate as destabilize the injured joint or whole eyes open and eyes closed for specified
training tools or as outcome measures body balance. These exercises include: durations can progress to unilateral
to track progress.59 1. augmenting joint position sense and and bilateral stance on foam, weight
Reliable and valid testing for pro- muscular co-activation for dynamic shifting, stepping, marching, walking,
prioceptive deficits should include joint stabilization (e.g., static uni-legged hopping, leaping, and jumping, all
comprehensive balance testing. 3,59 standing for ankle injuries); 2. activat- with additional interferences such as
Depending on the equipment used, ing postural synergies for reactive neu- talking or counting backwards by 3’s,
balance tests can assess postural sway romuscular control; 3. increasing the catching a ball, or holding a glass of
and limits of stability, sensory organiza- speed, force, and duration of muscle water.69 Repetition and reinforcement
tion, foot contact pressures, and muscle activation around injured joints in non- of goal-directed, dance-specific training
activation patterns. Balance batteries weightbearing and weightbearing; and with real space-time values helps con-
attempt to model real perturbations, 4. challenging balance in dance-specific solidate higher level learning, memory,
such as near or full falling, under activities.19 and recall.19 Protocols also should help
altered sensory and environmental Although protocols reported in dancers exploit multiple joint com-
conditions (e.g., with eyes closed or on the literature vary in terms of exer- binations in closed- and open-chain
an altered surface), as well as examin- cise modes, intensity, frequency and positions to develop flexible and novel
ing joint loading at various phases duration, perturbation exercises in strategies for movement.3,48
(e.g., landing from a jump). Balance altered sensory conditions challenge
drills done on various surfaces with the body’s normal responses to an- Further Considerations for
eyes open and closed help assess the ticipated environmental stimuli.8-10 Research
relative contribution to balance of Graded, potentially destabilizing In addition to what dancers can learn
various neural afferents (visual versus forces (manual, surface perturbations) about proprioception from rehabilita-
vestibular or proprioceptive) and, by are applied to the injured joint dur- tion and conditioning protocols, other
inference, joint stability.59 Tests that ing dynamic activities that challenge aspects of dance training also impact
are simple to administer and require sensory organization of balance.9 Re- proprioceptive responsiveness. The
little equipment include the clinical test training proprioception post-injury use of mirrors in the dance studio, for
of sensory organization and balance, theoretically addresses multiple levels example, has been the recent focus of a
or “Foam and Dome,”5 in which six of central nervous system mediation number of studies.70-72 Critique of their
different test conditions discriminate in motor control: reflex spinal level, use centers mainly around the conflict
somatosensory from visual and ves- brainstem level (equilibrium and right- of visual versus kinesthetic information
tibular deficits.5 Other simple clinical ing responses), and cortical level.3,19 as a source of motor learning. Small
tests include rocker (wobble) board Exploiting reflex levels of receptor sample sizes and other methodological
protocols or the Five-Star Balance sensitivity alone is insufficient for full considerations, as well as contradictory
Test.67 Platform posturography, such motor control, as receptors perform results, beg a number of questions
as the NeuroCom® or Balance Master® differently under active, goal-directed and require dancers to regard the
system, uses a moving force platform (as opposed to passive) conditions.68 conclusions with caution. Nonethe-
40 Volume 13, Number 2, 2009 • Journal of Dance Medicine & Science

less, consensus appears to support the cruciate ligament rehabilitation pro- 22. Kristinsdottir EK, Fransson PA,
notion that mirrors are important in grams for physically active individuals. Magnusson M. Changes in postural
confirming the accuracy of movement Phys Ther. 2000;80:128-40. control in healthy elderly subjects are
in the later stages of motor learning, 9. Risberg MA, Holm I, Myklebust related to vibration sensation, vision
but should be avoided as the sole source G, Engebretsen L. Neuromuscular and vestibular asymmetry. Acta Oto-
training versus strength training laryngol. 2001;121:700-6.
of feedback in earlier stages of learning. during first 6 months after anterior 23. Purves D, et al. Neuroscience (4th ed).
Investigation as to the effect of mirrors cruciate ligament reconstruction: a Sunderland, MA: Sinauer Associates,
on age and stage of learning of the randomized clinical trial. Phys Ther. 2007.
dancer, type and degree of difficulty 2007;87:737-50. 24. Johansson H, Sjolander P. Neuro-
of the material being presented, and 10. Chmielewski TL, Hurd WJ, Rudolph physiology of joints. In: Wright V,
whether cueing is implicit (focusing on KS, et al. Perturbation training im- Radin EL (eds): Mechanics of Human
internal proprioceptive cues to control proves knee kinematics and reduces Joints: Physiology, Pathophysiology, and
movement) or explicit (focusing on the muscle co-contraction after complete Treatment. New York: Marcel Dekker
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In summary, proprioception appears 11. Chmielewski TL, Hurd WJ, Snyder- repetitive contractions and ischemia
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