Proprioception and Neuromuscular Control




Chapter objectives





  • Define proprioception, kinesthesia, and other related aspects by using terminology consistent with the expanded classic definitions contained in this chapter.



  • Identify the different types and functions of mechanoreceptors in the upper and lower extremities.



  • List and describe clinical measurements of proprioception and kinesthesia in the upper and lower extremities.



  • Identify factors associated with diminished proprioception and the effects of injury, disuse, and aging on neuromuscular control and joint stability in the upper and lower extremities.



  • Design and implement progressive proprioception training programs that meet the functional demands of the patient and are appropriate for the patient’s level of skill and recovery when returning from an upper or lower extremity injury.



Human beings are unique in their capacity to propel themselves through their environment in an upright posture. This ability is achieved through a complex interaction of lower limb muscle activity coordinated by the central nervous system (CNS). To maintain balance and postural control we rely on sensory information from the periphery from our visual, vestibular, and somatosensory systems. The nervous system integrates this peripheral afferent information to maintain postural control during stance.


Control of locomotion, including walking or running, occurs through complex neural pathways in the spinal cord called central pattern generators or limb controllers. These motor programs for locomotion are automatic but are modulated by the CNS through feedback and feedforward mechanisms. The feedforward mechanism operates on the premise of initiating a motor response in anticipation of a load or activity that will disrupt the integrity of a joint and gauges the response from previous experiences. In contrast, the feedback system operates directly in response to a potentially destabilizing event by using a normal reference point to monitor the muscle activity necessary to restore homeostasis.


Both feedback and feedforward systems rely on processing of afferent information from the periphery at different levels of the CNS (spinal cord, brainstem and cerebellum, and cerebral cortex), with the end result being coordinated muscle activity during movement to maintain joint stability. The motor response varies depending on joint position, type of force, direction of force, and which higher center predominates in processing the information.


Segmental spinal reflexes involve the processing of afferent input between peripheral receptors in the muscle spindle and Golgi tendon organs at the musculotendinous junction with the efferent output of motor neurons in the ventral horn of the spinal cord. On the most basic level, monosynaptic reflexes produce an excitatory or inhibitory efferent motor response to the stimulus received from the periphery. Along with the physiologic properties of the muscle itself (length-tension curve), these peripheral receptors potentially assist in modulating muscle stiffness, with muscle tension varying according to the amount of afferent input.


The afferent information received in the cortical area of the brain from peripheral mechanoreceptors produces a voluntary motor response to potential disturbances in functional joint stability. The latency of the response is usually greater than 120 msec and sometimes longer, depending on the amount of information in the environment being processed. In addition to the response to an environmental stimulus, the potential exists for a theorized motor program operating under the assumption that the individual components of performing skilled movements, such as swinging a bat, that require sequential steps would be difficult to enact successfully without having a preprogrammed set of instructions to optimize efficiency, speed, and coordinated muscle activity.


The function of the cerebellum and brainstem is to integrate peripheral feedback from the environment with the motor commands from the cerebral cortex to enable humans to perform skilled and coordinated movement. The action of these neural centers allows the adjustments needed to carry out an intended motor skill with precision and efficiency.


A PubMed search of the terms proprioception and neuromuscular control was performed in October 2010. The results identified 305 references, the majority (260) of which have been published during the last decade. However, when the search is limited to higher levels of evidence, including randomized controlled trials (RCTs), systematic reviews, and metaanalysis studies, the actual number is 37 high-quality studies. In one such study, Riemann et al performed a literature review to identify sensorimotor assessment techniques, many of which are described throughout this chapter. Their conclusions indicate that the complex interactions and relationships among the individual components of the sensorimotor system make measuring and analyzing specific characteristics and functions difficult. Additionally, the specific assessment techniques used to measure a variable can influence the results obtained. Optimizing the application of sensorimotor research to clinical settings can best be accomplished through the use of common nomenclature to describe the underlying physiologic mechanisms and specific measurement techniques.




Definitions


Review of the orthopedic and musculoskeletal rehabilitation literature identifies many different versions of definitions for the terms associated with joint proprioception and neuromuscular control. In Goetz’s Textbook of Clinical Neurology , proprioception is defined as any postural, positional, or kinetic information provided to the CNS by sensory receptors in muscles, tendons, joints, or skin. Other texts define proprioception as “awareness of the position and movements of our limbs, fingers, and toes derived from receptors in the muscles, tendons and joints.” Sherrington’s classic definition of proprioception is “afferent information arising from the proprioceptive field,” and mechanoreceptors or proprioceptors were identified as being the source of the origination of this afferent information.


These original definitions of the term proprioception continue to be used today; however, a more advanced definition of the sensory functions that encompass human proprioceptive function is clearly needed. In a classic monograph titled Physiologie des Muskelsinnes , Goldsheider proposed that muscle sense be divided into four distinct and separate sensory functions. These functions were described as sensation of passive movements, sensation of active movements, sensation of position, and appreciation or sensation of heaviness and resistance. These original classifications or definitions have been expanded to decrease confusion. The sensation of passive movements is considered to be a product of sensations induced by external forces that result in a change in limb position with noncontracting muscles. The sensation of active movement (or kinesthesia as it is now better known) encompasses the appreciation of change in position of a limb with contracting muscles. Appreciation of the position of a limb in space has been termed stagnosia , and finally, in the presence of tension, appreciation of force applied during a voluntary contraction has been termed dynamaesthesia . Although these expanded definitions found in the classic literature provide additional information about human proprioception, adaptations of these classic definitions have been suggested and are used for the purposes of this chapter ( Box 24-1 ).



