0% found this document useful (0 votes)
10 views9 pages

Assessing Proprioception in Children A R

Tgf

Uploaded by

nakamal
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
0% found this document useful (0 votes)
10 views9 pages

Assessing Proprioception in Children A R

Tgf

Uploaded by

nakamal
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
You are on page 1/ 9

Journal of Motor Behavior, Vol. 0, No.

0, 2016
Copyright © Taylor & Francis Group, LLC

RESEARCH ARTICLE
Assessing Proprioception in Children: A Review
Virginia Way Tong Chu
Department of Occupational Therapy, Virginia Commonwealth University, Richmond, Virginia.

ABSTRACT. Proprioception is the subconscious and conscious In some literature, the term kinesthesia refers to move-
awareness of the spatial and mechanical status of the musculoskel- ment sense and proprioception refers to static position sense
etal framework. When working with children with motor delays
and sensory integrative dysfunction, occupational therapists rou- (Barrack & Skinner, 1990; Gardner, Martin, & Jessell,
tinely assess the client’s proprioceptive system. However, cur- 2000; van Beers, Sittig, & Denier van der Gon, 1998;
rently available assessments for occupational therapists are Warner, Lephart, & Fu, 1996), but I do not make this dis-
primarily observer-based and concerns have been raised about the tinction. Clinically, it is often difficult to distinguish move-
reliability of observer-based assessments of sensation. The ment sense from static position sense, as information from
author’s purpose was to review measures of proprioception cur-
rently available to occupational therapists and explore direct
joint positions will provide cues about direction and speed
measures of proprioception from neuroscience and rehabilitation of movement. Therefore, I do not make this distinction
that can be adapted for pediatric clinical use. Observer-based and between the two terms.
direct measurements of proprioception assessments complement Proprioception primarily originates from proprioceptors
each other in meeting clinical needs. A better understanding of in the joint receptors, muscle spindles, and Golgi tendon
both types of evaluation will improve proprioceptive evaluation.
organs. Signals from the proprioceptors are then processed
Keywords: proprioception, children’s motor development, at various levels: the spinal cord, the cerebellum, and the
assessments cerebral cortex (Figure 1). The signal that terminates at the
spinal cord forms the protective reflex loops with the Aa
and Ag motor neurons that protect our muscles from being
overstretched and protect our joints from dangerous
D uring the formative years of early development, chil-
dren experience and learn about the world through
their senses. As they sense and feel things around their
stresses. This particular pathway does not result in any sen-
sation of stimulus (e.g., stretch) and therefore is called an
asensory function of the proprioceptive system. Although
environment, they learn to move and navigate the world. In
protective reflexes are not considered a proprioceptive
the Ayer’s sensory integration theory, three senses are pos-
function in the strict sense of the definition, it is important
ited to have a major impact for motor development: tactile,
to note as we consider the assessments of the proprioceptive
vestibular, and proprioceptive (Ayres, 1972; Bundy, Lane,
system later in the discussion.
& Murray, 2002). Difficulties in any of these sensory sys-
The second destination of the proprioceptive signal is
tems may cause difficulty with developing motor skills in
the cerebellum, traveling through the spinocerebellar
children. In this paper, the focus is primarily on the proprio-
tract. These signals are subconscious but greatly impor-
ceptive senses and the importance of assessing propriocep-
tant for posture regulation, balance and fine-tuning of
tion when evaluating children with motor delays. In the
movement for accuracy and fluidity. Finally, there are
present article I also review proprioceptive assessments
connections that terminate at the cerebral cortex, which
available for clinicians who work with children.
primarily travel through the dorsal column medial lem-
niscal system. These are the only proprioceptive affer-
ents that reach the conscious mind and allow cognitive
Proprioception and Related Senses perception of the signals. Although proprioceptive sig-
nals can be brought to conscious awareness, they are
In the literature and in clinical practice, the term proprio- usually processed subconsciously in most day-to-day
ception can have slightly different definitions depending on activities.
the background of the user. Thus, it is important to start Aside from proprioceptors, mechanoreceptors in the
with a clear definition. I take a broad definition: propriocep- skin also provide information about movement. Pressure
tion is the subconscious and conscious awareness of the sensors in the soles of the feet provide information
spatial and mechanical status of the musculoskeletal frame- about the load distribution on the feet and are used to
work (Proske & Gandevia, 2012; Stillman, 2002). This assist with balance and postural control. Similarly, the
awareness includes joint position sense, movement sense, skin is stretched during movement and the mechanore-
force perception, and effort (Bastian, 1887; Proske, ceptors detect the stretch and provide information
Schaible, & Schmidt, 1988; Schmidt & Lee, 2014;
Sherrington, 1906). Stillman included balance within
Correspondence address: Virginia Way Tong Chu, Department
proprioception, but I address balance separately, as it is an of Occupational Therapy, Virginia Commonwealth University,
outcome of functioning proprioceptive and vestibular 730 East Broad Street, P.O. Box 980008, Richmond, VA 23298-
systems to be discussed in more detail later. 0008, USA. e-mail: [email protected]

