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.⁴ 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.”⁵ 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.⁶

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, Goldsheider⁷ 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.⁸ 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).

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.⁸ 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.^7,8

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.⁸ In the early 1970s, however, important research by Goodwin et al⁹ and Eklund¹⁰ 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).

Classification of Afferent Mechanoreceptor

Mechanoreceptors are sensory neurons or peripheral afferents located within joint capsular tissues, ligaments, tendons, muscle, and skin.^11,12 Deformation or stimulation of the tissues in which the mechanoreceptors lie produces gated release of sodium, which elicits an action potential.¹³ 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 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. Wyke¹² 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.¹² 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 mechanoreceptor¹² 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.¹ 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.¹² 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 structures¹² 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. Wyke¹⁴ 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.^12,14,15

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.¹²

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.¹² Ruffini receptors have also been found in the meniscofemoral, cruciate, and collateral ligaments of the knee.²

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.²

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.¹² These receptors have also been identified in the menisci of the knee.² 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.²

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^12,14 provides generalized information about the location of these receptors in the human body. Vangsness et al¹⁶ 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, Kikuchi¹⁷ and Shimoda¹⁸ 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 al¹³ 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.¹⁶ 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 al¹⁶ 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 al¹⁹ 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,¹⁶ Ide et al¹⁹ 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.^15,20 Research classifying muscle spindles has traditionally grouped intrafusal muscle fibers into two groups based on the type of afferent projections.^20,21 These two groups consist of nuclear bag and nuclear chain fibers. Nuclear chain fibers project from large afferent axons.^20,21 Nuclear bag fibers are innervated by γ₁ (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.²⁰ Intrafusal nuclear chain fibers are innervated by γ₂ (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

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.²⁰ 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.²² 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.²² This lower rotator cuff spindle density probably suggests synergistic mechanoreceptor activation with the scapulothoracic musculature during movement of the glenohumeral joint.^20,23 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.²⁴ This kinetic link activation concept is further demonstrated by the deltoid/rotator cuff force couple²³ 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.^15,20 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.^2,25,26 The method described by Barrack et al²⁷ and Skinner et al²⁸ 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.²⁸

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.²⁹ Barrack et al³⁰ 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).³¹ Lattanzio et al²⁵ and Marks and Quinney³² 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 al³³ 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.¹⁵ Proprioception for the purposes of this and many other articles, texts, and chapters^2,15,34 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.^2,15,35 Elaborate testing devices have been used in several studies that have reported on the TTDPM, such as an instrumented (motorized) shoulder wheel³⁵ and other devices such as the one used by the University of Pittsburgh, whose characteristics are described next (Fig. 24-2).² Extensive research^2,15,36 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.^2,15,36 As stated earlier, TTDPM in the human shoulder was measured by Blaiser et al,³⁴ 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 al³⁷ 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.³⁸ Allegrucci et al³⁹ 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,³⁴ Allegrucci et al³⁹ 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.³⁹ 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^{2,15,36,40,41} and passive⁴¹ 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 al⁴¹ 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^2,42,43 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 Hoffman⁴⁰ tested subjects in a seated position with an electronic digital inclinometer (EDI).* 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°.⁴⁰ 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.^2,15

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,^44-47 functional movement patterns such as the throwing motion⁴⁸ and tennis serve and groundstrokes,⁴⁹ and abnormal muscular activity patterns during planar motions^50-52 and functional activities⁵³ 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.^48,49

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

The effects of age and injury have been correlated with diminished proprioceptive sense.⁶² Studies^63,64 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.² 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.⁶⁵ Hurley and Newham⁶⁶ and Sharma and Pai⁶⁷ 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 al⁶⁸ 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 Newton⁶⁹ 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 al⁷⁰ 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 Fu² and Nawoczenski et al⁷¹ 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 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 fatigue on lower extremity proprioception