Box 24-1





  • Proprioception : Afferent information, including joint position sense, kinesthesia, and sensation of resistance




    • Joint position sense : The ability to recognize joint position in space



    • Kinesthesia : The ability to appreciate and recognize joint movement or motion



    • Sensation of resistance : The ability to appreciate and recognize force generated within a joint




  • Neuromuscular control : Appropriate efferent responses to afferent proprioceptive input



Definitions of Proprioception and Associated Functions in Humans




Afferent neurobiology of the joint


Early work on afferent proprioceptive function of the human joint included investigations into the role of joint- and muscle-based afferent receptors in human active and passive movement and detection of joint position. In 1898 Goldsheider proposed that the sensation of passive movements was solely the product of joint-based receptors. This view is still widely accepted today for passive movements.


The view up until the 1970s about the sensory feedback of active human movements was that when voluntary movement was initiated by the cerebral cortex, only low-level control was presented by the receptors in muscles and tendons. This sensory information from the muscles and tendons yielded information to the spinal cord and some subcortical extrapyramidal parts of the brain such as the cerebellum but played no contributing role in conscious sensation, which remained in the province of the joint receptors. In the early 1970s, however, important research by Goodwin et al and Eklund independently demonstrated the important role that muscular receptors play in contributing to sensations of active movement qualitatively. This section of the chapter focuses on both joint- and muscle-based afferent receptors to allow the clinician a more complete understanding of the sources of afferent information in the human body. This will later lead to a greater understanding of how specific treatment strategies can be used clinically to improve proprioceptive and neuromuscular function in both upper and lower extremity rehabilitation (Box 24-2) .



Box 24-2





  • Fatigue



  • Immobility



  • Injury



  • Surgery



  • Disuse



  • Ligamentous laxity



  • Aging



  • Arthritis



Factors Affecting Joint Proprioception


Classification of Afferent Mechanoreceptor


Mechanoreceptors are sensory neurons or peripheral afferents located within joint capsular tissues, ligaments, tendons, muscle, and skin. Deformation or stimulation of the tissues in which the mechanoreceptors lie produces gated release of sodium, which elicits an action potential. Four primary types of afferent mechanoreceptors have been classified and are commonly present in noncontractile capsular and ligamentous structures in human joints ( Table 24-1 ).



Table 24-1

Classification of Mechanoreceptors in the Human Body


































Type Location Threshold Response Active
I Superficial joint capsule
Limbs and vertebrae
Greater density proximal joints
Low Slow adapting Always
Static/dynamic
II Deeper layers of the joint capsule
Greater density distal joints
Low Rapidly adapting Dynamic only
III Superficial surface of the joint
Ligament
High Slowly adapting Dynamic end-range movements
Joint traction
IV Joint capsule, adjacent periosteum
Articular fat pads
Not active in normal circumstances


Type I articular receptors are traditionally globular or ovoid corpuscles with a very thin capsule. They are numerous in the capsular tissues of all the limb joints, as well as the apophyseal joints of the vertebral column. Wyke reported that the population of type I receptors appears to be more dense in proximal joints than in distal joints. Type I receptors are typically located in the superficial layers of the joint capsule.


Physiologically, type I receptors are low-threshold, slowly adapting mechanoreceptors. A proportion of type I receptors are always active in every joint position. The resting discharge of type I receptors allows the body to know where the limb is placed and receive constant input on limb position in virtually any joint position. The type I receptor is categorized as both a static and dynamic mechanoreceptor whose discharge pattern signals static joint position, changes in intraarticular pressure, and the direction, amplitude, and velocity of joint movements.


Type II mechanoreceptors are elongated, conical corpuscles with thick multilaminated connective tissue capsules. These type II corpuscles are present in the fibrous capsules of all joints but are reported to be present in greater number in distal joints than in proximal joints. Type II corpuscles are located in the deeper layers of the fibrous joint capsule, particularly at the border between the fibrous capsule and the subsynovial fibroadipose tissue and often alongside articular blood vessels. Type II mechanoreceptors are low-threshold, rapidly adapting receptors and are reported to be entirely inactive in immobile joints. These receptors become activated for very brief moments (1 second or less) at the onset of joint movement. The type II receptor is considered to be a dynamic mechanoreceptor whose brief, high-velocity discharges signal joint acceleration and deceleration during both active and passive joint movements.


The type I and type II mechanoreceptors described in the preceding paragraphs are the primary receptors located in the joint capsule. Type III receptors are primarily confined to the joint ligamentous structures. These type III receptors are found in both intrinsic and extrinsic ligamentous structures and are similar in nature to the Golgi tendon organs found in tendons, as discussed in later sections of this chapter. Type III receptors are found predominantly in the superficial surfaces of the joint ligaments, near their bony attachments. Research delineating the type III mechanoreceptor classifies this receptor as a high-threshold, slowly adapting structure, again similar in nature to the Golgi tendon organ. These type III receptors are completely inactive in immobile joints and become active or stimulated only toward the extreme ranges of joint motion where the ligamentous structures become taut. When considerable stress is generated in the joint ligaments, the type III receptor will become actively stimulated. Wyke also reported that type III receptors become activated with longitudinal traction on the limbs; the receptors remain activated centripetally at a high velocity only if extreme joint displacement or joint traction is maintained.


