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Scand J Med Sci Sports 2014: : 2014 John Wiley & Sons A/S.

doi: 10.1111/sms.12181 Published by John Wiley & Sons Ltd

Review

Neuromechanical coupling in the regulation of muscle tone and


joint stiffness
A. R. Needle, J. Baumeister, T. W. Kaminski, J. S. Higginson, W. B. Farquhar, C. B. Swanik
Department of Health and Exercise Science, Appalachian State University, Boone, North Carolina, USA
Corresponding author: Alan R. Needle, PhD, ATC, CSCS, Holmes Convocation Center 011, 111 Rivers St., ASU Box 32071, Boone,
NC 28608, USA. Tel: 828-262-4039, Fax: 828-262-3138, E-mail: needlear@appstate.edu
Accepted for publication 23 December 2013

The ability of the nervous system to accommodate outcomes, although research using proprioceptive tasks
changes to joint mechanics is crucial in the maintenance and quantifying reaction times has led to equivocal
of joint stability and the prevention of injury. This results. Recent innovations have allowed for the simulta-
neuromechanical coupling is achieved through several neous measurement of mechanical and nervous system
mechanisms such as the central and peripheral regulation function among these subsets. The intent of this review
of muscle tone and subsequent alterations to joint stiff- was to explore the relationships between joint stiffness
ness. Following joint injury, such as a ligamentous and nervous system function, and how it changes follow-
sprains, some patients develop functional instability or ing injury. By better understanding these mechanisms,
require surgery to stabilize the joint, while others are able researchers and clinicians may better develop and imple-
to cope and display limited impairments. Several ment rehabilitation protocols to target individual deficits
researchers have attempted to explain these divergent among injured populations.

The maintenance of joint stability is a critical factor of decerebrate felines (Bosma & Gellhorn, 1947; Eccles
for daily function and the prevention of falls and injury. & Lundberg, 1959; Burke, 1983; Sinkjaer, 1997;
Throughout physical activity, the neurological and Breakefield et al., 2008). However, limited research
mechanical components of a joint must work collec- exists regarding potential mechanisms capable of alter-
tively to both prepare for and react to injurious pertur- ing this descending drive among healthy adults, as well
bations (Sherrington, 1911; Freeman & Wyke, 1967; as those with joint injury. This information would be
Lacroix, 1981; Sinkjaer et al., 1988; Johansson et al., clinically useful because tone may be described as the
1991). The result of this neuromechanical coupling is a muscles state of readiness, which can be modified
modulation in muscle tone that can optimize joint stiff- based on specific functional tasks and the individuals
ness for specific tasks, contributing toward injury pre- level of anxiety (Saper, 2000; Davis et al., 2011). There-
vention and improved functional performance (Sinkjaer fore, the neuromechanical properties of muscle tone
et al., 1988; Nielsen et al., 1994). The intent of this have an important role for both maximizing functional
article is to examine the combined influence of muscle performance and preventing injury.
tone and joint stiffness regulation with specific consid-
eration to their roles in sports medicine practice. Peripheral mechanisms

Muscle tone Original theories suggested that muscle tone is mediated


peripherally by the fusimotor system the neural circuits
The phenomenon of muscle tone is a commonly misun- existing between the muscle spindle, its afferent axons
derstood concept when discussing injury prevention and (Type Ia & Type II) and the gamma () motor neurons
athletic performance (Masi & Hannon, 2008). Defined as that act to alter spindle sensitivity by changing the length
the low-level steady-state muscle contraction at rest, it and tension of intrafusal fibers (Burke, 1983; Johansson
exists unconsciously, and controls the tautness of a et al., 1986; Bergenheim et al., 1995; Pearson & Gordon,
relaxed muscle. Upon passive stretching of muscles with 2000). This increase, or gain in the gamma motor neuron
heightened tone, the mechanical response will be drive is associated with coactivation of the alpha motor
increased resistance to length changes (Davidoff, 1992). neurons controlling the contraction of the extrafusal
Much of what we understand about muscle tone relates skeletal muscle fibers (Johansson et al., 1986; Knutson,
to pathological populations including forms of hyperto- 2000). Therefore, increased activity of the fusimotor
nicity such as spasticity and rigidity; or in vitro models system translates into higher levels of resting skeletal

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Needle et al.
Table 1. Classification and conditions affecting muscle tone

Condition Description Potential Cause(s)

Hypotonicity Abnormal decrease in muscle tone; associated with hypoactive Lower motor neuron lesions
reflexes Posterior cerebellar lobe lesions
Hypertonicity Abnormal increase in muscle tone with resistance to active and Upper motor neuron lesions
passive movement; associated with hyperactive reflexes Anterior cerebella lobe lesions
Rigidity Hypertonicity to muscles on both sides of a joint Parkinsons disease and other neurological disorders
Spasticity Hypertonicity on one side of a joint Spinal cord injury above T12, head injury, cerebrovascular
accident, cerebral palsy
Clonus Uncontrolled oscillation of muscle in a spastic muscle group Upper motor neuron lesions
Dystonia Involuntary muscle contraction and abnormal posture in a specific Task-specific
part of the body Interruption of cortical-basal ganglia loops.