1
V. W. T. Chu

Cerebral cortex
Thalamus

Dorsal column Cerebellum


medial leminscal
system

Ventral Dorsal
spinocerebellar spinocerebellar
tract tract

Medulla

Tendon
reflex Stretch Muscle spindle
reflex

Golgi
tendon
organ Spinal cord
Muscle
spindle Golgi tendon
Joint
organ
receptor

FIGURE 1. Components of the proprioceptive system. Left: Proprioceptive reflex loops. Afferents from the muscle spindle and
Golgi tendon organ enter the spinal cord through the dorsal roots. The proprioception afferents from the muscle spindles synapse
with Aa motoneurons to the agonist muscle and through an inhibitory interneuron to the Aa motoneuron to the antagonist muscle
(stretch reflex). The proprioceptive afferents from the Golgi tendon organs synapse with Aa motoneuron through an inhibitory
interneuron to the agonist muscle, and through a facilitatory interneuron to the antagonis muscle (tendon reflex). Right: Propriocep-
tive pathways. Three major proprioceptive pathways carry information from the proprioceptive afferents to the cerebral cortex and
the cerebellum: the dorsal column medial leminscal system and the dorsal and ventral spinocerebellar tracts.

regarding joint movement. Localization of touch on the maintain functioning balance without visual information.
body also contributes to the development of body When either of these systems is dysfunctional, balance is hard
awareness. to maintain without visual input.
The vestibular system and the proprioceptive system work Motor commands from the cerebral cortex also provide
closely together in keeping a body in balance. The vestibular information to the proprioceptive system, contributing to
system is important for detecting gravity, orientation and lin- the accuracy of proprioception and the perception of effort.
ear movement, particularly that of the head. The semicircular Corollary discharge is carried through the upper motor neu-
canals in the ears detect rotational movement and the utricle ron from the motor cortex. Information from corollary dis-
and saccule in the ears detect linear movements. Integrating charge provides active motor command signals for the
information about orientation from the vestibular system and proprioceptive system to compare signal from the muscle
joint status from the proprioceptive system, a body is able to and joints during voluntary movement. This contributes to

2 Journal of Motor Behavior


Proprioception and Motor Development

improved accuracy of proprioception during active move- Keessen, Kuus, van Vliet, & Zegeling, 1987; Elliott, Con-
ments (Crapse & Sommer, 2008; Guthrie, Porter, & Sparks, nolly, & Doyle, 1988; Hearn, Crowe, & Keessen, 1989).
1983; Proske, 2005; Wurtz & Sommer, 2004). Children who have difficulty in proprioception may present
with difficulties with motor coordination and planning.
These children may also have poor postural control and bal-
Proprioception and Motor Development
ance due to inefficient ankle strategies and weight-shifting
As the sensory system that informs the motor system of to maintain balance (Blanche, Bodison, Chang, & Reinoso,
where the musculoskeletal system is in space, the proprio- 2012; Weimer, Schatz, Lincoln, Ballantyne, & Trauner,
ceptive system is an essential part of motor coordination 2001). These children are often reported to play too roughly
and planning. The proprioceptive system provides online with peers and often crash into things due to difficulty with
error information for correction of slow movements, allow- force gradation when interacting with objects and people
ing the limbs and the body to make corrections based on (Dunn, 1999; Parham & Ecker, 2007). Studies have shown
feedback of the location and status of the body in space. In that poor proprioception has been linked to difficulties with
ballistic (fast) movements, the movement is over before the handwriting (Falk, Tam, Schwellnus, & Chau, 2010;
proprioceptive feedback can be processed to alter the motor Schneck, 1991), and poor coordination (Fatoye, Palmer,
plan. In these movements, the proprioceptive system is use- Macmillan, Rowe, & van der Linden, 2009; Johnston,
ful in providing information before the movement begins, Short, & Crawford, 1987; Mon-Williams, Wann, & Pascal,
such as knowing where the limb is prior to the movement 1999). These difficulties often make it hard for children to
and its distance from the final state in order to plan for learn new motor skills, leading to motor delays.
appropriate motor commands for reaching the target. The Children with various conditions have also been shown
proprioceptive system provides feedback after the fast to have poor proprioception. Children with cerebral palsy
movement is completed, in order to verify movement accu- (CP), a primarily motor-related disorder, have been shown
racy and allows for correction for future movements. to have poor proprioception (Goble, Hurvitz, & Brown,
An essential component of motor learning is making cor- 2009) and sensory deficits (Cooper, Majnemer, Rosenblatt,
rections for future movements. When children first learn a & Birnbaum, 1995), showing that CP is not always a pure
new motor skill, the performance of the movements motor disorder. Children with developmental coordination
requires a lot of conscious effort, relying on all the informa- disorder (DCD), another disorder generally diagnosed
tion available, including visual, proprioceptive, and tactile based on motor delays, also show poor performance on
information. Information about the limb’s position, speed proprioceptive tests (Coleman, Piek, & Livesey, 2001;
and forces are perceived by the proprioceptive system, and Mon-Williams et al., 1999; Piek & Skinner, 1999;
combined with confirmation from the visual and tactile sys- Schoemaker et al., 2001; Smyth & Mason, 1998). Children
tems for correction to improve the accuracy and quality of with autism spectrum disorder (ASD) have been known to
the movement. As the skill improves, the movements are have motor delays and difficulty with motor coordination
refined and the control process becomes more subcon- (Bhat, Landa, & Galloway, 2011). Studies have shown chil-
scious. At this time, proprioceptive information is used pri- dren with ASD performed poorly in tests that rely on pro-
marily as subconscious feedback signal to confirm correct prioception, such as apraxia, balance and sequential finger
execution of efferent motor commands. opposition (Weimer et al., 2001). The Diagnostic and Sta-
Our understanding about the development of propriocep- tistical Manual of Mental Disorders, 5th edition (DSM-V)
tive ability during early childhood is growing through stud- also cites sensory processing differences as a diagnostic cri-
ies comparing children to adults. Studies have shown that teria of ASD (American Psychiatric Association, 2013).
accuracy in actively matching joint positions that are pas- Children who have hyper joint mobility have also been
sively presented improves from childhood to adolescence shown to have poorer proprioceptive sense possibly due to
(Goble, Lewis, Hurvitz, & Brown, 2005). More fine tuning diminished activation of the muscle spindles or joint recep-
of movements is observed in adolescents, demonstrating tors. The relationship between proprioceptive delays, pedi-
more conscious awareness of proprioception and effort in atric movement disorders and motor delays in children are
the actively matching the limb positions. However, the tightly linked. Proprioception is important in the control of
exact developmental trajectory expected of typically devel- fluidity and accuracy of movements. Studies in adults with
oping children is yet unclear. Most research showed that neuropathy have shown the role of proprioception in fine
proprioceptive ability improves from 5 to 8 years old, with tuning the control of movement. Patients with neuropathy
slowing improvement and stabilization in late childhood affecting lower extremity proprioception showed increased
and adolescence (Bairstow & Laszlo, 1981; Hay & Redon, incidences of falling and decreased dynamic stability (van
1997; Laszlo & Bairstow, 1980; Sigmundsson, Whiting, & Deursen & Simoneau, 1999). Studies examining multijoint
Loftesnes, 2000; von Hofsten & R€ osblad, 1988). However, movements in the upper extremities showed that patients
in other studies near linear increase in proprioceptive accu- who lack proprioceptive input showed spatially inefficient
racy was observed from 4 to 13 years old, and improve- hand movements (Sainburg, Ghilardi, Poizner, & Ghez,
ments continue to be observed up to 24 years old (Crowe, 1995; Sainburg, Poizner, & Ghez, 1993), poor spatial