The final joint receptor to be discussed in this section is the type IV receptor. These receptors are noncorpuscular, unlike type I, II, and III receptors, and are represented by plexuses of small unmyelinated nerve fibers or free nerve endings. Type IV receptors are typically distributed throughout the fibrous joint capsule, adjacent periosteum, and articular fat pads. The type IV receptor represents the pain receptor system of articular tissues and is entirely inactive in normal circumstances. Marked mechanical deformation or chemical irritation such as exposure of the nerve endings to agents such as histamine, bradykinin, and other inflammatory exudates produced by damaged or necrosing tissues can stimulate activation of the type IV receptor.




Afferent mechanoreceptors in the lower extremity


The distribution of afferent articular nerves in synovial joints consists of medium and large myelinated fibers innervating the small end-organs or mechanoreceptors throughout joint tissue. These nerves represent approximately 55% of the total quantity of articular nerves, with the remaining 45% consisting of small unmyelinated fibers that transmit nociception or pain sensation.


Type I or Ruffini receptors located in the superficial layers of the joint capsule are low-threshold, slowly adapting mechanoreceptors. These receptors respond to changing mechanical stress and are always active because of the gradient pressure difference in the joint capsule. They undergo deformation with natural movement because of their location in the superficial portion of the joint capsule. In the limbs, type I receptors are found to be more densely distributed in the proximal joints of the hip and are not as prevalent in the distal joints of the ankle. Ruffini receptors have also been found in the meniscofemoral, cruciate, and collateral ligaments of the knee.


Type II or pacinian receptors are located in the deep layers of the joint capsule, the meniscofemoral, cruciate, and collateral ligaments of the knee. In addition, type II receptors are located in the intraarticular and extraarticular fat pads of all synovial joints. These pacinian receptors are more prevalent in distal joints such as the ankle and are less densely distributed in proximal joints such as the hip. They function as rapidly adapting, low-threshold receptors and respond to acceleration, deceleration, and passive joint movement but are silent during inactivity and joint movement at constant velocity.


Type III or Golgi tendon organ–like endings are found predominantly in intraarticular and extraarticular joint ligaments, including the collateral ligaments and cruciate ligaments in the knee. These receptors have also been identified in the menisci of the knee. Type III Golgi tendon organ–like endings are structurally identical to the Golgi tendon organ receptors and function as slowly adapting, high-threshold receptors with a function similar to that of the Golgi tendon organs found in tendons.


Type IV free nerve endings function as the pain receptor or nociception system in synovial joints. These type IV receptor nerve endings are found throughout the joints of the extremities in the fibrous capsule and adjacent periosteum and in the articular fat pads and are the most prevalent receptor type in the knee menisci. They are completely inactive in normal situations and are activated by marked mechanical deformation or chemical stimuli resulting from an inflammatory response.




Afferent joint receptors in the upper extremity


The classification system mentioned earlier for the four primary types of mechanoreceptors found in human noncontractile capsular and ligamentous tissues described by Wyke provides generalized information about the location of these receptors in the human body. Vangsness et al studied the neural histology of the human shoulder joint, including the glenohumeral ligaments, labrum, and subacromial bursa. They found two types of mechanoreceptors and free nerve endings in the glenohumeral joint capsular ligaments. Two types of slowly adapting Ruffini end-organs and rapidly adapting pacinian corpuscles were identified in the superior, middle, and inferior portions of the glenohumeral ligaments. The most common mechanoreceptor was the classic Ruffini end-organ in the capsular ligaments of the glenohumeral joint. Pacinian corpuscles were less abundant overall; however, Kikuchi and Shimoda reported that type II pacinian corpuscles were more commonly found in the capsular ligaments of the human glenohumeral joint than in the human knee. Analysis of the coracoclavicular and acromioclavicular ligaments showed equal distribution of type I and II mechanoreceptors. Morisawa et al identified type I, II, III, and IV mechanoreceptors in human coracoacromial ligaments. These reviews show how the capsular ligaments of the glenohumeral joint aid in the provision of afferent proprioceptive input by their inherent distribution of both type I Ruffini mechanoreceptors and the more rapidly adapting pacinian receptors. A rapidly adapting receptor such as the pacinian receptor can identify changes in tension in the joint capsular ligaments but quickly decreases its input once the tension becomes constant. In this way the type II receptor has the ability to monitor acceleration and deceleration of the tension on a ligament.


Several authors have also studied the labrum and subacromial bursa. Vangsness et al reported that no evidence of mechanoreceptors was found in the glenoid labrum; however, free nerve endings were noted in the fibrocartilage tissue in the peripheral half. The subacromial bursa was found to have diffuse, yet copious free nerve endings, with no evidence of larger, more complex mechanoreceptors. Ide et al also studied the subacromial bursa, taken from three cadavers, and found a copious supply of free nerve endings, most of which were present on the roof side of the subacromial arch, which is exposed to impingement-type stress. Unlike the study by Vangsness et al, Ide et al did find evidence of both Ruffini and pacinian mechanoreceptors in the subacromial bursa. Their findings suggest that the subacromial bursa receives both nociceptive and proprioceptive stimuli and may play a role in regulation of shoulder movement. Further research into the exact distribution of these important structures in the human shoulder is indicated to give clinicians further information and enhance the understanding of proprioceptive function of the shoulder.




Afferent receptors of contractile structures in the upper extremity


In addition to the afferent structures found in noncontractile tissues of the human shoulder (joint capsule, subacromial bursa, and intrinsic and extrinsic ligaments), significant contributions to the regulation of human movement and proprioceptive feedback are obtained from receptors located in contractile structures.