Adapted from: Gutman, S.A. 2001, Quick Reference Neuroscience for Rehabilitation Professionals, 1st edition, Slack, Inc., Thorofare, NJ.

muscle contraction or tone. When this reflexive loop connect tone to the muscles state of readiness, we
becomes overactive, disorders of muscle tone such as should consider the process of events necessary for alter-
spasticity and hyperreflexia may occur (Burke, 1983; ing tone from a resting, baseline state.
Sinkjaer, 1997; Hallett, 1998; Breakefield et al., 2008; If the nervous system had to be turned on, such as
Hall, 2011). However, this approach to understanding awaking from a deep sleep, the sequence for generating
muscle tone is somewhat isolated to the peripheral muscle tone would proceed as such. The reticular for-
nervous system (PNS), but it is known that altera- mation will emit excitatory signals to arouse the brain
tions to the central nervous system (CNS) can lead to and trigger awareness across the cerebral cortex. Signals
pathologies related to muscle tone (Table 1) (Bosma & originating in the brainstem and cerebellum will travel to
Gellhorn, 1947; Eccles & Lundberg, 1959; Burke, the gamma motor neurons along extrapyramidal path-
1983). ways including the reticulospinal, vestibulospinal and
rubrospinal tracts. Muscle tone will then begin to spread
through extrapyramidal pathways that include the
Central mechanisms reticulospinal, vestibulospinal and rubrospinal tracts
Several central mechanisms have been associated with originating in the brainstem and cerebellum travelling to
heightened muscle tone including pathways from the the gamma motor neurons (Moruzzi & Magoun, 1949;
cerebellum, basal ganglia and thalamus (Burke, 1983; Siegel et al., 1983; Saper, 2000; Hall, 2011). This causes
Saper, 2000; Hall, 2011). These structures are capable of the spindle to become taut, as if the muscle were sud-
altering muscle spindle sensitivity by regulating inhibi- denly stretched, stimulating the intrafusal spindle
tion to the fusimotor loop (Eccles & Lundberg, 1957). sensory organ. The intrafusal fibers generate an excit-
Therefore, increased intracortical inhibitory activity is atory afferent signal that is transmitted back to the spinal
responsible for decreasing muscle tone (Eccles & cord through fast sensory nerves. These sensory fibers
Lundberg, 1957; Rymer et al., 1979; Ridding et al., directly synapse with motor neurons, resulting in a
1995; Hallett, 1998). Much of what we know about this monosynaptic stretch reflex and contraction of the same
relationship comes from observations among patients muscle containing the spindles (Pearson & Gordon,
with CNS disorders that, for a variety of reasons, have 2000). Together, with signals from the corticospinal
difficulty regulating inhibitory and excitatory signals tract, with modification by the basal ganglia, the alpha-
within the CNS. This leads to an outward appearance gamma co-activation will establish baseline levels of
of altered muscle tone, including spasticity and dysto- muscle tone (Burke, 1983). This would initially be medi-
nia (Breakefield et al., 2008). Findings of decreased ated simply through the fusimotor loop; however, as this
intracortical inhibition are consistently observed in process occurs, the anterior and posterior spinocerebellar
spastic and dystonic populations, as well as increased tracts will transmit new proprioceptive information to
motor excitability suggesting a loss of cortical mediation the cerebellum (Saper, 2000). The result leads to a
where the excitatory pathways are left uninhibited, feedforward/feedback loop such that the cerebellum
leading to continuous increased motor neuron firing modifies activity of the brainstem and basal ganglia to
(Ridding et al., 1995; Devanne et al., 1997; Hallett, control tone (King, 1948; Saper, 2000; Hall, 2011).
1998). Because of these complex interrelationships Without inhibition from higher cortical structures, the
among the PNS and CNS, very few studies have original monosynaptic stretch reflex is so potent that an
attempted to quantify subtle differences in muscle tone individual would exhibit hypertonicity or spasticity, and
among healthy or athletic patients, although preliminary movement becomes abrupt and erratic (Breakefield
links have been observed between the mechanical stiff- et al., 2008; Hall, 2011). In circumstances where indi-
ness of the joint and these cortical measures (Needle viduals become anxious, the cortex normally decreases
et al., 2013a). To comprehend this relationship and inhibitory influences, allowing for an increased stretch