Muscle fatigue reduces the force-generating capacity of the neuromuscular system, which essentially leads to increased laxity in the knee joint.⁸⁴ Skinner et al²⁸ found an increase in laxity of the ACL measured with a KT1000* arthrometer after a fatigue protocol. Similarly, Weisman et al⁸⁵ found increased laxity in the medial collateral ligament in athletes at a university after participation in various sporting activities. Furthermore, studies in the literature^2,28,86,87 have shown a decrease in the sensitivity of muscle receptors under fatigue conditions. The consequences of decreased proprioceptive sense from fatigue can be deleterious because of the possibility of sustaining injuries under these conditions when higher-level activities are performed. Skinner et al²⁸ studied the effects of fatigue on joint position sense and knee angle reproduction in a group of healthy, highly trained male recruits in the Special Forces division of the Navy. Subjects underwent an interval running program followed by isokinetic measurement of knee extension and flexion. Fatigue was determined by the percent decrement in work output measured from pretraining to posttraining conditions on an isokinetic device. The authors concluded that after fatigue ensues, values on angular replication tests are significantly decreased, but no significant changes were noted in the threshold of movement sense. They determined that loss of muscle receptor efficiency as a result of fatigue played a key role in angular replication errors. The authors concluded that the dual role of afferent input by the receptors in the contractile and noncontractile elements of the knee is important for proprioceptive sense.

Lattanzio et al²⁵ conducted a study involving healthy male and female subjects performing three different cycling protocols (ramp, continuous, and interval training) at a percentage of their o₂max. In this study, methods for determining the threshold for detection of movement were similar, but angular replications were performed with subjects in the standing weight-bearing position instead of the seated open kinetic chain (OKC) protocol used in the study of Skinner et al. The results of the study of Lattanzio et al²⁵ were similar to those of Skinner et al, with statistically significant decrements in joint replication in male subjects after the three different fatigue protocols. Female subjects similarly showed significant differences in joint replication after the continuous and interval programs, but not with the ramp protocol for joint angular replication. The conclusions drawn by the authors of this study were that anatomic gender differences possibly account for the variation in proprioception in response to fatigue.

Finally, Barrack et al³⁰ and Barrett et al⁷³ studied the effects of total knee replacement on knee joint proprioception. This research paradigm is of particular interest because insertion of a total knee joint prosthesis results in removal of most joint receptors in the human knee. Both groups of investigators found no significant loss of proprioception in the extremity that underwent total knee replacement in comparison to the contralateral extremity 6 months postoperatively. These groups of authors both concluded that their research again points to the important role that muscle-based mechanoreceptors play in knee joint proprioception.

Effects of muscular fatigue on upper extremity proprioception and neuromuscular control

The role of specific afferent receptors in the human body has been examined with different methods to better understand the role of joint and muscular afferents. Provins⁶² reported a decrease in the ability to detect passive motion of the finger when digital nerves containing both joint and cutaneous afferents were blocked by local anesthesia. He concluded that both types of afferent feedback may be equally important when joint proprioception is analyzed.

Zuckerman et al⁸⁸ injected lidocaine into the subacromial space and glenohumeral joint to assess proprioception in young and old male subjects. They found no adverse effects from the injection of lidocaine in either location and proposed that compensatory extracapsular feedback ensured intact proprioception after injection. No differences in joint position sense and TTDPM testing were noted between the dominant and nondominant extremity; however, a decline in proprioception with age was measured in the young (20 to 30 years of age) and older (50 to 70 years of age) subjects.

Several studies have been performed on the human shoulder to investigate the effect of muscular fatigue on various indices of joint proprioception and neuromuscular control. Carpenter et al⁸⁹ tested subjects using a TTDPM test with the shoulder in 90° of abduction and 90° of external rotation. After an isokinetic fatigue protocol, subjects’ detection of passive motion was marred or decreased by 171% for internal rotation and 179% for external rotation. In preexercise testing, Carpenter et al found increased sensitivity when moving into external rotation versus internal rotation but no difference between the dominant and nondominant extremities.⁸⁹ These authors concluded that the effect of muscular fatigue on joint proprioception may play a role in injury and decrease athletic performance.

Voight et al⁴¹ tested subjects with an active and passive joint angular replication protocol after isokinetically induced muscular fatigue of the glenohumeral joint internal and external rotators. No significant difference in shoulder joint angular replication was found between the dominant and nondominant extremities. Significant decreases in accuracy were noted after muscular fatigue in both the active and passive joint angular replication tests. Pederson et al⁹⁰ tested the ability of healthy subjects to discriminate movement velocity of the glenohumeral joint in the transverse plane. The results of their study showed that subjects had a decrement in discrimination of movement velocity after a hard isokinetic horizontal flexion/extension exercise fatigue protocol versus a light exercise condition.

Myers et al⁹¹ used an active angular replication test and neuromuscular control test to examine the effects of muscle fatigue in normal shoulders. A concentric isokinetic internal and external rotation fatigue protocol was used. Fatigue of the internal and external rotators of the shoulder decreased subjects’ accuracy in detecting both midrange and end-range absolute angular error but did not have a negative effect on neuromuscular control in a bilaterally assessed unilateral CKC stability-type test measuring postural sway velocity.

