Powerful, precise, controlled movements are an integral part of sports activities and daily functional activities. The somatosensory system provides multiple inputs to the central nervous system (CNS) from various muscle and connective tissue receptors contributing to proprioception. In conjunction with vestibular and visual information, it allows us to maintain stability and move body segments efficiently, accurately, and effectively to accomplish a given task in a specific environment. This is, in a general sense, motor control (48). A thorough understanding of proprioceptive function is essential to understanding its contributions to, and implications for, sports injury rehabilitation and athletic conditioning and performance.
Several questions are pertinent to the topic under consideration in this article. First, what is proprioception? Second, is proprioceptive function diminished significantly enough from injury (or disease) to affect high-level function? Third, can proprioceptive function be improved through exercise or training? And finally, can so-called proprioceptive training or exercise prevent injury? The purpose of this article was to address these questions. Subsequently, it is hoped that the reader will have a more thorough understanding of what constitutes proprioceptive exercise/training if in fact such exercises/training actually exists.
WHAT IS PROPRIOCEPTION?
The term “proprioception” literally means to receive (-ception) one's own (propio-). Proprioception is a subsystem of the somatosensory system that also includes pain, touch, and temperature sensation from the skin and musculoskeletal structures (31). It is the body's own sense of position and motion, which includes body segment static position, displacement, velocity, acceleration, and muscular sense of force or effort (13,43). This sensory information is derived from changes to internal structures as opposed to external stimuli (exteroreception), such as chemicals or heat acting on the body (43,44). Signals derived from various sensory endings, that is, proprioceptors, in response to mechanical deformation are transformed into electrical impulses that are represented at both conscious (cerebral cortex) and unconscious (cerebellum) levels of the CNS (31). These signals are transformed into relative position and movement parameters (43). Kinesthesia (kinesis: movement, aisthesis: sensation), or movement sense, is a component of proprioception. Although it is traditional to think of proprioception as only a sensory function, Gandevia et al. (14) provided evidence that there may be a motor (efferent) component to determining position and movement of the limbs and trunk, noting that volitional effort resulted in an increased illusion of limb motion in a paralyzed limb. This seems to apply to the definition of proprioception regarding muscular effort, as noted above.
The sensory receptors that subserve proprioceptive function are located in various connective tissues, including skin, ligaments and joint capsules, and muscle tissue throughout the limbs, trunk, and neck. It is thought that muscle spindles are a primary source of proprioceptive input during most movement (14,18), whereas capsular, ligamentous, and cutaneous mechanoreceptors provide additional input that augments spindle input for position and movement sense (31,43,44). Ligamentous receptors are particularly sensitive to end-range forces and are thought to participate in a ligament-muscle reflex that is protective in nature (43). Integrated sensory input from these receptors at multiple joints creates a highly redundant system for the purpose of accurate sensing and determination of limb position and movement during specific activities in both closed- and open-chain activities.
PROPRIOCEPTION AND INJURY
The second question is whether proprioceptive function can be altered by injury. Somatosensory input, along with sensory input from the vestibular and visual (special sensory) systems, provides for maintenance of dynamic balance during movement activities. Any significant alteration or loss of information from any one or combination of these systems may result in significant challenges to normal movement and postural stability leading to possible injury (36). The question then becomes, to what extent can an injury to joint structures and/or muscles affect proprioceptive function?
A number of studies have been conducted to assess changes in proprioception after a sports injury, particularly at the knee after ACL (anterior cruciate ligament) injury (4,6,7,11,20,26,32,34,38) and ligamentous injuries to the ankle (15,16). In the literature, proprioception is typically indirectly measured using threshold to detection of passive motion (TDPM) and reproduction of joint position (RJP) procedures for determining motion and position sense, respectively (45). TDPM tests the point at which a subject can sense a change in limb-segment position, that is, identify when, and in what direction, the limb segment has moved (angular displacement has occurred). RJP tests the ability of a subject to accurately reproduce a specific joint angle, noted as degrees difference from an initial joint angle (position) and the repeated joint angle, that is, joint angle error (JAE), and involves passive and/or active motions. The JAE can be calculated as absolute, constant (real), and/or variable error (8).