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Neuromechanical coupling and stiffness regulation
reflex and heightened muscle tone. This may serve to inhibitory mechanisms observed from these measures
maximize muscular responsiveness and protect the indi- have been associated with the corticofugal projection
vidual under stressful conditions (Davis et al., 2011). fibers to the basal ganglia and thalamus the same
However, if muscle tone is increased excessively, such as pathways leading to hypertonicity (Hallett, 2007). Iden-
when an individual becomes startled, it could disrupt tifying these CNS correlates of muscle tone creates the
normal agonist antagonist co-activation and inhibition opportunity to study how neuromechanical coupling may
(Freeman & Wyke, 1965, 1967). This leads to erratic be affected among injuries common to sports medicine
movements and subsequent errors in coordination that practice.
decrease functional performance and increase risk of While much remains unknown about muscle tone, it
injury (Iversen et al., 2000; Swanik et al., 2007; Moffit, appears that this property provides a strong link between
2008; Mobbs et al., 2009). the PNS, the CNS and the mechanical properties of the
joint. Therefore, when one considers the phenomenon of
joint instability as consisting of both mechanical and
Measurement of tone neurophysiological deficits, it warrant questions by both
Our understanding of muscle tone, in otherwise neuro- clinicians and researchers regarding how this quality
logically healthy individuals, has been limited by the may affect the ability to protect the joint while maximiz-
absence of instruments to concurrently measure both ing functional performance.
neural and mechanical contributors with sufficient
temporal resolution to couple events. Quantifying joint Muscle and joint stiffness
stiffness by applying a sudden perturbation has been
previously utilized to quantify tone (Boiteau et al., 1995; Modification of muscle tone is one component contrib-
Lorentzen et al., 2012); however, limitations exist as uting to a joints stiffness properties. Defined as the
these characteristics are dependent on the velocity of the resistance of the joint and its supporting structures to
perturbation, and the almost instantaneous superimposi- stretch, these stiffness properties would determine the
tion of reflexive muscle responses (Sinkjaer, 1997). While amount of force required to cause injury (Latash &
several investigators have constructed customized Zatsiorsky, 1993). This has important clinical implica-
devices to measure muscle tone, no device has been used tions as higher joint stiffness may represent better joint
consistently throughout the literature, potentially because stability and a failure to appropriately regulate stiffness
of poor reliability (Boiteau et al., 1995; Lorentzen et al., contributes to injury (Johansson et al., 1991; Wilson
2012). Therefore, some researchers have focused on et al. 1991a). Alternately, to improve performance, stiff-
understanding the brains relationship to resting muscle ness must be optimized, using potentially less stiffness
activity and stiffness. or greater compliance to allow for greater absorption of
One tool for investigating this relationship, transcranial load and storing elastic energy. Selective muscle recruit-
magnetic stimulation, is often employed because of its ment may therefore be necessary to allow individuals to
versatility as techniques allow for understanding both operate within an ideal performance envelope and avoid
excitatory and inhibitory mechanisms of cortical motor injury (Bach et al., 1983; Wilson et al. 1991a; Gottlieb,
neurons (Hallett, 2007). This technique involves admin- 1996). Often represented by a load-deformation curve
istration of brief magnetic pulses over various areas of the that represents the amount of displacement per unit
cerebral cortex, sometimes with multiple pulses applied force, these properties may predict the force at which a
rapidly, and measuring the size of a motor response from tissue would become damaged. Additionally, by study-
a targeted muscle (Devanne et al., 1997; Hallett, 2007). ing the toe region during which the joint moves from a
Several transcranial magnetic stimulation-derived vari- shortened state to its resting length, we may understand
ables have been linked to disorders of muscle tone. the threshold at which embedded mechanoreceptors
Among patients with hand-grip dystonia, separate studies might be stimulated (Sinkjaer et al., 1988; Wilson et al.,
have reported a higher gain in the stimulus-response 1991b). While each tissue possesses its own stiffness
properties, indicating that for a given size stimulus, there characteristics, the overall joint stiffness is representa-
exists a more rapid recruitment of additional cortical tive of the combined resistance from the surrounding
motor neurons. These findings indicate stronger connec- joint capsule, ligaments, muscle and skin. All of these
tions between the brain and the muscle, and perhaps a structures have their own intrinsic properties, but mus-
disorder of cortical modification to the alpha motor cular stiffness would additionally be modulated by the
neurons (Ridding et al., 1995). While these excitatory amount of contraction and formed crossbridges.
connections are an important link, it is important to recall
that inhibitory mechanisms within the cortex are largely
responsible for downregulating the stretch reflex and Passive stiffness
muscle tone. Thus, accordingly, suppression of inhibitory Muscular contraction adds a degree of complexity to the
pathways (disinhibition) is present among hypertonic joints stiffness, creating a link between the joints resis-
populations (Ridding et al., 1995; Hallett, 2007). The tance to load and neuromuscular function (Sinkjaer