Two of the primary mechanisms for afferent feedback from the muscle-tendon unit are the muscle spindle and the Golgi tendon organ. Research classifying muscle spindles has traditionally grouped intrafusal muscle fibers into two groups based on the type of afferent projections. These two groups consist of nuclear bag and nuclear chain fibers. Nuclear chain fibers project from large afferent axons. Nuclear bag fibers are innervated by γ 1 (dynamic) motor neurons and are more sensitive to the rate of change in muscle length, such as that occurring during rapid stretch of a muscle during an eccentric contraction or passive stretch. Intrafusal nuclear chain fibers are innervated by γ 2 (static) motor neurons and are more sensitive to static muscle length. The combination of nuclear chain and nuclear bag fibers allows afferent communication from the muscle-tendon unit to remain sensitive over a wide range of joint motion during both reflex and voluntary activation ( Table 24-2 ).



Table 24-2

Characteristics of the Muscle Spindle



















Type Fiber Length Motor Axon Type Function
Nuclear bag 7-8 mm long Medium size Stimulation of larger motor fibers increases tension in the bag.
Nuclear chain 4-5 mm long Small Stimulation of smaller motor fibers reduces tension on the bag.


Muscle spindles provide much of the primary information for motor learning, including muscle length and joint position. Upper levels of the CNS can bias the sensitivity of muscle spindle input and sampling. Muscle spindles do not occur in similar density in all muscles in the human body. Spindle density is probably related to muscle function, with greater densities of muscle spindles being reported in muscles that initiate and control fine movements or maintain posture. Muscles that cross the front of the shoulder, such as the pectoralis major and biceps, have a very high number of muscle spindles per unit of muscle weight. Muscles with attachment to the coracoid, such as the biceps, pectoralis minor, and coracobrachialis, also have high spindle densities. Lower spindle densities have been reported for the rotator cuff muscle-tendon units, with the subscapularis and infraspinatus having greater densities than the supraspinatus and teres minor. This lower rotator cuff spindle density probably suggests synergistic mechanoreceptor activation with the scapulothoracic musculature during movement of the glenohumeral joint. This coupled or shared mechanoreceptor activation is an example of the kinetic link or proximal-to-distal sequencing that occurs with predictable or programmed movement patterns in the human body. This kinetic link activation concept is further demonstrated by the deltoid/rotator cuff force couple and other important biomechanical features of the human glenohumeral joint and is discussed later in this chapter.


The second major aspect of musculotendinous afferent activity is the Golgi tendon organ. These tendinous mechanoreceptors are present in the human shoulder and respond to the tension generated by muscular contraction. Activation of the Golgi tendon organs relays afferent feedback about muscle tension and joint position. Additionally, as a protective mechanism, activation of the tension-sensitive Golgi tendon organ produces a protective mechanism that causes relaxation of the agonist muscle that is undergoing tension, with simultaneous stimulation of antagonistic musculature.




Clincal assessment of proprioception in the lower extremity


The two primary tests measuring proprioception and kinesthetic awareness in the knee joint are the threshold to detection of passive motion (TTDPM) for movement sense and reproduction of angular position for joint position sense. The TTDPM test has been more standardized in the literature. The method described by Barrack et al and Skinner et al involves placing the subject in a seated position with the leg hanging freely over the seat and suspended by a motorized pulley system in 90° of flexion ( Fig. 24-1 ). Tactile, visual, and auditory cues are eliminated with the use of custom-fitted Jobst air splints and wearing of a blindfold. Initiation of movement into either flexion or extension proceeds at a rate of angular deflection of 0.5°/sec. When subjects initially detect movement to occur, they engage a control switch to indicate that the test leg has been moved.




Figure 24-1


Proprioceptive testing device. a, Rotational transducer; b, motor; c, moving arm; d, stationary arm; e, control panel; f, digital microprocessor; g, handheld disengage switch; h, pneumatic compression boot; and i, pneumatic compression device. The threshold for detecting passive movement is assessed by measuring angular displacement until the subject senses motion in the knee.

(From Lephart, S.M., Kocher, M.S., Fu, F.H., et al. [1992]: Proprioception following anterior cruciate ligament reconstruction. J. Sport Rehabil., 1:188–196.)


Testing for joint position sense involves passive movement of the extremity to a specified angle by the clinician, holding of the position for several seconds, and passive return of the extremity to the starting reference position. The patient is then asked to actively move the extremity to the specified angle without visual input. The difference between the actual and replicated angle can be calculated as either an absolute or a real angular error. With absolute error, only the magnitude of the error is determined, and whether the subject overestimates or underestimates knee position is not considered. Real error calculations, however, consider both the magnitude and direction of the error and can be used to determine whether a subject overestimates or underestimates the reference angle. Barrack et al demonstrated through studies on proprioception that extremities with no evidence of pathologic conditions have a high degree of symmetry in joint position sense.


Because essentially no standard protocols have been established for measuring joint position sense or for performing joint replication tests, many variations exist, including apparatuses used for angular measurement, starting reference angle, active or passive reproduction, and open chain (seated) versus closed chain (standing). Lattanzio et al and Marks and Quinney used closed chain weight-bearing joint replications and reported a high degree of accuracy. Their results may be due to the fact that proprioceptive input is greater in the standing weight-bearing position, in which multiple joints are being loaded.