Additional research by Myers et al⁹² has demonstrated that patients with anterior glenohumeral instability have alterations in muscle activation. Therefore, clinicians can implement therapeutic exercises that address the suppressed muscles as the scientific foundation of a rehabilitation program. Myers et al^93,94 found that capsuloligamentous injury to the shoulder decreases proprioceptive input to the CNS and thereby results in decreased neuromuscular control. Consequently, clinicians need to address the mechanical instability but also implement functional rehabilitation interventions to return an athlete to competition. Tripp et al⁹⁵ demonstrated that functional fatigue affects the acuity of the entire upper extremity.

Lin et al⁹⁶ investigated the effects of scapular taping on shoulder proprioception and EMG activity in several muscles of the shoulder complex. The magnitude of proprioceptive feedback was significantly lower in the taping conditions. The results suggest that scapular tape affects the activity of the shoulder muscles and ultimately that these effects are related to the proprioceptive feedback provided by the tape. Further research will continue to be needed to better understand and demonstrate the efficacy of shoulder and scapular taping because it is a very popular technique with many anecdotal reports demonstrating effectiveness; however, high-level research support for this technique is limited at this time.

The consistent finding in these studies of a decrement in proprioception after muscular fatigue has led researchers to emphasize the importance of the muscle-based receptors. The use of active joint angular positioning tests has been reported to stimulate both joint and muscle mechanoreceptors and is considered to be a more functional assessment of the afferent pathways.^2,15,91 The exact mechanism by which muscle-based proprioception is affected is not entirely clear or known. Muscle fatigue is thought to desensitize the muscle spindle threshold and thereby lead to decrements in both joint position sense and neuromuscular control. Djupsjobacka et al^97-99 reported alterations in muscle spindle output in the presence of lactic acid, potassium chloride, arachidonic acid, and bradykinin. Intramuscular concentrations of these substances are altered during muscular exertion and fatigue. This consistent relationship has provided further rationale and support for improvement in muscular endurance of the dynamic stabilizers of the glenohumeral joint. This topic is covered in detail in the application section of this chapter.

Effects of training on proprioception in the lower extremity

Some studies in the literature have investigated the notion of injury prevention and improvement in neuromuscular stabilization through proprioceptive training. A review of research in this section will provide the reader with important references that support the use of proprioceptive training of the lower part of the body for both injury prevention and rehabilitation.

In a prospective study by Cerulli et al,¹⁰⁰ 600 semiprofessional and amateur soccer players were monitored for three seasons to determine the frequency of ACL injury in players who underwent a progressive proprioceptive training program and in a control group who performed only traditional strengthening exercises. The results showed significant differences between the experimental and control groups, with the proprioception training group sustaining fewer lesions of the ACL than the control group who performed traditional strengthening exercises.

Osborne et al¹⁰¹ studied the effects of ankle disk training in eight individuals who sustained an inversion ankle sprain within the preceding years and who had not received any formal rehabilitation. The subjects performed 15 minutes of daily training on a disk with the involved leg in an 8-week training program. After completion of the 8-week training program, the subjects were tested for onset latencies with surface EMG electrodes on the muscles of the ankle influencing stability to measure the motor response to a simulated inversion sprain on a platform. The results showed significant improvements in anterior tibialis latency times in both the trained and untrained control ankles.

A similar study by Eils and Dieter¹⁰² showed significant improvements in muscle reaction times and patterns of muscle coactivation in 30 subjects with chronic ankle sprains. The subjects performed a multistation proprioceptive exercise program that included 12 stations with various devices once weekly for 6 weeks. The frequency of once per week and the types of exercises were chosen for their ability to be implemented easily into a rehabilitation program. The exercises included a Biodex balance system,* inversion boards, minitrampoline, and ankle disk. The subjects performing the exercises showed significant improvement over the control group in position sense and reported subjective improvements in functional stability.