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Needle et al.
et al., 1988; Latash & Zatsiorsky, 1993). In a relaxed laxity changes in the capsuloligamentous structures, as
state, with volitional muscle activity absent, stiffness is well as resistance from the relaxed muscle (Kovaleski
regulated largely by the elastic components of the sur- et al., 2002; Needle et al., 2013a). An advantage of these
rounding joint capsule, ligaments, the parallel and series devices is their ability to identify deficits across discrete
elastic components from the musculotendinous unit, and loading ranges, and offer a unique opportunity to study
resting muscle tone (Sinkjaer et al., 1988; Toft et al., the toe region where early mechanoreceptor stimula-
1989a, b). If a joint perturbation is of enough speed and tion occurs (Needle et al., 2013b). Investigators have
magnitude, a reflexive muscle response may, almost used free oscillating platforms or motors to apply a rota-
instantaneously, aid in increasing joint stiffness. As tional perturbation to a joint, while the resistance the
muscle spindles mediate the monosynaptic reflex, the joint provides is measured through a load cell. These
amount of muscle tone and subsequent sensitivity of devices allow for measurement of stiffness over a variety
those receptors could potentially increase the likelihood of controlled conditions, with the ability to manipulate
of a reflexive response (Nielsen et al., 1994). For the amount of volitional muscle contraction (Thomas
instance, if muscle tone were higher, this would imply a et al., 2013; Zinder et al., 2009). Furthermore, perturba-
higher gain to the muscle spindle, and therefore an tions applied with a motor offer the advantage of con-
increased sensitivity to stretch. While passive stiffness trolling the exact magnitude, velocity and acceleration of
has been studied in sports medicine research, the exact the perturbation to closely replicate injurious mecha-
contributions of muscle tone are unclear as this resting nisms, whereas oscillatory platforms derive stiffness
activity is not apparent on electromyography. from the dampening response of the device (Otis et al.,
1983; Latash & Zatsiorsky, 1993; Oatis, 1993; Swanik
et al., 2004; Blackburn et al., 2006; Huxel et al., 2008).
Contribution of volitional contraction Finally, calculating joint stiffness through inverse
Volitional muscle activity has a profound effect on the dynamics during motion analysis has been used to quan-
stiffness of the joint, leading to more than fourfold tify changes while performing an activity, but these
increase in measured joint resistance simply by main- values may not reflect loads associated with injury
taining a baseline level of precontraction throughout a (McGinnis et al., 2013; Shamaei et al., 2013).
perturbation (Huxel et al., 2008; Thomas et al., 2013).
This increase from muscular stiffness represents the Joint injury pathway
individuals ability to regulate the reverse cycling of the
actin-myosin crossbridges (Nielsen et al., 1994; Huxel As muscle tone and the subsequent joint stiffness demon-
et al., 2008; Thomas et al., 2013). Furthermore, as an strate a coupling of the nervous system and joint mechan-
individual experiences a potentially injurious load, ics, they have an important role in the preparation and
length changes in the surrounding muscle would initiate responses to joint perturbations. Prevention of joint injury is
reflexive muscular activation, which may serve to create often addressed through two separate mechanisms: feed-
a more drastic increase in joint stiffness to protect back (closed-loop/reactive) and feedforward (open-loop/
musculoskeletal structures. The relationship between preparatory) neuromuscular control (Lacroix, 1981; Dunn
muscle activation and joint stiffness therefore represents et al., 1986). To understand these concepts, it is helpful to
the capacity to integrate mechanical and neurophysi- address the cascade of events that lead to injury from the
ologic mechanisms to improve performance and prevent start of a perturbation.
injury.
Application of a load
Stiffness measurement techniques As the joint is loaded and stress is applied to the sup-
Several researchers have investigated joint stiffness porting tissues, a complex sensorimotor response at mul-
in healthy and injured populations. Methods include tiple levels of the nervous system is triggered. Initial
handheld devices such as joint arthrometry (Fox et al., detection of the load is dependent on the peripheral
1985; Kovaleski et al., 2002, 2008; Bahk et al., 2007), mechanoreceptors embedded in the skin, joint capsule,
application of joint perturbations (Huxel et al., 2008; ligaments and the musculotendinous unit (Freeman &
Zinder et al., 2009) and use of motion analysis and Wyke, 1965, 1967; Johansson, 1991; Hutton & Atwater,
inverse dynamics to calculate joint stiffness during 1992; Michelson & Hutchins, 1995). These receptors
activity (McGinnis et al., 2013; Shamaei et al., 2013). include both slow- and fast-adapting receptors that
Arthrometry involves the manual application of transla- detect stretch, tension and load (Michelson & Hutchins,
tional or rotational stresses of a known load, allowing 1995). Arguably, the most important of these receptors
investigators to study the contributions of passive struc- are the muscle spindles, as afferents from other joint
tures to joint stiffness across various ranges (Fox et al., mechanoreceptors act to modify fusimotor activity
1985; Kovaleski et al., 2002; Bahk et al., 2007). These through polysynaptic reflex pathways (Johansson et al.,
devices are designed to passively quantify stiffness and 1986, 1991). Some of the most compelling evidence for