Single-limb postural stability tests have also been used for measuring the amount of sway in individuals with complaints of ankle instability. Tropp et al developed such a test for measuring ankle instability that has been used with variations throughout the years. Individuals stand for 60 seconds on a force platform, and the instantaneous center of pressure is recorded along a graph; the magnitude of sway is compared with that on the uninvolved side.


Single-leg hop tests are often used for assessing stability in patients with pathologic knee or ankle conditions. Variations of the test include single-leg or triple-leg hop tests for distance, the crossover hop test, and the timed hop test. The relationship of hop tests to functional parameters such as instability, proprioception, and leg strength has been inconclusive in studies to date.




Assessment of proprioception and neuromuscular control in the upper extremity with specific reference to the human shoulder


Determination of which patients require particular emphasis in rehabilitation on restoring proprioception and neuromuscular control requires the use of clinical assessment techniques. In this section, techniques used in research investigations, as well as in clinical applications, to allow the clinician to perform a detailed evaluation are reviewed.


Primary Measures of Proprioception and Neuromuscular Control for the Shoulder


Evaluation of proprioception and neuromuscular control in the human shoulder encompasses both afferent and efferent neural function, as well as the resulting muscular activation patterns. Proprioception for the purposes of this and many other articles, texts, and chapters consists of three major submodalities: kinesthesia, joint position sense, and sensation of resistance. Separate techniques can be used to assess each of these aspects of proprioception.


Measurement of Kinesthesia


Assessment of glenohumeral joint kinesthesia has been performed with a test called the TTDPM. This test assesses the subject’s or patient’s ability to detect a passive movement occurring typically at very slow angular velocities. Elaborate testing devices have been used in several studies that have reported on the TTDPM, such as an instrumented (motorized) shoulder wheel and other devices such as the one used by the University of Pittsburgh, whose characteristics are described next ( Fig. 24-2 ). Extensive research using the TTDPM test has resulted in the selection and recommendation of slow angular velocities (0.5° to 2°/sec) to enhance the reliability of data acquisition. In addition to the device used, blindfolds, earphones, and a pneumatic cuff are recommended to eliminate cues from the visual, auditory, and tactile realm. This ensures that only joint kinesthesia is being assessed and not simply visual or auditory responses to perceived movement.




Figure 24-2


Upper extremity proprioceptive testing device.

(From Pollack, R. [2000]: Role of shoulder stabilization relative to restoration of neuromuscular control and joint kinematics. In Lephart, S.M., and Fu, F.H. [eds.]: Proprioception and Neuromuscular Control. Champaign, IL: Human Kinetics.)


Physiologically, the TTDPM test is designed to selectively stimulate the Ruffini or Golgi-type mechanoreceptors in the articular structures being tested. Testing is typically performed for internal and external rotation of the glenohumeral joint in varying positions of elevation in the scapular and coronal planes. Testing in the literature has been done at the midrange and end-range positions of glenohumeral rotation. As stated earlier, TTDPM in the human shoulder was measured by Blaiser et al, and passive motion was found to be enhanced (smaller amount of movement before detection) at or near the end range of external rotation versus the midrange of external rotation or internal rotation.


Normative data on 40 healthy college-aged individuals undergoing the TTDPM test were reported by Warner et al from both neutral rotational starting positions and 30° of humeral rotation with 90° of glenohumeral joint abduction. They found an average of 1.5° to 2.2° for all testing conditions, with no significant difference measured between the dominant or preferred hand relative to the nondominant extremity. Allegrucci et al measured shoulder kinesthesia in healthy athletes who performed unilateral upper extremity sports, such as baseball, tennis, or volleyball. The TTDPM test was performed with the shoulder in 90° of abduction and both 0° and 75° of external rotation and compared bilaterally. The results showed that the athletes had greater difficulty detecting passive motion in the dominant extremity than in the nondominant extremity. Consistent with earlier research, Allegrucci et al measured greater sensitivity to passive movement with the shoulder in 75° of external rotation bilaterally than with the shoulder in a more neutral condition. The findings in this study suggest that athletes in unilaterally dominant upper extremity sports may have a proprioceptive deficit in the dominant arm that may interfere with optimal afferent feedback regarding joint position. This finding provides a rationale for proprioceptive upper extremity training in athletes from this population.


Measurement of Joint Position Sense


Joint position sense is the ability of the subject to appreciate where the extremity is oriented in space. Testing procedures to assess joint position sense are called joint angular replication tests . These tests typically place the extremity in a particular position to allow the subject to appreciate the spatial orientation of the extremity. After this period of joint positioning, the subject’s extremity is returned to a starting position. The subject then reapproximates the position initially selected as closely as possible, without any visual, auditory, or tactile cues. Researchers have used both active and passive angular replication tests for assessment of the glenohumeral joint, and various apparatuses have been used to facilitate the accuracy of joint angular replication testing. Voight et al used an isokinetic dynamometer with 90° of abduction and elbow flexion and standard isokinetic stabilization to perform active angular joint replication testing via a fatigue paradigm. They also used the passive mode of the isokinetic dynamometer set at 2°/sec to perform passive joint angular replication testing. Various authors have used complex three-dimensional spatial tracking devices and multiple positions of active joint angular replication testing to quantify arm position.


In the most clinically applicable research study on active joint angular reproduction, Davies and Hoffman tested subjects in a seated position with an electronic digital inclinometer (EDI). *


* Available from Cybex, Inc., Medway, MA.