Friden et al³¹ conducted a study in subjects with ACL deficiencies who performed traditional lower extremity strengthening exercises and in subjects who performed traditional rehabilitation along with perturbation training. The perturbation program consisted of progressive exercises using rocker boards and roller boards, with advancement to the next phase after successful completion of the task without evidence of instability or pain. After the training program, the perturbation group was found to have significantly greater success with subjective reports of stability during completion of higher-level activities than did the traditional training group. Beard et al⁷⁶ conducted a similar study but used hamstring reflex latencies and the Lyshom rating scale for measuring functional outcomes. They concluded that the group that underwent perturbation training had improved functional outcomes in knee stability while performing ADLs. Additionally, numerous studies have evaluated the effectiveness of neuromuscular training programs, including perturbation training, in patients with ACL injuries.^52,103-107 Numerous studies have also evaluated the effectiveness of neuromuscular training programs, including perturbation training, in patients with chronic/functional ankle instability.^108-111

One very important aspect inherent in most lower extremity proprioceptive training programs is inclusion of the entire lower extremity kinetic chain in the exercise. Most proprioceptive exercises in the literature described herein use multiple joint-training positions and CKC positioning environments that allow the entire lower extremity kinetic chain to be included. Research^112-114 has emphasized the importance of examining the entire kinematic chain from the trunk and hip musculature throughout the lower extremity for postural control mechanisms in rehabilitation and prevention of injury. Furthermore, using absolute angular error measurements, Miura et al¹¹⁵ found that local and general fatigue affects knee proprioception, decreases muscular power, and has effects on different mechanisms in the proprioceptive pathway. Consequently, to prevent injury caused by a fatigue-induced decline in proprioception, local muscle training by itself is not enough, but neuromuscular training, including central programming, is essential for the entire lower extremity kinetic chain.

Neuromuscular training for rehabilitation and prevention of sports injuries

Zech et al¹¹⁶ performed a systematic review of the use of neuromuscular training for rehabilitation of sports injuries. Fifteen studies met the inclusion criteria and demonstrated the effectiveness of neuromuscular training in increasing functionality and decreasing the incidence of recurrence after ankle and knee injuries. However, no studies demonstrated the effectiveness of neuromuscular training in rehabilitating sports injuries in the shoulder, only for lower body injuries. Though used inherently and recommended for shoulder rehabilitation, this systematic review showed much less scientific support for the use of neuromuscular control exercises in the upper extremity. Hübscher et al¹¹⁷ performed a systematic review of the use of neuromuscular training for rehabilitation of sports injuries. Thirty-two articles were identified, but only seven methodically well conducted studies were included in the review. Multiintervention training was effective in reducing the risk for lower limb injuries. Balance training alone decreased the incidence of ankle sprains in athletes. Interestingly, exercise interventions were more effective in athletes with a history of sports injuries than in those without. This probably relates to the concept of inadequate rehabilitation following the initial sports injury. Additional research on the use of balance training to improve neuromuscular control was performed by Zech et al.¹¹⁸ They completed a systematic review of balance training for neuromuscular control and enhancement of performance. Twenty RCTs met the inclusion criteria. Balance training was effective in improving postural sway and functional balance, and larger effect sizes were demonstrated for training programs of longer duration. It is controversial whether balance training was effective in improving jumping performance, agility, and neuromuscular control.

Clinical application: techniques to improve lower extremity proprioception and neuromuscular control

Lower extremity injuries occur often in competitive and recreational sports. These injuries are sometimes caused by physical contact with another individual, but they usually result from a noncontact injury in which the external forces in the environment exceed the internal forces of the body.¹⁰⁰ Some of the more common injuries involve damage to the ligamentous and cartilaginous components in the knee and ankle. Injuries that do not involve another person occur when the player or individual attempts to suddenly change the rate of speed or course of direction or when an obstacle in the external environment causes overload on the static joint restraints. The questions that have received recent attention in the literature are the degree to which these injuries can be prevented and, once an individual is injured, the ways in which recurrent injuries to an existing compromised system can be prevented through dynamic neuromuscular stabilization.¹¹⁹

For a patient with ACL deficiency, neuromuscular training is achieved through coordinated muscle activation in response to controlled perturbation forces imparted on the joint. One strategy for dynamic stabilization is cocontraction of opposing muscle groups to essentially stabilize the knee in a rigid posture. This strategy may be successful for simple tasks, but with higher-level activities such as sports, stabilization is achieved through selective motor recruitment that is dependent on the task. A force feedback mechanism in which stability is achieved through varied patterns of muscle recruitment, depending on the situational needs of the task, has been discussed.^1,2 This theory acknowledges that different patterns of movement require varied muscular stabilization, depending on the direction, speed, and amount of force occurring at the joint.