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Neuromechanical coupling and stiffness regulation
the role of muscle spindle activity on peripheral sensa- et al., 1988; Konradsen 2002b; Swanik et al., 2004).
tion was derived by Johansson et al. (1986) in a series of Therefore, if the quickest response is not enough to
studies that severed the feline anterior cruciate ligament protect the joint, how would a volitional response
and observed altered afferent spindle activity. It was (180250 ms) provide stabilization to the joint?
hypothesized that as muscle spindle sensitivity was One answer to this timing dilemma is found in the
modifiable by ascending and descending pathways, these preparatory, or feedforward, muscle activity. Before each
spindle afferents transmitted a final common input of joint load, whether landing from a jump or taking a step,
sensory activity to the nervous system. Furthermore, sev- muscular tension is produced to prepare the joint for
ering the anterior cruciate ligament and thereby remov- impact, with the amount highly modifiable to account for
ing its afferent input had a profound effect on spindle any unforeseen perturbations or unanticipated events
sensitivity, and therefore could influence the reflexive (such as landing on someones foot or stepping on an
responses in muscles surrounding the joint (Johansson uneven surface) (Dunn et al., 1986; Huxel et al., 2008;
et al., 1991). Gutierrez et al., 2009). This serves two main purposes.
The input from the muscle spindle to the spinal cord First, joint pre-activation will increase the muscle activ-
may be enough to trigger a monosynaptic reflex provid- ity and subsequent stiffness of the joint, meaning
ing some degree of joint stabilization. However, the a higher amount of load would be required to perturb the
afferent stimulus will continue to ascend in the CNS via joint (Latash & Zatsiorsky, 1993; Huxel et al., 2008;
the dorsal column-medial lemniscal and spinothalamic Thomas et al., 2013). Second, this pre-activation will
tracts to the thalamus, internal capsule, and ultimately increase the aforementioned fusimotor activity for the
the somatosensory cortex, with parallel tracts (spinocer- muscles surrounding the joint through alpha-gamma
ebellar and spinoreticular) conveying sensory informa- coactivation, allowing for quicker sensation of length
tion to the medulla, pons and cerebellum (Prudhomme change, with faster and larger reflexive responses (Dietz
& Kalaska, 1994; Hall, 2011). While these pathways et al., 1981; Johansson et al., 1986; Bergenheim et al.,
may be enough to induce reflexive responses from higher 1995). This pre-activation therefore serves to both
centers, largely through the cerebellums role in the protect the joint prior to load and facilitate a response in
maintenance of tone, a volitional response to stabilize the case of an unanticipated perturbation.
the joint will form in the primary motor cortex (Kolb Muscular pre-activation may also be modified by
et al., 1997; Ehrsson et al., 2007). To initiate this several factors. These include memory, visual cues, ves-
response, projection fibers from the somatosensory tibular cues and planning (Gottlieb, 1996; Hermsdrfer
cortex will extend toward the prefrontal cortex, supple- et al., 2008; Jackson et al., 2009). This means that signals
mentary motor areas, premotor areas and, ultimately, the from the frontal, temporal and occipital lobes act
primary motor cortex. This is where a volitional muscle together to change activity from the primary motor cortex
activity will be triggered by motor neuron bodies in the and supplementary motor areas. In many cases, the
cortex, with their axons forming the descending cortico- integration of information may serve to optimize levels of
spinal tracts, leading to contraction (or potentially deac- pre-activation based on visual cues, such as seeing an
tivation) of stabilizing muscles (Hall, 2011). uneven surface or recalling successful movement strate-
gies from previous experience. However, these complex
interconnections could also serve to negatively impact
Preparing for injury joint stability. Increased cognitive loading and anxiety
As the speed at which these events occur is extremely may lead either to a decreased amount of pre-activation
fast, limited instrumentation is capable of investigating and altered tone, or alternately a rapid, mistimed activa-
this chain of events in vivo to determine the loading tion of various muscles that could negatively impact joint
stimulus intensities and velocities necessary to elicit stability (Moffit, 2008). Some researchers have suggested
responses at each level, or precisely how the CNS opti- that these associations may contribute to a negative feed-
mizes muscle tone and joint stiffness for the prevention back loop following injury that contributes to recurrent
of injuries. However, multiple studies have investigated problems such as reinjury and instability (Wikstrom
the input and output of the system in isolated situa- et al., 2013).
tions. This involves perturbing the joint and measuring Limited studies have investigated the ability of the
the relative timing and amplitude of the muscle response CNS to rapidly negotiate an appropriate response to joint
or stiffness change following a joint perturbation perturbations. Currently, changes in sensorimotor control
(Konradsen & Ravn, 1991; Konradsen 2002b; Myers that occur centrally are quantified using functional mag-
et al., 2004; Delahunt, 2007). While the effect of joint netic resonance imaging (fMRI) (Kapreli et al., 2009) or
injury on this ability has led to conflicting results, electroencephalography (EEG) (Baumeister et al., 2008).
researchers have hypothesized that the fastest reflexive Both of these techniques have various strengths and limi-
muscle responses (approximately 3080 ms) may not be tations, as fMRI offers high spatial resolution and low
rapid enough to prevent ligamentous injury (occurring as temporal resolution, with the converse true of EEG. One
quickly as 50 ms) (Freeman & Wyke, 1967; Sinkjaer notable study by de Graaf et al. (2009) used fMRI to