Reference angles were chosen in several ranges and verified with the EDI; the patient then attempted to replicate the angular position, with the EDI being used to verify the position of the extremity. Angles chosen were greater than 90° and less than 90° of flexion and abduction, external rotation greater than 45° and less than 45°, and internal rotation greater than 45° and less than 45°. Normative data developed by Davies and Hoffman for 100 male subjects without pathologic shoulder conditions showed the average of the seven measurements to be 2.7°. This represents the average difference between the seven reference angles and the actual matched angles by the subjects over the seven measurements.


Regardless of the testing methodology, active joint angular position replication tests primarily involve stimulation of both joint and muscle receptors and provide a thorough assessment of the afferent pathways of the human shoulder.


Assessment of Neuromuscular Control of the Shoulder


Several methods have been used by clinicians and researchers to assess neuromuscular control of the shoulder. Widespread use of electromyographic (EMG) studies to measure muscular activity during shoulder rehabilitative exercise, functional movement patterns such as the throwing motion and tennis serve and groundstrokes, and abnormal muscular activity patterns during planar motions and functional activities is reported in the scientific and clinical literature. Most of these studies comparing muscular activity expressed the contribution or activity of the muscle in terms of the amount of muscle activity relative to the maximal activity assessed via a maximal isolated manual muscle test (MMT). This is commonly referred to as %MMT or %MVC (maximum voluntary contraction) and allows comparison and expression of the relative activity of human muscle activity during activities of daily living (ADLs) and sport-specific movement patterns.


Muscular Strength Testing


Another important aspect of assessing neuromuscular control is measurement of muscular strength. Methods such as the MMT and the use of handheld dynamometers and isokinetic apparatuses have been used extensively for the documentation of both upper and lower extremity strength. Further discussion is beyond the scope of this chapter; however, the reader is referred to Chapter 25 .


Closed Kinetic Chain Upper Extremity Testing


Closed kinetic chain (CKC) upper extremity tests are also used to assess neuromuscular control of the shoulder. Although widespread use of CKC training techniques has been reported in the physical medicine and rehabilitation literature, currently existing evaluation methods to properly assess CKC function of the upper extremity are limited.


One of the “gold standards” in physical education for gross assessment of upper extremity strength has been the push-up. This test has been used to generate sport-specific normative data in normal populations, but it is not typically considered appropriate for use in patients with shoulder dysfunction. The positional demands placed on the anterior capsule and the increased joint loading limit the effectiveness of this test in musculoskeletal rehabilitation. Modification of the push-up has been reported, and the modified push-up has been used clinically as an acceptable alternative to assess CKC function in the upper extremities.


Davies developed the CKC upper extremity stability test in an attempt to provide a means of assessing the functional ability of the upper extremity more accurately. The test is initiated in the starting position of a standard push-up for males and modified (off the knees) push-up for females. Two strips of tape are placed parallel to each other, 3 feet apart on the floor. The subject or patient then moves both hands back and forth and touches each line alternatively as many times as possible in 15 seconds. Each touch of the line is counted and tallied to generate the CKC upper extremity stability test score. Normative results have been established, with males averaging 18.5 touches and females averaging 20.5 touches in 15 seconds. The CKC upper extremity stability test has been subjected to a test-retest reliability measure, with an intraclass correlation coefficient of 0.927 being generated, which is indicative of high clinical reliability between sessions with this examination method.




Effects of aging, instability, and injury on lower extremity proprioception


The effects of age and injury have been correlated with diminished proprioceptive sense. Studies have shown decreased proprioceptive acuity in older adults with testing, and it has been suggested that this decreased capacity for movement sense results in a higher incidence of falling and joint degeneration in this population. However, it has also been found that with regular physical activity, the age-related decline in proprioception can be lessened through dampening of the effect of disuse atrophy on the neuromuscular system. In addition to age-related deficits, injuries to the lower extremity joints sustained as a result of repetitive microtrauma or a single traumatic event can create an environment in which degenerative changes occur in the joint along with disruption of the neuromuscular response. The presence of pain and inflammation in a joint produces an inhibitory effect on neuromuscular activation with decreased afferent mechanoreceptor signals. Hurley and Newham and Sharma and Pai demonstrated arthrogenous muscle inhibition in patients with degenerative arthritis. The inability to achieve full voluntary muscle contraction may lead to continued overload on the joints through the loss of dynamic control and attenuation of force.


Loss of capsuloligamentous stability has been shown to cause proprioceptive deficits as a result of inadequate activation of mechanoreceptors leading to delayed muscle reaction latencies. Barrack et al found decreased proprioception in a group of ballet dancers and attributed this clinical loss of proprioception to the hyperlaxity found in the ligamentous restraints in this population. It is theorized that without adequate tension in the capsuloligamentous restraints, insufficient stimulation of the mechanoreceptors used for proprioception occurs and results in decreased motor control. A study by Garn and Newton also showed that individuals suffering from chronic ankle instability have diminished proprioception with a low threshold for passive plantar flexion. A similar study by Lentell et al tested subjects with chronic lateral ankle instability who demonstrated decreased passive movement sense, with the uninvolved ankle being used as the control. Subjects in this study demonstrated no evidence of everter strength contributing to the functional instability. Therefore, the chronic instability was due to loss of mechanoreceptor function from ligamentous laxity and the resultant delayed muscular reflex. Lephart and Fu and Nawoczenski et al confirmed this decreased muscular stabilization in a study involving subjects with ankle instability. The results of their studies supported this loss of motor control, with a delay in onset latency in the peroneal muscles when subjected to sudden inversion stress.