At the University of Delaware, Snyder-Mackler et al^1,120 designed a rehabilitation program based on the premise of achieving dynamic muscular stabilization during normal and higher-level skills through neuromuscular perturbation training. They use the term copers for individuals who successfully perform varied high-level activities without experiencing functional instability. In copers, the muscular strategies used for joint stability allow normal joint movement, whereas deleterious compressive and shear forces at the joint are minimized. The term given to individuals who are unsuccessful in maintaining joint stability during lower extremity weight-bearing tasks is noncopers. In the group of noncopers, a cocontraction stiffening strategy is used with all tasks, which results in inefficient movement strategies and functional instability. Furthermore, with this inadequate coping mechanism, progressive deterioration of joint surfaces and capsuloligamentous restraints occurs as a result of excessive shear and compressive forces at the joint.^1,2

The faculty at the University of Delaware designed a program using the guidelines of Fitzgerald et al to implement a neuromuscular training program for patients with ACL deficiency in an attempt to restore functional stability during higher-level sporting activities. In selection of individuals for the program, certain criteria had to be met to ensure a successful outcome of the training.

The program is designed to identify individuals who would be successful rehabilitation candidates through a screening process. The criteria include isolated injury to the ACL, infrequent episodes of instability (< 1), a passing score on functional hop tests, and a passing percentage on two subjective rating scales for functional knee impairment. Before a stabilization program is initiated, the early focus of rehabilitation is on decreasing joint effusion, restoring ROM, and increasing quadriceps and hamstring strength to allow stabilization through muscle recruitment.¹ When these goals have been met, an advanced neuromuscular training program can be initiated. The program is progressive in nature and designed for specificity of sport or activity.

The program consists of 10 treatment sessions at a frequency of two to three times per week and is progressive in nature with three phases of implementation (early phase, sessions 1 to 4; middle phase, sessions 5 to 7; and late phase, sessions 8 to 10). Progression of the program is based on the symptomatic patient response (i.e., increased effusion or pain), which is used as a guideline, and the ability of the patient to perform successful motor strategies to counteract the perturbation force, which includes no episodes of falling or instability. All three phases include the use of rocker boards, roller boards, and platforms with an introduction to sport-specific agility drills in the middle to later stages.

In the early phase of perturbation training, patients are subjected to perturbation forces on all three devices in slow predictable directions with the use of verbal cues as necessary for the onset and direction of the forces. Initially, the direction of the applied forces is in the anterior/posterior and medial/lateral directions with progression to diagonal and rotational planes. The clinical implication of this phase thus involves the application of progressive variable perturbation forces in multiple directions (sagittal, transverse, and frontal planes) in a controlled manner to retrain the nervous system in a number of applications or situational needs while avoiding the use of rigid cocontraction strategies.²

The middle phase of training continues with perturbation training and requires successful adaptation of strategies in the early phase. Variations in the parameters of training, including predictability, speed, amplitude, intensity, and direction of force, are advanced, along with the implementation of light sport-specific drills while the individual is wearing a functional knee brace. In the last phase of treatment, sport-specific movements are emphasized with the use of agility drills. Initially, training begins in straight planes and then moves to variable-direction drills such as cutting and changing direction on command. The drills are initially performed at 50% and progress to 100% in the later stages. Examples of some of the agility drills are side shuffles, shuttle running, and cutting maneuvers at 45° and 90° angles. With no evidence of instability, patients then perform sport-specific activities while undergoing perturbations on roller boards and platforms to simulate the competitive demands of the sporting environment. Before returning to full athletic competition, athletes are required to pass a posttreatment ACL screening involving measures similar to those used during prescreening for acceptance into the program.²

Guidelines for implementing lower extremity proprioceptive training

Regardless of whether surgery or conservative care is chosen to restore stability and function to a degenerative or unstable joint, rehabilitation is crucial for reestablishing neuromuscular control or dynamic stability in a compromised joint. The loss of neuromuscular control results from damage to the mechanoreceptors within the capsuloligamentous structures of the joint and from interruption of the afferent sensory pathways that play a crucial role in producing smooth, coordinated movement.²

Several considerations are important when a rehabilitation program is designed to restore proprioception and dynamic stability. In selecting exercises for training, a focus on restoring function to the individual should remain at the forefront. Exercises chosen should then focus on an individual’s deficits in strength, ROM, and balance and, most importantly, on the individual’s ability to meet the demands of stability while performing daily or sporting activities.