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Needle et al.
examine activity of the primary and secondary motor and neuromuscular control most often use indirect method-
sensory areas before and after a perturbation, with instruc- ology: tests that require motor output (depression of a
tions to either resist or allow for a passive perturbation. An switch, contraction of a muscle) following a propriocep-
increase in primary motor cortex and somatosensory tive cue (joint movement or loading) to presume changes
cortex activity in preparation for the activity was observed, in the nervous system (Riemann & Lephart, 2002).
suggesting both an increase in motor pre-activation and However, many neurophysiological processes occur in
preparatory sensation where the brain may be anticipating the latency between onset of the cue and the motor
how a perturbation should feel. This demonstrates the role output, making it difficult to detect impairments
of the cortex to not only increase joint stiffness prior to a (Konradsen 2002a; Munn et al., 2010). Second, current
load, but also reflexively plan potency of muscular reflexes research utilizing more direct measures of neurophysi-
in a feedforward manner (Henderson & Dittrich, 1998; ological control does so without quantifying mechanical
Santello, 2005; de Graaf et al., 2009). joint stability (Baumeister et al., 2008, 2011; Kapreli
et al., 2009; Pietrosimone et al., 2012). Therefore, it is
Joint instability difficult to determine how much muscle tone or joint
stiffness is normal for that patient, and how coupling
This review has addressed the normal processes behind between the mechanical joint properties and the PNS and
the regulation of muscle tone and joint stiffness and CNS become disrupted. Lastly, research frequently
how these work together to prepare for and react to employs study designs that compare unstable joints with
joint injury, but the question remains regarding how liga- the unaffected limb or with a group of uninjured sub-
mentous injury affects these processes. Complaints of jects; but, only recently have studies incorporated groups
functional joint instability, where a patient experiences of copers who suffer a joint injury but do not develop
repeated sensations of giving-way, are common in the recurrent instability as a secondary control group
ankle, knee and shoulder joints (Yeung et al., 1994; (Eastlack et al., 1999; Courtney et al., 2005; Wikstrom
Anandacoomarasamy & Barnsley, 2005; Clayton & & Brown, 2013). This cohort of subjects may be capable
Court-Brown, 2008; Murray et al., 2012). This may mani- of providing valuable insight into mechanisms through
fest as recurrent ankle sprains, loss of function which proper healing occurs, or how the nervous system
and frequent falls, and repeated subluxations of the shoul- may optimize itself and allow for healthy return to
der joint and, furthermore, have all been attributed to activity.
early onset post-traumatic osteoarthritis (Valderrabano To understand the mechanisms behind joint instabil-
et al., 2006; Clayton & Court-Brown, 2008). As these ity, it must be restated that episodes of rolling an ankle,
may arise following ligamentous injury, it was originally the knee giving-way or a shoulder subluxation repre-
believed that the repeated injuries were secondary to sents a failure to properly regulate joint stiffness (Wilson
increased joint laxity (Freeman, 1965). However, laxity et al., 1991a). While research exists supporting the role
did not correlate with sensations of instability as highly of increased laxity of the capsuloligamentous structures
lax joints may function normally, and previously injured, in complaints of joint instability (Lentell et al., 1995;
unstable joints may heal and present with no mechanical Hubbard et al., 2004), an equal or greater amount of
insufficiencies (Eastlack et al., 1999; Bahk et al., 2007; literature to the contrary is also present (Eastlack et al.,
Wikstrom & Brown, 2013). It was therefore suggested 1999; Kerkhoffs et al., 2001a). This therefore implies
that following injury, the ligament itself might heal, but that injury to the static joint stabilizers affect dynamic
the capsuloligamentous mechanoreceptors may remain restraint mechanisms, leading to failures in stiffness
damaged, limiting the proprioceptive information to the regulation and subsequent instability.
nervous system, altering both preparatory muscle activity
and delaying reaction times (Freeman et al., 1965;
Johansson et al., 1991; Lephart et al., 1997; Myers et al., Dynamic restraint mechanism and instability
2004). However, these proprioceptive and neuromuscular Many theories regarding altered dynamic restraint focus
deficits inconsistently correlate with sensations of joint on the peripheral deafferentation that may occur in
instability (Lephart et al., 1997; Arnold et al., 2009; capsuloligamentous receptors following injury. The
Munn et al., 2010; Wright & Arnold, 2011; Gokeler et al., most direct manifestation of this would be a delayed
2012; Laudner et al., 2012). As a result, the etiology and detection of an impending episode of giving-way,
more importantly optimal treatment of joint instability leading to a delayed muscular response. However, as
continue to elude clinicians and researchers. previously mentioned, proprioception has been inconsis-
tently correlated with history of injury or instability.
Furthermore, this proprioceptive deficit may only affect
Challenges in current research the feedback loop of neuromuscular control, with no
Some problems currently exist with investigations into change in the equally important feedforward (prepara-
joint instability. First, changes in proprioception (the tory) control (Konradsen 2002a; Gutierrez et al., 2009).
sensation of joint position, movement and force) and However, researchers have proposed altered mechanisms