2016, Vol. 0, No. 0 3


V. W. T. Chu

reference for movements (Bard, Fleury, Teasdale, Paillard, proprioceptive information for motor control in a comprehen-
& Nougier, 1995), and difficulty with timing of movements sive evaluation. Neglecting it would be doing a disservice to
(LaRue et al., 1995). A BBC documentary followed a man the child, and potentially missing critical opportunities to
who had isolated proprioceptive sensory loss and initially deliver interventions to improve the child’s development.
lost his ability to walk and move. Though after extensive This paper will highlight proprioceptive assessments
training, he relearned the ability to walk and control move- available to clinicians. Three of the clinical propriocep-
ments, but his movement patterns lacked fluidity and accu- tive assessments (Sensory Profile, Sensory Processing
racy (Rawlence, 1998). Although most children who have Measure, and Sensory Integration and Praxis Test)
poor proprioception do not have complete proprioceptive described in this paper are commonly taught in current
sensory loss, one can infer the implications of poor proprio- occupational therapy curriculums. These assessments are
ception on a developing motor system. Due to the impor- widely accepted clinically in pediatrics by occupational
tance of proprioception in motor planning and motor therapy practitioners. Subsequent literature search in
coordination, it is important that clinicians assess proprio- other assessments of proprioception is done through
ception when assessing motor skills. MEDLINE database and the American Journal of Occu-
pational Therapy database using combinations of words
related to proprioception assessment, including proprio-
Assessments of Proprioception
ception, assessment, joint position sense, kinesthesia,
Due to the limited availability of standardized and norm-ref- movement sense, and force perception. Research results
erenced assessments of proprioception standardized for use in were reviewed to identify commonly used propriocep-
pediatrics (Blanche et al., 2012), many occupational therapists tive assessments in research and adult rehabilitation
focus on assessing proprioception’s role in regulation and sen- evaluations. Clinical assessment tools (refer to Table 1
sory seeking behavior using parent report questionnaire, over- for summary) are separated from research assessment
looking proprioception’s role in motor development. protocols. Most of the relevant literature reveal research
Assessing how a child responds to proprioceptive signals for assessment protocols that require extensive laboratory
regulation and modulation is important for characterizing a equipment that may not be available to clinicians. This
child’s ability to participate in activities in daily life. But it is discussion includes adaptations to make these assess-
also important to assess the child’s ability to process and utilize ments clinically feasible (refer to Table 2 for summary).

TABLE 1. Comparison of Clinically Available Assessments of Proprioception

Subtests that address Assessment Proprioception


Name proprioception type areas assessed

Sensory Profile (Dunn, 1999) Movement processing Indirect Does not directly
assess an area of
proprioception
Body position processing (Caregiver questionnaire)
Sensory Processing Measure Body awareness Indirect Force perception
(Parham & Ecker, 2007) Balance and motion (Caregiver questionnaire)
Planning and ideas
Comprehensive Observation of All items Indirect Force perception
Proprioception
(Blanche et. al, 2012) (clinician observation)
Sensory Integration and Praxis Kinesthesia Direct Joint position sense,
Test (Ayres, 1989) movement sense
(proprioception-related subtests:
standing and walking balance,
postural praxis, finger
identification, graphesthesia,
localization of tactile stimuli)
Kinaesthetic Sensitivity Test Kinesthetic acuity Direct Joint position sense,
(Laszlo & Bairstow, 1980) movement sense
Kinesthetic perception and
memory
Tendon tap Direct - reflex Proprioceptive reflex
Perturbations of actively held Direct - reflex Proprioceptive reflex
positions
a
Based on the areas of proprioception identified in the definition: joint position sense, movement sense, force perception, and effort.