The specific methodology of each test varies considerably from study to study, making comparisons of results difficult. Studies have noted increased TDPM (poorer movement sense) with ligamentous injuries at the knee, ankle, and shoulder. However, some studies of similar subjects have noted no significant changes in TDPM (7,27,32) depending on study methods and test independent variables (e.g., joint angle at which tests are started). Increased TDPM has also been noted as a result of muscle fatigue (53), with normal thresholds reestablished within a brief period after a fatiguing bout of exercise. Proprioception has been noted to diminish with age (41,54), and in persons with osteoarthritis (55), although some studies have shown no differences (46). Generally, significant threshold increases are in the range of 0.5°-1.5° (12,45). However, the clinical or functional significance of these small changes is still uncertain.
Studies using RJP after ACL injury and surgery have generally noted no significant changes in position sense (11,20,34,39). Normal angular error can range from as little as 0.7° to greater than 6° in normal subjects depending on test conditions (e.g., weight bearing versus non-weight bearing) and methods (12,34,39). Correlations of results comparing TDPM and RJP have failed to note a significant association between the 2 testing methods (19). These tests may involve different neural processes that have not been clearly differentiated with regard to how the CNS uses this sensory information during activity (5). Grob et al. (19) concluded that there is no comprehensive test of proprioception available. Finally, studies have demonstrated weak to moderate correlations between changes in proprioception and functional outcome measures (12,37,39).
Clinical tests of proprioception include having patients close their eyes and note when, and in which direction, limb segment has been moved, touching a point on the body accurately, matching limb/segment positions or motions, and noting number of errors (17,31). However, no studies of proprioception in orthopedic or athletic populations using these clinical tests for proprioception were found in the literature.
Ashton-Miller et al. (2), in agreement with Grob et al. (19), noted that we may not have yet developed the best test for proprioception, and, until that is accomplished, we cannot effectively address the importance of such small changes on function and performance. Nashner (36) stated that only massive loss of proprioceptive information can lead to significant functional changes, so small changes in TDPM and RJP, although statistically significant, are not likely to be clinically significant. Indeed, there is limited evidence that these small changes in either position or motion sense contribute to significant functional and/or performance deficits in an athletic population.
IMPROVING PROPRIOCEPTION THROUGH EXERCISE OR TRAINING
Cerulli et al. (10) defined proprioceptive training (preventive) as “a series of exercises or situations that will elicit a response from the nervous system in order to counteract external stimuli.” This definition implies that some exercises do not elicit a neural response to counteract external stimuli. In fact, all exercises, whether active or passive, static or dynamic, will elicit responses from receptors that provide for sensations of limb/trunk/head position and motion. The question as to whether proprioception can actually be improved through exercise or training has proved to be very difficult to answer.
Much of our understanding regarding proprioceptive exercise or training is confused by improper understanding and use of concepts and terminology. A number of articles imply that the use of “proprioceptive training” or “proprioceptive exercise” is an essential element for rehabilitation of ankle and knee injuries (6,9,10,24,25,29,30,51,56). The combined terms “proprioceptive/balance” and “proprioceptive/neuromuscular” training are also commonly used. In many articles, this training is not clearly defined or related to the specific prescribed exercises or activities. Furthermore, balance is not synonymous with proprioception. Balance is the ability to maintain the center of mass within the base of support and depends on accurate information from the somatosensory, vestibular, and visual systems (Figure 1). The somatosensory input is the primary source of sensory input in adults for maintaining balance (48,49). Proprioception is the CNS process of determining the relative position/movement of the limbs/trunk while balancing. Motor control, or neuromuscular function, determines the outcome, that is, a specific performance parameter. It is this aspect that most likely changes with training.
Performing proprioceptive exercise on a balance board is really a misnomer. Attempting to balance while standing on an unstable surface (Figure 3) does not selectively train the proprioceptive system, it reweights the vestibular and visual information (versus somatosensory input) to a different degree than standing on a stable surface (43,44,49). When athletes or patients use unstable surfaces for training or rehabilitation (Figures 2-4), they actually lack orientationally accurate somatosensory information, altering proprioceptive input to the CNS, and must depend on visual and vestibular inputs to a greater extent to maintain balance (49). If the eyes are closed at the same time, then the only accurate information comes from the vestibular system (43,44,49) (Figures 3 and 4). The CNS must accommodate appropriately for balance to be maintained without orientationally accurate somatosensory information to then provide the appropriate neuromuscular output (motor control). So, when exercises are performed on an unstable surface, proprioception is not being trained to improve, per se. This activity, that is, balance training, is reweighting inputs from the somatosensory, vestibular, and visual systems, contributing to the determination of position and motion of the limbs and trunk as required to meet the challenge of the activity (Figures 1-5). In summary, effective CNS processing of somatosensory information is likely best attained by performing balance activities on a stable surface and then using other challenge strategies, for example, eyes closed and expected or unexpected perturbations.