Effects of Knee Injury on Proprioception


Degenerative arthritis in the knee causes pain, inflammation, and muscular inhibition, which results in decreased functional performance during gait and weight-bearing activities. When combined with pain and altered muscle activity, the inadequate ligamentous tension resulting from narrowing of the joint space contributes to the interruption in afferent signals for proprioception and neuromuscular control. The goal of joint replacement surgery is to restore function through resurfacing joints, retensioning soft tissue structures, and ultimately restoring dynamic stability. Research performed by Warren et al and Barrett et al suggested that joint replacement surgery may actually improve joint position sense, with subjects showing significant improvement in position sense 6 months postoperatively. Furthermore, correlations have been made between improved functional outcomes and gait parameters and proprioceptive scores, thus suggesting a relationship between restoration of proprioception and improved functional outcomes.


The results of studies to date on the selection of joint prostheses and the effects of retaining versus sacrificing the posterior cruciate ligament (PCL) on proprioception have been inconclusive. However, it has been theorized that by restoring joint integrity and retensioning soft tissue structures, retention of the PCL will enhance dynamic joint stability through preservation of the neural reflexive pathway.


Studies in the literature have consistently demonstrated decreases in proprioceptive sense and altered muscle patterns after rupture of the anterior cruciate ligament (ACL). Loss of stability of the ACL causes alterations in muscle activity and reflex patterns, primarily the ACL-hamstring reflex. Measuring the ACL-hamstring reflex in patients with ACL rupture, Beard et al showed significant reflex latency delays that were directly correlated with functional instability. Using EMG studies, Limbird et al showed variations in muscle activation patterns with increased hamstring activation and concomitant decreased quadriceps activity with joint loading during gait. Andriacchi and Birac had similar findings in patients performing normal activities of ambulation, stair climbing, and jogging. With the loss of stability and neural sensory input, many individuals experience functional disability in performance of normal ADLs.




Effects of pathologic shoulder conditions on proprioception and neuromuscular control


In this section the normal afferent neurobiology of the joint and periarticular structures is reviewed, and examples of how proprioception and neuromuscular control are affected in pathologic conditions of the shoulder are provided. Examples of both glenohumeral joint instability and pathologic rotator cuff conditions are presented, as well as dysfunction of the scapulothoracic joint.


Effects of Glenohumeral Joint Instability on Proprioception


Several studies have addressed the influence of glenohumeral joint instability on proprioception. One of the most common clinical maladies seen by clinicians is anterior glenohumeral joint instability. Speer et al studied the effects of a simulated Bankart lesion in cadavers. Coupled anterior/posterior translations were assessed in the presence of sequentially applied loads of 50 N in the anterior, posterior, superior, and inferior directions. The effects of a simulated Bankart lesion were small increases (maximum of 3.4 mm) in anterior and inferior translation of the humeral head relative to the glenoid in all positions of elevation and in posterior translation at 90° of elevation only. The relevance of this article to the current discussion on proprioception is that Speer et al concluded that detachment of the anterior inferior labrum from the glenoid (Bankart lesion) alone does not create large enough increases in humeral head translation to allow anterior glenohumeral joint dislocation. They indicated that permanent stretching or elongation of the inferior glenohumeral ligament may also occur and is necessary to produce full dislocation of the glenohumeral joint. This elongation or permanent stretching of the ligamentous structures may lead to alterations in the intrinsic tensile relationships of the glenohumeral joint capsule and capsular ligaments. The authors concluded that capsular elongation may be responsible for the high incidence of anterior reconstructions that fail to address anterior glenohumeral joint instability and do not fully restore normal capsular tension in the anterior structures.


Blaiser et al examined the proprioceptive ability of subjects without known pathologic shoulder conditions and compared them with individuals with clinically determined generalized joint laxity. Individuals with greater glenohumeral joint laxity were found to have less sensitive proprioception than were those with less glenohumeral joint laxity. The authors found enhanced proprioception at or near the end range of external rotation, a position at which the anterior capsular structures have greater internal tension. They concluded that decreased joint angular reposition sense is one characteristic in individuals with increased glenohumeral joint laxity.


Smith and Brunolli examined kinesthesia after glenohumeral joint dislocation in 8 subjects and compared their inherent joint position sense with that in 10 normal subjects by using an instrumented modification of a shoulder wheel. Their results indicated a significant decrease in joint awareness in the involved shoulders after shoulder dislocation in comparison to all uninvolved shoulders tested in the study.


Barden et al tested subjects with multidirectional instability (MDI) for joint angular replication in multiple positions, including overhead reaching and abduction with external rotation. Subjects with MDI exhibited significantly greater hand position error than did control subjects without instability. This study showed significant proprioceptive deficits in patient with MDI.


Lephart et al studied glenohumeral joint proprioception in 90 subjects in three experimental groups. One group consisted of 40 normal college-aged subjects, another group consisted of 30 patients with anterior instability, and the third group included 20 subjects who underwent surgical reconstruction for shoulder instability. No significant difference was found between extremities (dominant versus nondominant) in the normal subjects’ proprioceptive ability; however, subjects with anterior instability had significant differences between the normal and unstable shoulders. Finally, Lephart et al found no significant difference in the operated extremity versus the uninjured extremity after reconstructive surgery. This study was performed at least 6 months after subjects underwent open or arthroscopic repair for chronic, recurrent shoulder anterior instability. The authors concluded that these results provide evidence, consistent with the studies mentioned earlier, for partial deafferentation leading to proprioceptive deficits when the capsuloligamentous structures are damaged. Reconstructive surgery in this experiment appeared to restore normal joint proprioception 6 months or more after the surgical procedure.