4 Journal of Motor Behavior


Proprioception and Motor Development

TABLE 2. Direct Measurements of Proprioception and Suggested Clinical Procedure

Proprioception area Test type Procedure Outcome Motor ability

Joint position sense Verbal identification Passive positioning the joint Accuracy of Not required
where the participant verbally identification
identifies the movement
without vision of limb
Unilateral limb matching Passive positioning of the joint Accuracy of Movement
which is subsequently moved replacement of limb required
where the participant has to
move the limb back to the
original position
Contralateral limb matching Passive positioning the joint Accuracy of matching Movement
where the participant match required
with the contralateral limb
without vision of limb
Location identification Passive positioning of the joint Accuracy of location Movement
where the participant locates a required
distal segment (e.g. thumb)
with contralateral hand
without vision of limb
Isometric contraction Participant actively holds a Stability of held limb Ability to hold
position of the limb without limb against
vision of the limb. gravity
Movement sense Contralateral limb matching Passive movement of the limb Accuracy of matching Movement
where the participant match required
with contralateral limb
without vision of the limb
Force perception Weight identification Place weights on each hand and Accuracy of Not required
participant identifies which identification
hand has the heavier weight
Other proprioception- Dynamic balance Participant balance on uneven Amount of sway, time Movement
related function surface to examine ankle in balance required
correction strategies
Tendon tap (proprioceptive Striking tendon briskly with a Brisk muscle Not required
reflex) reflex hammer to test the contraction
intactness of the stretch reflex
loop
Perturbation of actively held Participant actively holds a Accuracy and time to Movement
joint (proprioceptive position of the limb and the return to held required
reflex) limb is suddenly perturbed position

The assessments presented here are divided into three examines a child’s sensory processing patterns. Two of its
categories: (a) indirect assessment of proprioception, (b) sections focus on movement processing and body position
direct assessment of proprioceptive function, and (c) processing related to how proprioceptive processing affects
assessment of proprioceptive reflex. participation in daily activities. There are eight items in
each section examining how much the child pursues move-
ment, ability to navigate the environment, and postural con-
Indirect Assessments of Proprioception
trol. The Sensory Processing Measureis a similar parents’
Clinically, proprioception is usually assessed indirectly questionnaire that focuses on sensory processing and
through parents’ report or clinician observation checklist. praxis. The Sensory Processing Measure has three sections
Currently available to occupational therapists and other that focus on proprioception and related functions: body
pediatric clinicians are three tests that examine propriocep- awareness, balance and motion, and planning and ideas.
tion: Sensory Profile (Dunn, 1999), Sensory Processing These sections focus on ability to grade and control forces
Measure (Parham & Ecker, 2007), and Comprehensive and body movements, to navigate the environment, and to
Observation of Proprioception (Blanche et al., 2012). The plan and execute movements. The Comprehensive Obser-
Sensory Profile is a parent report questionnaire that vation of Proprioception is a clinician observation scale,

2016, Vol. 0, No. 0 5


V. W. T. Chu

focusing solely on behaviors and movement patterns that provides the most accurate information about each proprio-
are relevant to proprioceptive processing. The observational ceptive sense. Unfortunately, most direct assessments of
items are drawn from the literature relating to propriocep- proprioceptive are research protocols and require laboratory
tive dysfunction. These indirect assessments provide clini- equipment. Clinical adaptations of these tests can be made
cians with information about the child’s behavioral patterns to provide crude but direct measurements of proprioception.
relating to proprioceptive functioning with short testing Joint position sense can be assessed by moving a limb
time. They are commonly used screening tools to identify and asking the child to identify where the limb has been
children that require further proprioceptive testing. moved without vision of the moved limb. The position
identification can be done through verbal description
(Fugl-Meyer, Jaasko, Leyman, Olsson, & Steglind, 1975),
Direct Assessments of Proprioceptive Function
contralateral limb matching (Goble, 2010), or pointing to
The Sensory Integration and Praxis Test (Ayres, 1989) is the location (Dover & Powers, 2003; Gilman, 2002). The
one standard clinical test available for directly testing vari- most accurate way of testing position sense requires elabo-
ous sensory functions in children, including subtests related rate laboratory equipment in order to move the limb without
to proprioception. The kinesthesia subtest assesses the providing additional tactile information, such as using air
child’s ability to return to the finger to a specific test loca- splints (Hurkmans et al., 2007; Pickard, Sullivan, Allison,
tion without vision. This subtest most directly measures & Singer, 2003). Without the elaborate laboratory equip-
proprioceptive function, namely position sense and move- ment, joint position sense can still be tested by moving the
ment sense. Five other subtests in the Sensory Integration limb manually. Care must be taken to hold the limb at a
and Praxis Test also provide some information about pro- location that minimizes tactile information provided, such
prioceptive performance. The standing and walking balance as grip forces applied orthogonal to the direction of move-
subtest assesses the child’s static and dynamic balance with ment. The position sensation subtest of the Fugl-Meyer test
eyes open and eyes closed, assessing vestibular and propri- has standardized tests of joint position sense by moving the
oceptive function. The postural praxis subtest examines a joint segment up or down (Fugl-Meyer et al., 1975). An
child’s ability to imitate postures, assessing the child’s abil- alternative to test joint position sense is to place the child’s
ity to use proprioceptive information for motor planning. hand in space and ask the child to use the other hand to find
The finger identification, graphesthesia, and localization of the thumb without vision of the hand. Another way to test
tactile stimuli subtests assess the child’s ability to integrate joint position sense is to test a child’s ability to hold the
tactile and proprioceptive information related to body limb in isometric contraction without vision. Large devia-
awareness. The Sensory Integration and Praxis Test is lim- tions from the held position can indicate poor propriocep-
ited in its use for proprioceptive testing due to only having tion or poor motor control. The child can also be asked to
one form of pure proprioceptive assessment, and requiring match the held limb position with the contralateral limb or
special certification to administer the test. Furthermore, the replace a limb to the held position after it has been moved.
test is only standardized for children between 4 years old Movement sense is usually tested with similar laboratory
and 8 years, 11 months old. equipment as the joint position sense. Researchers have
Although less commonly used in recent years, the Kines- tested movement sensitivity by establishing the joint dis-
thetic Sensitivity Test is another standardized test used to placement detection threshold, as the joint is gradually and
measure movement sense acuity and movement perception subtly moved by the equipment until the person is able to
and memory (Laszlo & Bairstow, 1980). In the kinesthetic identify the direction of movement (De Santis et al., 2014;
acuity subtest, the participants’ hands moved up and down Hall & McCloskey, 1983; McCloskey, 1978; Pai, Rymer,
two ramps with different slope without vision of their hand Chang, & Sharma, 1997). Without elaborate equipment in
and the ramp, and they are asked to identify which ramp is the clinic, movement sense can be tested by moving the
steeper. The kinesthetic perception and memory require the limb manually and asking the direction of movement or
participants to remember the path their hand traced on a assessing the contralateral limb’s ability to match the move-
stencil using a stylus without vision of the hand and stencil. ment without vision.
The stencil is rotated prior to being unmasked and the par- Force sense, also called load perception, can be assessed
ticipant is asked to re-orient the stencil to the original posi- by measuring a person’s ability to replicate forces (Chu,
tion. The test has normalized data for children from 5 years Hornby, & Schmit, 2015; Dover & Powers, 2003; Lafargue,
old to adult (Laszlo & Bairstow, 1985). This test examines Paillard, Lamarre, & Sirigu, 2003; Murtaugh & Costigan,
both joint position sense and movement sense, but has lim- 2003). In these tests, participants are asked to replicate forces
ited use due to the equipment needed to perform the assess- in the contralateral limb or a previously produced force that
ment and the test is no longer commercially available. was matched to a target force. Although load perception has
In the following discussion I highlight other methods that been reported to have no correlation with position sense
assess each proprioceptive sense and related motor func- (Stillman, 2002), it is important to be considered in motor
tion: position sense, movement sense, force sense, and bal- control as accurate movements to interact in the world relies
ance. Direct assessment of proprioceptive function on the ability to accurately sense and produce forces.