Barrack et al. (5) demonstrated that ballet dancers had lower TDPM values than nondancers but also less accurate RJP. They concluded that training as dancers does affect proprioception and that the 2 tests involve different neural mechanisms. However, the ballet dancers were not tested before undergoing training as ballet dancers, so it is difficult to conclude that measures on either test can be directly attributed to being trained ballet dancers despite being compared with a control group of nondancers. Vuillerme et al. (57) demonstrated that gymnasts were able to reintegrate proprioceptive information (sensory reweighting) more rapidly than other athletes after tendon vibration at the ankle, suggesting that their specific training, particularly with regard to balance, could affect their ability to process proprioceptive information. However, the gymnasts were not measured before their training, so it is difficult to attribute the effect to their training alone despite comparison with other athletes (nongymnasts). These athletes had no history of injury, and only 1 joint was tested.
Li et al. (28) demonstrated that 16 weeks of Tai Chi training in older adults resulted in slight but significant improvements in TDPM with combined ankle motions (no difference with isolated plantar flexion versus dorsiflexion). However, there was no difference between groups over time, demonstrating no training effect for ankle joint kinesthesia. Xu et al. (58) found that elderly subjects who were long-term practitioners of Tai Chi had significantly better ankle TDPM than a cohort of active (swimmers/runners) and sedentary subjects. However, there was no difference at the knee joint.
Patrella et al. (41) demonstrated that older (>60 years) active adults had significantly better proprioception (RJP) than sedentary adults, indicating that activity may slow the loss of proprioceptive function with age. Sahin et al. (46) found that “kinesthesia and exercises of balance” (including slow and fast sit-to-stand to sit, backward/forward walking, plyometrics, agility, and various balance board and mini-trampoline exercises) for more than 8 weeks resulted in significant improvement in RJP in a group of subjects with benign joint hypermobility syndrome (BJHS). However, these subjects demonstrated improvement in only 1 value (occupational activity) of a multivalue functional assessment tool (Arthritis Impact Measurement, Scales-2) when compared with a nonexercise group with BJHS. There was no difference between groups in physical status, symptoms, emotional status, or social activity status. So, although use of kinesthesia and balance exercises appeared to result in improved proprioception as measured by RJP, there seems to be some question as to how, and to what extent, improved RJP relates to improved function or performance.
Lin et al. (30) found that subjects with osteoarthritis were able to significantly improve RJP error after proprioception training that was highly specific to the form of RJP testing performed. Subjects used a targeting activity for the lower limb to improve accuracy of movement. Subjects who performed only strength training at the knee also had improved proprioception, but the change was not statistically significant. Both groups demonstrated clinically meaningful improvements in function. Conversely, other studies have shown that subjects with osteoarthritis have improved knee joint proprioception after performing simple knee strengthening exercises (47,54), as well as with increased general activity (54).
In summary, it must be noted that in all these studies, the broad range of what are classified as “proprioceptive exercises” clearly involve a variety of both simple and complex activities, all of which elicit sensory responses from muscles and joint structures and can lead to varied changes in measures of proprioception, that is, TDPM or RJP.
PROPRIOCEPTIVE EXERCISE/TRAINING FOR INJURY PREVENTION
A number of recent injury prevention studies have used a wide range of training regimens to prevent initial or recurring injuries (3,9,10,33,40,52,56). In general, interventions included strengthening, balance (stable and unstable surfaces with and without perturbation), agility, plyometrics, and sports-specific activities. Outcomes varied regarding the incidence of injury and/or reinjury. Verhagen et al. (56) found a significant decrease in the incidence of recurrent ankle sprains in volleyball players who participated in a variety of “proprioceptive balance” activities on both stable and unstable surfaces. However, this was not the case in subjects who had no history of ankle sprains. In addition, subjects with a history of knee injury actually had a higher incidence of overuse injuries compared with the control group. No measure of proprioceptive testing was included in this study, so the notion that proprioception was improved could not be determined. The terminology “proprioceptive training” or “proprioceptive exercise” seems inappropriate in this context given the wide range of intervention activities. These exercises quite simply provided motor control challenges, that is, motor control training or neuromuscular training, to the system under progressively challenging tasks. The terminology “neuromuscular exercise/training” or “motor control activities” would seem to be a more appropriate description of the exercises used in this study.