6
Neuromechanical coupling and stiffness regulation
by which peripheral deafferentation may impair in this subset (Needle et al., 2013a). These findings
feedforward neuromuscular control, and subsequently suggest that the nervous system is tuned based upon the
the planning of future movements. As Johansson et al. mechanical properties of the joints, and more impor-
(1991) observed a potent effect of ligamentous afferents tantly this relationship is altered by injury. While corti-
on fusimotor activity and therefore muscle spindle cal research has only recently begun in these patient
sensitivity, one may recognize how damage to those populations, data suggest that neuromechanical cou-
ligamentous receptors could subsequently decrease pling may occur between the joint and nervous system,
fusimotor drive, and therefore amplify sensory deficits and ligamentous injury may cause neuroplasticity. Most
and lower muscle tone and stiffness. notably lacking from this line of research is compari-
sons of cortical changes in the context of alterations in
joint laxity to better understand the coupling of these
CNS changes following injury components.
Throughout the evolution of joint instability research, Few studies have incorporated direct neurophysi-
evidence has emerged supporting segmental and cortical ologic measures while quantifying mechanical laxity.
changes following joint injury. Some of these earlier However, those that have integrated these variables are
findings concentrated on the Hoffman reflex, a combi- observing links between the PNS and CNS, and joint
nation of sensory and motor activity, measuring spinal excursion (Needle et al., 2013a, b). This suggests that
excitability and fusimotor function. These data suggest innate asymmetries in laxity exist among the uninjured
that among unstable joints, this spinal excitability is population; however, the nervous system is tuned to that
diminished (McVey et al., 2005; Sefton et al., 2008; Kim innate laxity. Following injury, several adaptations can
et al., 2012). Two proposed mechanisms have been sug- occur to disrupt this relationship. For instance, while
gested to explain these changes, where decreased affer- joint laxity might increase, it may not be pathological;
ent activity from the joint receptors lowered fusimotor but the nervous system is no longer able to negotiate the
activity; or decreased cortical drive alters fusimotor increased joint excursion. Alternately, the nervous
function (Sefton et al., 2008; Palmieri-Smith et al., system might be affected following injury, whether from
2009). The use of microneurography (peripheral nerve peripheral deafferentation or inflammatory changes, and
recordings) has identified that muscle spindle afferents therefore the nervous system is no longer calibrated with
have a decreased response to joint loading among func- the joints mechanical properties (i.e., stiffness). This
tionally unstable ankles (Needle et al., 2013b). The neuromechanical decoupling may explain the highly
authors suggested this fusimotor dysfunction was a variable results observed across populations of unstable
result of peripheral deafferentation, providing the first joints, and could also potentially explain why some
direct measurements of a sensory deficit in this popula- patients do not develop instability following injury,
tion. However, limited research has studied cortical as the nervous system activity in copers may remain
changes among these populations. accurately tuned to mechanical constraints of the joint
Using techniques such as fMRI and EEG, researchers (Fig. 1).
have found discrete alterations among patients with a
history of joint injury and instability. Kapreli et al. Treatment
(2009) found that during simple knee flexion and exten-
sion, patients with a history of anterior cruciate ligament Following injury, a cascade of mechanical, propriocep-
injury had an increased dependence on joint sensation tive and neuroplastic changes appear to occur on an
and planning for performance of the task when com- individual basis, leading some to develop sensations of
pared with healthy patients, evidenced by increased joint instability. As researchers begin to understand how
presupplementary motor area, posterior secondary these changes arise, studies must shift toward clinical
somatosensory cortex and posterior inferior temporal recommendations to prevent instability and subsequent
gyrus activity. Similarly, a pair of studies by Baumeister disability among these patients. This goal becomes dif-
et al. (2008, 2011) found higher frontal cortex activation ficult when research cannot suggest any single factor that
among anterior cruciate ligament-deficient knees during equivocally changes following joint injury. Rather, it
proprioceptive tasks, suggesting higher reliance on may be more important to evaluate patients on an indi-
attentional control and working memory in this subset. vidual basis for mechanical insufficiencies, senso-
This is in line with clinical studies investigating the rimotor and fusimotor changes, and cortical alterations;
relationship between neurocognitive function and risk of and tailor treatment programs based on those specific
injury (Swanik et al., 2007). While this research has not changes.
been replicated at other joints, studies have investigated
changes in the motor cortex among unstable ankles. The
studies have found decreases in cortical excitability in Mechanical insufficiencies
patients with ankle instability (Pietrosimone et al., Mechanical insufficiencies could potentially be the most
2012), as well as altered tuning of excitability to laxity difficult to modify following injury, without the use of

7
Needle et al.

Fig. 1. Sensorimotor pathway from loading of capsuloligamentous structures (bottom left) to stabilization of the joint by the
musculotendinous unit (bottom right). Neuromechanical decoupling or dissociations between the structures that provide static and
dynamic joint stabilization and the nervous system (dashed lines) contribute to sensations of instability of the joint.