6 Journal of Motor Behavior


Proprioception and Motor Development

Without the use of elaborate equipment, one can assess force Bachmeier, & Coelho, 2001; Riemann & Lephart, 2002).
sense with children by putting a weight in each of the child’s These tests can be adapted for simpler clinical use, where
hand and asking the child which one weighed more. participants hold the tested limb in a predetermined position,
Balance is assessed in several clinical tests: Romberg’s and clinicians can observe reactions to manual perturbations.
test, Fugl-Meyer test, and neurological exams (Fugl-Meyer Normal proprioceptive response would be to correct for the
et al., 1975; Khasnis & Gokula, 2003). In standing balance perturbation and return the limb to the pre-perturbed position
with and without vision, the primary system involved in quickly. If a child is unable to return the limb to the preper-
keeping balance is the vestibular system. The propriocep- turbed position and no motor disorder is noted, it is likely
tive system takes more of a role in dynamic balance, such due to problems with the proprioceptive system.
as balance on uneven surface that requires ankle move-
ments to make subtle corrections. The amount of sway and
the amount of time maintaining balance in various condi- Conclusion
tions (stable surface, uneven surface, one-legged stance)
In the present article I give an overview of the proprio-
will provide insight about the child’s proprioceptive and
ceptive system and highlights the importance of proprio-
vestibular capabilities.
ception in motor development in children. As clinicians
assess motor performance in children, it is important to also
Assessments of Proprioceptive Reflex include a comprehensive assessment of proprioception.
Assessments of proprioception currently used by clinicians
Assessing proprioceptive reflexes is one way to confirm
are mostly indirect assessments that provide a method for
intact proprioceptive afferents. As discussed previously,
screening, where clinicians follow-up by clinical observa-
proprioceptive reflexes do not contribute to the sensory
tion. Direct proprioceptive assessments that allow for more
function of the proprioceptive system. However, they allow
accurate evaluation remained primarily research based.
for a unique opportunity to isolate and test the functioning
Methods to adapt some of these proprioceptive assessments
of the proprioceptors prior to the signals reaching the motor
to make them appropriate for clinical use have been sug-
cortex for proprioceptive processing. Proprioceptive
gested. Development and standardization of more clinical
reflexes can be assessed in two ways: passive tendon tap
tools to directly assess proprioceptive function is needed.
(Beard, Kyberd, Fergusson, & Dodd, 1993; Eklund, 1972;
Priebe, Sherwood, Thornby, Kharas, & Markowski, 1996)
and perturbations of actively held joint positions (Colebatch ORCID
& McCloskey, 1987; Evarts & Granit, 1976; Fitzpatrick,
Virginia Way Tong Chu http://orcid.org/0000-0001-
Taylor, & McCloskey, 1992; Uwe Proske, 2005). It should
9420-2284
be noted that abnormal results from reflex tests cannot be
used to confirm dysfunction at the proprioceptor level, as
the abnormal motor response can be a consequence of pro-
prioceptive, neurological, or motoric mechanisms. A nor-
REFERENCES
mal proprioceptive reflex result can on the other hand be
used to rule out dysfunction of the proprioceptors. American Psychiatric Association. (2013). Diagnostic and statistical
Tendon taps (stretch reflex) are routinely used in neuro- manual of mental disorders (5th ed.). Washington, DC: Author.
Ayres, A. J. (1972). Sensory integration and learning disorders.
logical exams to assess functions of the CNS. The proce- Los Angeles, CA: Western Psychological Services.
dure involves identifying the tendon of the muscle to be Ayres, A. J. (1989). Sensory Integration and Praxis Test: SIPT
tested, and striking the tendon briskly with a reflex hammer manual. Los Angeles, CA: Western Psychological Services.
while the limb is at rest. The subsequent muscle contraction Bairstow, P. J., & Laszlo, J. I. (1981). Kinaesthetic sensitivity to
and limb movement is observed. This test is commonly per- passive movements and its relationship to motor development
and motor control. Developmental Medicine and Child Neurol-
formed at the biceps tendon, brachioradialis tendon, triceps ogy, 23, 606–616.
tendon, patellar tendon and Achilles tendon. A brisk Bard, C., Fleury, M., Teasdale, N., Paillard, J., & Nougier, V.
response from the muscle contraction in response to the (1995). Contribution of proprioception for calibrating and
muscle stretch resulting from the tendon tap is considered a updating the motor space. Canadian Journal of Physiology and
normal response. No response could indicate a problem Pharmacology, 73, 246–254. http://doi.org/10.1139/y95-035
Barrack, R. L., & Skinner, H. B. (1990). The sensory function of
with the proprioceptors or neurological dysfunction in the knee ligaments. In D. M. Daniel, W. H. Akeson, & J. J.
reflex loop. Hyperactive stretch reflexes often occur as a O’Connor (Eds.), Knee Ligaments: Structure, function, injury
result to injury to the nervous system. and repair (pp. 95–114). New York, NY: Raven Press.
Proprioceptive reflexes can also be tested with perturba- Bastian, H. C. (1887). The “muscular sense”: its nature and cortical
tions of actively held joint position. These protocols typically localisation. Brain, 10, 1–89. http://doi.org/10.1093/brain/10.1.1
Beard, D. J., Kyberd, P. J., Fergusson, C. M., & Dodd, C. A. (1993).
require sophisticated instruments to elicit the perturbations Proprioception after rupture of the anterior cruciate ligament. An
and to measure the small correctional movements from the objective indication of the need for surgery? The Journal of Bone
sudden perturbation (Brunt et al., 1992; Pincivero, and Joint Surgery. British Volume, 75, 311–315.