Mandelbaum et al. (33) implemented proprioceptive and neuromuscular training for 14- to 18-year-old female soccer players for more than 2 seasons that resulted in 88 and 74% fewer ACL injuries when compared with athletes who did not participate in the training. The interventions included education, strength, flexibility, plyometrics, and sport-specific agility activities. No proprioceptive measures were included either before or after training. Stasinopoulos (52) instituted an ankle sprain prevention program for female volleyball players, including a group performing technical activities, that is, takeoff and landing activities specific to soccer, a group performing “proprioceptive balance board exercises,” and a group using an ankle orthosis. All groups had a decrease in the incidence of ankle injuries during the season, with the technical group demonstrating fewer injuries than the proprioceptive and orthosis groups. Clearly, specific activities related to the sport, along with a variety of balance activities, will improve motor control and performance.
These studies suggest that multifaceted intervention programs appear to prevent ankle sprains and, to some extent, knee injuries in specific groups of athletes. It must be noted that there is no single exercise that is specifically “proprioceptive,” nor are the results generalizable to larger unspecified populations. This has been confirmed in meta-analysis studies by Hubscher et al. (23) and Alentorn-Geli et al. (1) that found wide variations in exercises used for prevention of injuries to the lower extremity and reasonable evidence for the effectiveness of these programs. Alentorn-Geli et al. (1) stated that multicomponent programs are the most effective regarding injury prevention, particularly preventing recurrent injuries. Hubscher et al. (23) concluded that balance and multifaceted training activities may result in injury prevention at the knee and ankle in a specific population of athletes. However, they noted that the physiological mechanisms, for example, proprioceptive function, that result in the fewer injuries still need to be identified to determine the most effective efficient training approaches.
In studies where kinematic variables have been correlated to increased risks of ACL injury, neuromuscular training has been implemented to train subjects to change motor patterns during specific activities (22,35,42,50). For example, during landing, female athletes tend to have less knee flexion and greater hip adduction/knee valgus than male athletes, which is thought to contribute to an increased incidence of noncontact ACL injuries (22,42,50). Athletes then undergo training to land more softly with greater knee flexion (Figure 6) and with the knee moving directly forward over the foot rather than collapsing medially (50). Neuromuscular training then refers to the sensory and motor aspects of controlling movement patterns and involves motor learning that results in permanent changes in performance, hopefully contributing to fewer injuries.
An issue that needs to be addressed is the ability to isolate proprioceptive input using specific exercises. Cerulli et al. (10) stated that “a training program including weight-bearing exercises and a progressive reduction in stability (wobble board, eyes open and then closed) with increasing repetitions and rate of contractions appears better than a traditional program of muscle strengthening (non-weight-bearing and graduated weight-resisted exercises) in improving reflex hamstring contraction latency and dynamic joint stability.” Arguably, these activities require the integration of somatosensory, visual, and/or vestibular inputs to the CNS at all levels to stabilize the body through motor responses during these challenges (10,44). There is evidence that balance will be enhanced when these types of activities are included and that injuries to the knee and ankle may be prevented and reduced through this kind of training (9,10,21,24,35,56). But it must be reiterated that these activities elicit a broad range of sensory inputs and motor outputs across the CNS and peripheral nervous system that lead to enhanced neuromuscular responses, motor control, and motor learning. To ascribe these changes solely to the proprioceptive system alone is a very limited and inaccurate viewpoint.
Proprioception is an important sensory function for all normal movement activities, including the ability to maintain dynamic balance and move accurately. All exercises elicit proprioceptive responses to some extent. However, it is still uncertain which exercises may be more or less proprioceptive, resulting in direct improvement of proprioception, function, and athletic performance. There is reasonable evidence to suggest that interventions challenging dynamic stability using various strengthening, balance, agility, and sport-specific activities may lead to improved performance, recovery from injury, and injury prevention. It is important that correct concepts and terminology be used when describing these concepts and activities.
Sincere thanks to Ms. Karen Stephenson, administrative assistant, The University of Alabama at Birmingham Department of Physical Therapy, for her valuable assistance in preparing figures for this article.
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Keywords:© 2011 National Strength and Conditioning Association
proprioception; somatosensory; injury prevention; balance; proprioceptive exercise; neuromuscular training