Safran et al used a testing device to study 21 collegiate baseball pitchers to determine whether bilateral differences in joint angular replication (JAR) and kinesthesia were present between extremities. They found that JAR was more accurate in the nondominant extremity when moving from a position of 75° of external rotation into internal rotation. Measurements were taken in 90° of abduction. No difference in proprioceptive ability was observed when moving from 75° of external rotation to end range of motion (ROM) between the extremities. Six collegiate pitchers with reports of shoulder pain were tested by Safran et al and found to have a kinesthetic deficit in the injured dominant shoulder versus the nondominant shoulder when moving from neutral rotation into internal rotation. These results show JAR to be bilaterally symmetric from 75° of external rotation to end ROM between extremities in healthy skilled baseball pitchers despite increases in laxity and training effects. Additionally, despite a small sample size, Safran et al did show very importantly that pitchers with a recent report of injury involving the shoulder do have kinesthetic deficits in the injured arm that may affect further performance.


The finding of reduced proprioception in unstable shoulders has prompted researchers to examine the effect of surgical stabilization procedures on restoring proprioception following surgery. Rokito et al studied the effects of two open surgical procedures for recurrent unidirectional anterior instability. Thirty subjects underwent an open inferior capsular shift procedure involving an approach that detached the subscapularis from the lesser tuberosity to gain exposure. Twenty-five underwent anterior capsulolabral reconstruction with a transverse splitting approach to the subscapularis for exposure. At 6 months postoperatively patients underwent proprioceptive testing, and the group with transverse splitting of the subscapularis had no deficits in proprioception and mean strength with respect to the contralateral uninvolved extremity. However, the group that underwent open capsular shift with subscapularis detachment had significant deficits in proprioception and mean strength that did not return to full functional values until 1 year postoperatively. This study shows that deficits in proprioception and strength following an open approach with detachment of the subscapularis require up to 1 year for return to the same functional level as the contralateral baseline extremity.


Effects of Glenohumeral Joint Instability on Neuromuscular Control


Lephart and Fu defined neuromuscular control as the unconscious efferent response to an afferent signal concerning dynamic joint stability. Several studies highlighting changes in neuromuscular control in subjects with glenohumeral joint instability have been published. Glousman et al, using an indwelling EMG electrode, studied the muscular activity patterns of normal healthy baseball pitchers and compared them with throwers with anterior glenohumeral joint instability. The results of the study showed marked increases in muscular activation of the supraspinatus and biceps muscle, as well as selective increases in the infraspinatus muscle during the early cocking and follow-through phases. Also of interest was the finding of decreased muscular activation of the pectoralis major, latissimus dorsi, subscapularis, and serratus anterior muscles in the throwing athletes with anterior glenohumeral joint instability. This study showed neuromuscular compensations in the group with glenohumeral joint instability, as evidenced by increased activation of the primary dynamic stabilizers. Inhibition of the serratus anterior in the group with anterior instability may decrease scapular stability and further jeopardize joint congruity through improper scapulothoracic muscle sequencing.


McMahon and et al tested normal shoulders and those with anterior instability and monitored them via indwelling EMG muscular activation patterns. Planar motions of flexion, abduction, and scapular-plane elevation (scaption) were studied in 30° increments. Significant decreases in serratus anterior muscle activity were measured in all three planar motions in the group of subjects with anterior glenohumeral joint instability. None of the other muscles—rotator cuff, deltoid, or scapular—showed a significant difference in testing during standard planar movement patterns. This study clearly shows the importance of the scapulothoracic musculature and dynamic stabilization during both aggressive overhead and common ADL-type movement patterns.


Finally, Kronberg et al used intramuscular electrodes to compare shoulder muscle activity in patients with generalized joint laxity and normal control subjects. Increased subscapularis muscular activity was measured during internal rotation in the subjects with increased glenohumeral joint laxity, as well as increased middle and anterior deltoid activity during abduction and flexion. These studies clearly show the increased demand required by the dynamic stabilizers in subjects with joint laxity and glenohumeral joint instability. Application of the resistive exercise progressions and use of the kinetic chain exercise series listed later in this chapter have these research-based rationales and can directly enhance neuromuscular control of the shoulder complex.


Effects of Rotator Cuff Dysfunction on Neuromuscular Control in the Shoulder


Research similar to that discussed in the preceding section in which muscular activation patterns in patients with rotator cuff impingement were measured has been published. Ludewig and Cook studied 52 male construction workers, 26 of whom had unilateral shoulder impingement and 26 had no symptoms of impingement or other pathologic shoulder condition. Similar to subjects in the previously discussed research studies on glenohumeral joint instability, those with unilateral impingement demonstrated a decrease in serratus anterior muscle activation during active elevation of the arm in comparison to normal, uninjured subjects. Additionally, increases in upper and lower trapezius muscle activity were found in the subjects with unilateral impingement. This altered neuromuscular control mechanism also resulted in abnormal scapular posturing consisting of decreased upward rotation with elevation, increased anterior tipping, and increased medial rotation. These scapular modifications are thought to be contributing factors to rotator cuff impingement and demonstrate the importance of optimal and coordinated muscular control of the scapulothoracic and glenohumeral joints.

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Apr 13, 2019 | Posted by in PHYSICAL MEDICINE & REHABILITATION | Comments Off on Proprioception and Neuromuscular Control
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