2016, Vol. 0, No. 0 7


V. W. T. Chu

Bhat, A. N., Landa, R. J., & Galloway, J. C. (2011). Current per- Fitzpatrick, R. C., Taylor, J. L., & McCloskey, D. I. (1992). Ankle
spectives on motor functioning in infants, children, and adults stiffness of standing humans in response to imperceptible per-
with autism spectrum disorders. Physical Therapy, 91, 1116– turbation: reflex and task-dependent components. The Journal
1129. http://doi.org/10.2522/ptj.20100294ptj.20100294[pii] of Physiology, 454, 533–547. http://doi.org/10.1113/jphy-
Blanche, E. I., Bodison, S., Chang, M. C., & Reinoso, G. (2012). siol.1992.sp019278
Development of the comprehensive observations of propriocep- Fugl-Meyer, A. R., Jaasko, L., Leyman, I., Olsson, S., & Steglind,
tion (COP): Validity, reliability, and factor analysis. The Ameri- S. (1975). The post-stroke hemiplegic patient. 1. A method for
can Journal of Occupational Therapy , 66, 691–698. http://doi. evaluation of physical performance. Scandinavian Journal of
org/10.5014/ajot.2012.003608 Rehabilitation Medicine, 7, 13–31.
Brunt, D., Andersen, J. C., Huntsman, B., Reinhert, L. B., Thorell, Gardner, E. P., Martin, J. H., & Jessell, T. M. (2000). The bodily
A. C., & Sterling, J. C. (1992). Postural responses to lateral per- senses. In E. R. Kandel, J. H. Schwarz, & T. M. Jessell (Eds.),
turbation in healthy subjects and ankle sprain patients. Medicine Principles of neural science (4th ed., pp. 430–450). New York,
and Science in Sports and Exercise, 24, 171–176. NY: McGraw-Hill.
Bundy, A. C., Lane, S. E., & Murray, E. A. (2002). Sensory inte- Gilman, S. (2002). Joint position sense and vibration sense: ana-
gration: Theory and practice (2nd ed.). Philadelphia, PA: F. A. tomical organisation and assessment. Journal of Neurology,
Davis Company. Neurosurgery & Psychiatry, 73, 473–477. http://doi.org/
Chu, V. W., Hornby, T. G., & Schmit, B. D. (2015). Perception 10.1136/jnnp.73.5.473
of lower extremity loads in stroke survivors. Clinical Neuro- Goble, D. J. (2010). Proprioceptive acuity assessment via joint
physiology, 126, 372–381. http://doi.org/10.1016/j.clinph. position matching: from basic science to general practice. Phys-
2014.06.047 ical Therapy, 90, 1176–1184. http://doi.org/10.2522/
Colebatch, J. G., & McCloskey, D. I. (1987). Maintenance of con- ptj.20090399
stant arm position or force: Reflex and volitional components in Goble, D. J., Hurvitz, E. A., & Brown, S. H. (2009). Deficits in the
man. The Journal of Physiology, 386, 247–261. http://doi.org/ ability to use proprioceptive feedback in children with hemiple-
10.1113/jphysiol.1987.sp016532 gic cerebral palsy. International Journal of Rehabilitation
Coleman, R., Piek, J. P., & Livesey, D. J. (2001). A longitudinal Research, 32, 267–269. http://doi.org/10.1097/
study of motor ability and kinaesthetic acuity in young children MRR.0b013e32832a62d5
at risk of developmental coordination disorder. Human Move- Goble, D. J., Lewis, C. A., Hurvitz, E. A., & Brown, S. H. (2005).
ment Science, 20, 95–110. Development of upper limb proprioceptive accuracy in children
Cooper, J., Majnemer, A., Rosenblatt, B., & Birnbaum, R. (1995). and adolescents. Human Movement Science, 24, 155–170.
The determination of sensory deficits in children with hemiple- http://doi.org/10.1016/j.humov.2005.05.004
gic cerebral palsy. Journal of Child Neurology, 10, 300–309. Guthrie, B., Porter, J., & Sparks, D. (1983). Corollary discharge
Crapse, T. B., & Sommer, M. A. (2008). Corollary discharge provides accurate eye position information to the oculomotor