Traditionally, a combination of OKC and CKC exercises have been used in rehabilitation. OKC exercises have been defined as movements in which the distal segment is free to move in space, and CKC movements occur when the distal segment is fixed or meets considerable resistance.¹²¹ Emphasis on the use of CKC exercises has predominated because they are thought to more closely resemble the functional demands placed on the lower extremity during a variety of activities. Another advantage of CKC exercises is the simultaneous movement of multiple joints, which requires cocontraction of opposing muscle groups to control joint movement. CKC exercises can also reduce shear forces across joint surfaces as a result of the stability of joint-through-joint compression forces and cocontraction of opposing muscle groups. The advantage of OKC exercises is their ability to isolate targeted muscle groups for strengthening.

In a study by Snyder-Mackler et al,¹²² isolated OKC quadriceps strengthening was found to be superior to CKC exercises in improving quadriceps function in patients after ACL surgery because the involvement of other muscle groups in performing the CKC exercises did not isolate the quadriceps as effectively. In fact, most functional activities, such as ambulation, use a combination of both OKC and CKC muscle activation patterns, and therefore both should be incorporated in the design of a successful program.

In the early stages of rehabilitation, the development of an exercise program should identify deficits in ROM, strength, and joint effusion, and progression should not exceed the rate of natural healing or limitations in the involved structures. Any number of exercises will elicit proprioception training based on the fact that deformation of the joint mechanoreceptors occurs with active, active assisted, and passive movements and provides sensory input to improve neural mechanisms.² Performing ROM exercises on an immobilized joint and weight shifting early after an ankle sprain or surgery on the ACL are examples of early forms of proprioception training.

When sufficient healing has taken place in the subacute stages of recovery, initiation of resistance exercises for building muscular strength and endurance will enable sufficient muscle recruitment patterns for the dynamic stabilization needed for advanced forms of training. Proprioceptive training in this stage may involve two-legged stance exercises on an unstable surface such as the Biodex stability balance system (Fig. 24-3), which can be advanced to a functional squatting movement pattern. The exercise progression can include single-leg stance (Fig. 24-4) and single-leg stance with partial squatting on the machine with the benefit of a visual cursor to assess weight distribution so that compensatory patterns can be avoided.

Figure 24-3 Incorporating functional movements such as the squat on the Biodex balance system.

Figure 24-4 Single-leg balance on Biodex balance system. The level of difficulty is progressed by decreasing the stability of the platform or removing visual cues by having the patient close his eyes.

Other exercises that are beneficial for proprioception involve the use of rocker boards for directional perturbations to activate selective muscle recruitment patterns in a variety of planes of movement. These training techniques can be advanced to sport-specific activities such as tossing a ball against a trampoline while manual perturbations are applied to the board (Fig. 24-5). Movement patterns such as a straight plane or multidirectional lunge are also useful for selective motor recruitment in functional or sport-related activities (Figs. 24-6 and 24-7). These patterns can be performed on balance pads or exercise mats to enhance motor control through maintenance of balance while performing initially slow and then more rapid movements beyond the base of support (Fig. 24-8).

Figure 24-5 Chest pass with a weighted ball incorporates plyometric exercises with proprioceptive exercise, with difficulty being increased by manual perturbations of the rocker board while the patient throws and catches the ball.

Figure 24-6 Combination of proximal pelvic control with lower extremity proprioception while the patient performs lunges on Thera-Band balance pads.

Figure 24-7 A lunge being performed with rotation of the torso while a weighted ball is held outside the base of support for the integration of upper and lower extremity movement patterns.

Figure 24-8 Single-leg balance on Thera-Band balance pads while opposite extremity movements are resisted beyond the base of support in functional planes.

The goal of proprioceptive training is to reestablish stability or dynamic neuromuscular control and should emphasize return to functional or sport-specific activity. In the later stages of training, exercise should focus on restoring and ideally optimizing the adaptive neuromuscular response to situational needs. If stabilization training has yielded the appropriate muscular response toward the final stages of rehabilitation, more advanced exercises incorporating sport-specific drills should be performed. Exercises on a Fitter board* or slide board can be performed to challenge the patient with higher-velocity movements while performing sport- specific drills involving full body movement patterns on a yielding surface (Figs. 24-9 and 24-10). Agility drills, including progressively quicker changes in direction while pivoting on the involved extremity, should be incorporated in the final stages of rehabilitation for athletes who perform such maneuvers in the competitive arena.

Figure 24-9 Dynamic balance on a slide board incorporating upper body movements with resistance in proprioceptive neuromuscular facilitation patterns. A, Reaching high. B, Reaching low.