surgical procedures. At the ankle joint, Lamb et al. stiffness regulation, contributing toward improved out-
(2009) has suggested that casting for as long as 3 weeks comes among unstable joints. Benefits of joint mobili-
may provide the best long-term outcomes following joint zation include improved range of motion in the joint as
injury, although evidence suggests this may not be ideal well as improved balance, potentially through an
for returning to functional activities (Kerkhoffs et al., increase in afferent input toward the fusimotor system
2001b). While reducing mechanical laxity of the joint contributing to better proprioception (Hoch & McKeon,
following initial treatment may only be achievable 2011), although it is unclear if these effects last over a
through surgical intervention, it remains to be deter- prolonged treatment protocol (Hoch et al., 2014). Ross
mined how other conservative approaches may improve et al. (2007) has incorporated similar principles in the
the passive stiffness characteristics of the joint. While treatment of functional ankle instability, by utilizing sto-
both preparatory and reactive muscle contraction is able chastic resonance subthreshold vibratory stimulus that
to alter mechanical stiffness, it remains unclear if muscle would serve to enhance the transmission of mechanore-
tone would be modifiable following injury. ceptor activity and subsequently improve afferent feed-
back from the joint. This technique has demonstrated
effectiveness in addressing balance deficits among
Functional deficits patients with functional ankle instability (Ross &
In the case that mechanical insufficiencies appear within Guskiewicz, 2006; Ross et al., 2007). Similar improve-
normal limits, several interventions have been proposed ments have been observed using a massage intervention
to improve peripheral sensation and neuromuscular that could serve to enhance tactile feedback at the joint,
control at the joint. Among these techniques are modali- although proprioceptive improvements were only
ties such as joint mobilization (Hoch & McKeon, observed with visual feedback, making it unclear at
2011), stochastic resonance (Ross et al., 2007), massage which level of the nervous system this would be effective
(LeClaire & Wikstrom, 2012), as well as a variety of (LeClaire & Wikstrom, 2012).
training techniques (Fitzgerald et al., 2000; Swanik et al., While modalities demonstrate promise in correcting
2002). However, each one of these may have separate specific patient deficits, certain training techniques may
roles in improving neuromechanical coupling and serve to better correct long-term deficits. While strength

8
Neuromechanical coupling and stiffness regulation
training is traditionally included into rehabilitation pro- patients with joint instability, although these changes
tocols, their effectiveness in correcting proprioceptive appear to be variable. With growing evidence describing
deficits is limited (Smith et al., 2012). Strengthening neurophysiologic changes in response to therapeutic
exercises have been effective at improving stiffness at interventions and training techniques, clinicians should
the shoulder joint, but it is unclear if this carries over to better individualize treatment following joint injury.
the ankle and knee joints (Laudner et al., 2013). Rather, Joint instability is a multifaceted problem that may
current recommendations indicate balance and perturba- include alterations to joint laxity, peripheral sensation,
tion training, or plyometric training may better serve neuromuscular control and cortical alterations. However,
these populations. Balance and perturbation training are changes to any of these may be present in varied mag-
tied to improved detection of joint loading secondary to nitudes, and therefore patients should be assessed on an
altered Golgi tendon organ and muscle spindle sensitiv- individual basis. Several links have been observed that
ity (Fitzgerald et al., 2000), while plyometric training may predict the stiffness of a joint through measurement
would act to limit the inhibitory effect to the Golgi of nervous system parameters. Evidence is emerging and
tendon organ and subsequently improve proprioception suggesting that neuromechanical decoupling may occur
(Swanik et al., 2002; Chimera et al., 2004). While each following injury, where some patients exhibit mechani-
of these has been observed to improve symptoms among cal changes for which the nervous fails to adapt; while
patients with joint instability at the ankle, knee and shoul- others have a nervous system that has adapted while the
der; they would best serve among patients with evidence joint remains mechanically stable. Research must con-
of decreased proprioception and neuromuscular control at tinue to utilize direct neurophysiologic techniques in
the joint (Swanik et al., 2002). Only recently are cortical conjunction with measures of mechanical function to
changes following injury being discussed in the litera- truly understand this relationship, as well as incorporat-
ture (Kapreli & Athanasopoulos, 2006), but studies have ing these direct neurological measures with treatment
not yet evaluated whether the aforementioned tech- interventions to individually guide each patient.
niques would act to recalibrate the cortex to the joints Several factors remain unknown as research continues
mechanical properties or whether tasks requiring higher to investigate this highly variable pathology. While links
cognitive loads would be required to initiate changes in are consistently observed between joint stability and the
the CNS. PNS and CNS, it is unclear how these factors are coupled
in a normal population, limiting our understanding of
Perspective how these factors become decoupled following injury.
The brain remains a new frontier for joint instability
As muscle tone and joint stiffness remain misunderstood research, and its continued investigation could drasti-
and understudied in sports medicine research, it is impor- cally increase our knowledge of this pathology, as could
tant for clinicians to consider these factors in the context a group of previously injured subjects that have not
of injury in order to appropriately guide the diagnosis and developed instability (copers). Including these subjects
treatment of joint instability. The PNS and CNS both in future studies is crucial to understanding, preventing,
serve to alter fusimotor control surrounding the joint, and treating this phenomenon.
providing a further link between joint injury and the
nervous system (Burke, 1983). Morphological and Key words: joint instability, neuroplasticity, muscle
neuroplastic changes have both been reported among spindle, corticospinal excitability.

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