across the animal kingdom. Nature Reviews Neuroscience, 9, system. Science, 221, 1193–1195.
587–600. http://doi.org/10.1038/nrn2457nrn2457[pii] Hall, L. A., & McCloskey, D. I. (1983). Detections of movements
Crowe, A., Keessen, W., Kuus, W., van Vliet, R., & Zegeling, A. imposed on finger, elbow and shoulder joints. The Journal of
(1987). Proprioceptive accuracy in two dimensions. Perceptual Physiology, 335, 519–533.
and Motor Skills, 64, 831–846. http://doi.org/10.2466/ Hay, L., & Redon, C. (1997). The control of goal-directed move-
pms.1987.64.3.831 ments in children: Role of proprioceptive muscle afferents.
De Santis, D., Zenzeri, J., Casadio, M., Masia, L., Morasso, P., & Human Movement Science, 16, 433–451. http://doi.org/
Squeri, V. (2014). A new method for evaluating kinesthetic acu- 10.1016/S0167-9457(97)00005-5
ity during haptic interaction. Robotica, 32, 1399–1414. http:// Hearn, M., Crowe, A., & Keessen, W. (1989). Influence of age on pro-
doi.org/10.1017/S0263574714002252 prioceptive accuracy in two dimensions. Perceptual and Motor
Dover, G., & Powers, M. E. (2003). Reliability of Joint Position Skills, 69, 811–818. http://doi.org/10.2466/pms.1989.69.3.811
Sense and Force-Reproduction Measures During Internal and Hurkmans, E. J., van der Esch, M., Ostelo, R. W. J. G., Knol, D.,
External Rotation of the Shoulder. Journal of Athletic Training, Dekker, J., & Steultjens, M. P. M. (2007). Reproducibility of
38, 304–310. the measurement of knee joint proprioception in patients with
Dunn, W. (1999). The Sensory profile manual. San Antonio, TX: osteoarthritis of the knee. Arthritis and Rheumatism, 57, 1398–
Psychological Corporation. 1403. http://doi.org/10.1002/art.23082
Eklund, G. (1972). Position sense and state of contraction; the Johnston, O., Short, H., & Crawford, J. (1987). Poorly coordinated
effects of vibration. Journal of Neurology, Neurosurgery & children: A survey of 95 cases. Child: Care, Health and Devel-
Psychiatry, 35, 606–611. http://doi.org/10.1136/jnnp.35.5.606 opment, 13, 361–376.
Elliott, J. M., Connolly, K. J., & Doyle, A. J. (1988). Development Khasnis, A., & Gokula, R. M. (2003). Romberg’s test. Journal of
of kinaesthetic sensitivity and motor performance in children. Postgraduate Medicine, 49, 169–172.
Developmental Medicine and Child Neurology, 30, 80–92. Lafargue, G., Paillard, J., Lamarre, Y., & Sirigu, A. (2003). Pro-
Evarts, E. V, & Granit, R. (1976). Relations of reflexes and duction and perception of grip force without proprioception: Is
intended movements. Progress in Brain Research, 44, 1–14. there a sense of effort in deafferented subjects? The European
http://doi.org/10.1016/S0079-6123(08)60719-0 Journal of Neuroscience, 17, 2741–2749.
Falk, T. H., Tam, C., Schwellnus, H., & Chau, T. (2010). Grip LaRue, J., Bard, C., Fleury, M., Teasdale, N., Paillard, J., For-
force variability and its effects on children’s handwriting legi- get, R., & Lamarre, Y. (1995). Is proprioception important
bility, form, and strokes. Journal of Biomechanical Engineer- for the timing of motor activities? Canadian Journal of
ing, 132, 114504. http://doi.org/10.1115/1.4002611 Physiology and Pharmacology, 73, 255–261. http://doi.org/
Fatoye, F., Palmer, S., Macmillan, F., Rowe, P., & van der Linden, 10.1139/y95-036
M. (2009). Proprioception and muscle torque deficits in children Laszlo, J. I., & Bairstow, P. J. (1980). The measurement of kinaes-
with hypermobility syndrome. Rheumatology (Oxford, England), thetic sensitivity in children and adults. Developmental Medi-
48, 152–157. http://doi.org/10.1093/rheumatology/ken435 cine and Child Neurology, 22, 454–464.