Figure 24-10 Dynamic balance on a Fitter board with sport-specific drills such as the ground stroke in tennis. A, Forehand. B, Backhand.

Clinical application: techniques to improve proprioception and neuromuscular control of the upper extremity with specific reference to the shoulder

Application of the basic science information on proprioception and neuromuscular control of the shoulder to clinical practice allows clinicians to most appropriately provide stability to the glenohumeral joint and optimize shoulder girdle arthrokinematics. Several areas are covered in this section, including the use of CKC and joint approximation exercises, joint oscillation exercises, postoperative interventions, and techniques to improve muscular endurance of the rotator cuff and scapular musculature.

Closed Kinetic Chain (Joint Approximation) Exercises

Exercises that produce approximation of the glenohumeral joint and are characterized by a fixed distal aspect of the extremity are typically referred to as joint approximation or CKC upper extremity exercises. The approximation of the joint surfaces and the multiple joint loading inherent in CKC exercises are reported to increase mechanoreceptor stimulation^2,123 and produce muscular cocontraction. The presence of muscular cocontraction around the human shoulder is particularly beneficial because of the important role that the musculature surrounding the scapulothoracic joint plays in stabilizing and controlling movement of the shoulder.^124,125

Significantly less EMG research has been published on upper extremity CKC exercise than on upper extremity OKC exercise. Moesley et al⁴⁶ published a comprehensive analysis of the scapular muscles during traditional rehabilitation exercises. Two CKC upper extremity exercises were included in their analysis. These exercises were the push-up with a plus and the press-up. The push-up with a plus includes maximal protraction of the scapula during the end of the ascent phase of a modified push-up and produces very high levels of serratus anterior muscle activity. The press-up exercise did not elicit high levels of muscular activity in the trapezius or serratus but instead produced high activation levels in the pectoralis minor. Decker et al¹²⁶ confirmed the importance of the plus position for serratus anterior activation and concluded that exercises emphasizing scapular upward rotation and accentuated protraction produce the highest levels of muscular activity in the serratus anterior.

Kibler et al¹²⁵ published EMG research on a series of very low level CKC exercises for the upper extremity, including weight-bearing upper extremity weight shifts and exercises on the rocker board or biomechanical ankle platform system with the upper extremity. Muscle activation levels during these exercises were very low in the rotator cuff, deltoid, and scapular muscles; however, low levels of activity were present in virtually all these muscles during these activities. This indicates that high degrees of coactivation and cocontraction are inherent in this type of exercise.

Research has demonstrated the important role that joint compression plays in glenohumeral joint CKC exercise. Warner et al³⁷ studied the effects of applying a 5-, 25-, and 50-lb compressive force to cadaveric shoulder specimens. These amounts of compression resulted in decreases in anterior humeral head translation in neutral elevation from 11 to 2 mm with 5 and 25 lb of compressive force and from 21.5 to 1.4 mm at 45° of abduction, respectively. This study shows the potential benefit of a compressive load in the provision of glenohumeral joint stability and points out the important application that CKC exercises may have in enhancement of neuromuscular control in patients with glenohumeral joint instability.

Application of CKC exercises clinically is facilitated by a thorough review of glenohumeral joint anatomy. It is imperative that the clinician realize the osseous relationship of the glenohumeral joint. The human glenoid is oriented slightly inferiorly with the arm held at the side and tilted anteriorly 30° from the coronal plane of the body.^127,128 This anterior version of the scapula is aligned with 30° of retrotorsion of the humeral head, and optimal bony congruity occurs with the arm placed in the scapular plane.¹²⁸ Understanding these important relationships will guide the clinician in shoulder positioning and ROM selection during joint approximation exercises with the arm placed in the scapular plane.¹²⁸

Research on CKC upper extremity training is limited. Lephart et al⁸⁶ used five neuromuscular control exercises that emphasized joint positioning, joint approximation and compression, and muscular cocontraction in one experimental group, in addition to traditional OKC shoulder rehabilitation exercises in patients with glenohumeral joint instability. They found significant improvements in kinesthetic ability, scapular slide testing, and isokinetically documented protraction and retraction strength in the group that performed these neuromuscular control exercises during rehabilitation.