8 Journal of Motor Behavior


Proprioception and Motor Development

Laszlo, J. I., & Bairstow, P. J. (1985). Test of kinaesthetic sensitiv- Sainburg, R. L., Poizner, H., & Ghez, C. (1993). Loss of proprio-
ity. London, England: Senkit PTY in association with Holt, ception produces deficits in interjoint coordination. J Neurophy-
Rinehart and Winston. siol, 70, 2136–2147.
McCloskey, D. I. (1978). Kinesthetic sensibility. Physiological Schmidt, R., & Lee, T. (2014). Motor learning and performance:
Reviews, 58, 763–820. From principles to application (5th ed.). Champaign, IL:
Mon-Williams, M. A., Wann, J. P., & Pascal, E. (1999). Visual-propri- Human Kinetics.
oceptive mapping in children with developmental coordination dis- Schneck, C. M. (1991). Comparison of pencil-grip patterns in first
order. Developmental Medicine and Child Neurology, 41, 247–254. graders with good and poor writing skills. American Journal of
Murtaugh, K., & Costigan, P. A. (2003). Evaluating the proprio- Occupational Therapy, 45, 701–706. http://doi.org/10.5014/
ception of lower extremity loads. Queen’s Health Sciences ajot.45.8.701
Journal, 6(2), 15–18. Schoemaker, M. M., van der Wees, M., Flapper, B., Verheij-Jan-
Pai, Y. C., Rymer, W. Z., Chang, R. W., & Sharma, L. (1997). sen, N., Scholten-Jaegers, S., & Geuze, R. H. (2001). Perceptual
Effect of age and osteoarthritis on knee proprioception. Arthritis skills of children with developmental coordination disorder.
and Rheumatism, 40, 2260–2265. http://doi.org/10.1002/1529- Human Movement Science, 20, 111–133.
0131(199712)40:12<2260::AID-ART22>3.0.CO;2-S Sherrington, C. S. (1906). The Integrative action of the Nervous
Parham, L. D., & Ecker, C. (2007). Sensory processing measure. System. New Haven, CT: Yale University Press.
Los Angeles, CA: Western Psychological Services. Sigmundsson, H., Whiting, H. T., & Loftesnes, J. M. (2000).
Pickard, C. M., Sullivan, P. E., Allison, G. T., & Singer, K. P. Development of proprioceptive sensitivity. Experimental Brain
(2003). Is There a Difference in Hip Joint Position Sense Research, 135, 348–352.
Between Young and Older Groups? The Journals of Gerontol- Smyth, M. M., & Mason, U. C. (1998). Use of proprioception in
ogy Series A: Biological Sciences and Medical Sciences, 58, normal and clumsy children. Developmental Medicine and
M631–M635. http://doi.org/10.1093/gerona/58.7.M631 Child Neurology, 40, 672–681.
Piek, J. P., & Skinner, R. A. (1999). Timing and force control dur- Stillman, B. C. (2002). Making sense of proprioception. Physio-
ing a sequential tapping task in children with and without motor therapy, 88, 667–676. http://doi.org/10.1016/S0031-9406(05)
coordination problems. Journal of the International Neuropsy- 60109-5
chological Society, 5, 320–329. Van Beers, R. J., Sittig, A. C., & Denier van der Gon, J. J. (1998).
Pincivero, D. M., Bachmeier, B., & Coelho, A. J. (2001). The The precision of proprioceptive position sense. Experimental
effects of joint angle and reliability on knee proprioception. Brain Research, 122, 367–377. http://doi.org/10.1007/s0022100
Medicine and Science in Sports and Exercise, 33, 1708–1712. 50525
Priebe, M. M., Sherwood, A. M., Thornby, J. I., Kharas, N. F., & Van Deursen, R. W., & Simoneau, G.G. (1999). Foot and ankle
Markowski, J. (1996). Clinical assessment of spasticity in spinal sensory neuropathy, proprioception, and postural stability. The
cord injury: A multidimensional problem. Archives of Physical Journal of Orthopaedic and Sports Physical Therapy, 29, 718–
Medicine and Rehabilitation, 77, 713–716. http://doi.org/ 726. http://doi.org/10.2519/jospt.1999.29.12.718
10.1016/S0003-9993(96)90014-3 Von Hofsten, C., & R€ osblad, B. (1988). The integration of sensory
Proske, U. (2005). What is the role of muscle receptors in information in the development of precise manual pointing.
proprioception? Muscle & Nerve, 31, 780–7. http://doi.org/ Neuropsychologia, 26, 805–821.
10.1002/mus.20330 Warner, J. J. P., Lephart, S., & Fu, F. H. (1996). Role of proprio-
Proske, U., & Gandevia, S. C. (2012). The proprioceptive senses: ception in pathoetiology of shoulder instability. Clinical Ortho-
their roles in signaling body shape, body position and move- paedics and Related Research, 330, 35–39.
ment, and muscle force. Physiological Reviews, 92, 1651–97. Weimer, A. K., Schatz, A. M., Lincoln, A., Ballantyne, A.
http://doi.org/10.1152/physrev.00048.2011 O., & Trauner, D. A. (2001). “Motor” impairment in
Proske, U., Schaible, H.-G., & Schmidt, R. F. (1988). Joint recep- Asperger syndrome: Evidence for a deficit in propriocep-
tors and kinaesthesia. Experimental Brain Research, 72, 219– tion. Journal of Developmental and Behavioral Pediatrics,
224. http://doi.org/10.1007/BF00250245 22, 92–101.
Rawlence, C. (1998). The man who lost his body. London, Eng- Wurtz, R. H., & Sommer, M. A. (2004). Identifying corollary dis-
land: BBC’s Horizon Series. charges for movement in the primate brain. Progress in Brain
Riemann, B. L., & Lephart, S. M. (2002). The sensorimotor sys- Research, 144, 47–60. http://doi.org/10.1016/S0079-6123(03)
tem, part I: The physiologic basis of functional joint stability. 14403-2
Journal of Athletic Training, 37, 71–79.
Sainburg, R. L., Ghilardi, M. F., Poizner, H., & Ghez, C. (1995). Received January 30, 2016
Control of limb dynamics in normal subjects and patients with- Revised June 25, 2016
out proprioception. Journal of Neurophysiology, 73, 820–835. Accepted July 19, 2016

2016, Vol. 0, No. 0 9

You might also like