Application of these concepts in patients with rotator cuff dysfunction and glenohumeral joint instability is pictured in Figures 24-11 to 24-15. Guidelines for the time-based sets of exercise depend on the patient, with the ability of the patient to maintain the desired scapulothoracic stabilization being a governing factor. Careful monitoring of the medial and inferior borders of the scapula is important to ensure proper neuromuscular control and avoid the development of undesired motor patterning.¹²⁴ Sets of exercises lasting up to 30 or 45 seconds are desired in the later stages of rehabilitation.

Figure 24-11 Closed chain wall scapular-plane rhythmic stabilization. The patient’s arm is placed on a medicine ball or small exercise ball in varying degrees of abduction in the scapular plane. The clinician performs rhythmic stabilization with the patient remaining as stable as possible over the ball; varying the position of the hand contacts by progressing further toward the patient’s hand increases the intensity of the exercise.

Figure 24-12 Quadruped rhythmic stabilization exercise progression with instruction to maintain scapular protraction or the “plus” position during repeated multidirectional challenges.

Figure 24-13 Tripod rhythmic stabilization technique with the involved extremity in the closed chain position and maintenance of the “plus” position to increase activation of the serratus anterior muscle. The clinician alternately provides multidirectional challenges to the non–weight-bearing limb as the patient attempts to isometrically hold the pictured position.

Figure 24-14 Unilateral prone exercise ball stabilization exercise. The degree of support is progressively decreased to increase the challenge to the patient by sliding the patient in a cephalad direction.

Figure 24-15 High-level unilateral scapular stabilization exercise with the patient in a closed chain unilateral scapular-plane stance position with rhythmic stabilization superimposed on the upper extremity to increase the challenge of the exercise.

Joint Oscillation Exercises

Rehabilitative exercises involving joint oscillation have increased in popularity in recent years. Appliances such as the Bodyblade,* BOING (body oscillation integrates neuromuscular gain),† and resistance bar‡ have facilitated the use of joint oscillation exercises. Rapid oscillation of these devices coupled with external loads such as light weights, manual resistance, and TheraTubing‡ can provide additional emphasis on particular muscle groups during these exercises. Figures 24-16 to 24-19 show exercises using oscillatory devices or manual contact that require the rotator cuff and scapular musculature to respond to external cues induced via the oscillation and stretch imparted during the exercise. The ability of these time-based exercises to promote local muscular endurance is increased by manipulation of set duration and rest cycles.¹²⁹ Progression to the external rotation oscillation exercise in Figure 24-17 by using the 90° abducted scapular-plane position is followed as rehabilitation progresses to more closely approximate the glenohumeral and scapulothoracic positions inherent in overhead sport-specific movement patterns.¹³⁰Figure 24-20 shows the push-up with a plus exercise. Care is taken with this exercise to protect the shoulder complex by descending only approximately one half the distance of a standard push-up and then maximally protracting the scapula on the ascent phase to increase activity of the serratus anterior muscle.⁴⁶

Figure 24-16 Supine modified rhythmic stabilization technique performed in 90° of shoulder flexion with scapular protraction.

Figure 24-17 Side-lying glenohumeral rotational oscillation exercise using the Bodyblade.

Figure 24-18 Biped closed kinetic chain exercise using the Bodyblade to provide joint oscillation in the non–weight-bearing upper extremity and a medicine ball to decrease surface stability of the closed chain upper extremity. Scapular position can be altered in this exercise, depending on the intended goal of muscular activation.

Figure 24-19 “Statue of Liberty” external rotation oscillation exercise using Thera-band elastic resistance and a resistance bar for oscillation. A scapular-plane position in 90° of elevation is used while the contralateral extremity provides support to decrease the role of the deltoid in actively holding the exercising extremity in the 90° position.

Figure 24-20 Push-up with a plus and maximal protraction of the scapula to elicit higher levels of serratus anterior activity. A, Starting position. B, Ending position of movement.

Holt et al¹³¹ investigated four different positions of exercise with the Bodyblade and its effect on infraspinatus muscle activity. These four positions included (1) standing with the glenohumeral joint in a neutral abduction/adduction position for internal and external rotation, (2) side-lying position with the glenohumeral joint in neutral abduction/adduction for internal and external rotation (see Fig. 24-17), (3) 90° of glenohumeral joint scapular-plane elevation with stabilization, and (4) 90° of scapular-plane elevation with the unsupported arm. The results of a repeated-measures analysis of variance showed that the side-lying internal/external rotation oscillatory pattern elicited the highest levels of infraspinatus muscle activation.¹³¹ Further research such as this is needed to guide clinicians in the use of oscillatory-type exercise.

Conclusion