Definitions and Background Information
Motor control is essential for postural balance and for the movement of the body through space. Garrett and Kirkendall 18 stated that, “motor control is a function about which we may know a great deal but, in reality, understand very little”. For years, conditioning programs that stressed increasing muscle strength, flexibility, endurance, and power (isolated joint mechanics) have been thought to be the basics necessary for injury prevention in sport. 11,13
More recently, there has been an increased recognition that to prevent injury in sports one also must improve functional joint stability through enhancement of neuromuscular control mechanisms. For example, all of the recently developed anterior cruciate ligament injury prevention programs emphasize the importance of neuromuscular control. This requires integration of sensory input and motor output, coordinated by the central nervous system. Sources of sensory input include visual, vestibular, and somatosensory. 40,46,47
The somatosensory system (the peripheral afferent mechanism related to postural control) provides information concerning the orientation of body segments relative to one another and to the support surface. Input to the somatosensory system can be subdivided into tactile and proprioceptive senses and comes from peripheral sensory receptors located in the skin, muscles, and joints. Proprioception has been defined as the specialized variation of touch that encompasses the sensation of joint movement (kinesthesia) and joint position (static joint position sense). 39,40 As reported by Ashton-Miller, 2 the term proprioception was introduced by Sherrington in 1906 and comes from the Latin words (re)ception (the act of receiving) and proprius (one’s own). It has been termed the mediator of neuromuscular control. 39,40
Mechanoreceptors are specialized sensory receptors that transduce mechanical deformation into an electric neural signal that travels via cortical and reflex pathways to provide information pertinent to proprioception, that is, information concerning joint position and joint movement. Mechanoreceptors include Pacinian corpuscles, Meissner corpuscles, Golgi tendon organs, muscle spindle cells, Ruffini nerve endings, and free nerve endings that are found in the capsule, retinaculum, and ligaments of the joint and in the skin, muscle bellies, and tendons around the joint. 39,46 Initiation of reflex arcs stimulated by mechanoreceptors occur at a faster rate (70–100 m/second) than those stimulated by nociceptors that travel only 1 to 3 meters per second. 10,22 Therefore, this would suggest that proprioception may play a more significant role than pain in preventing injury. 39
Information gathered by this system is processed at three levels. 16,39 At the spinal level, responses provide dynamic muscular stabilization through activation of the spinal reflexes. The cerebellum mediates posture and balance by integrating input from vestibular, visual, and somatosensory systems. The brain’s cortical centers control voluntary motor function.
Proprioception can be evaluated qualitatively by analyzing joint position sense as detected by the technique of reproduction of passive positioning and by assessing the threshold to detect passive motion. 35,38,40 The threshold to detect motion quantifies one’s ability to consciously detect motion whereas with reproduction of passive positioning the subject merely reproduces the position of the joint as previously placed by the tester.
Motor control (functional joint stability) can be evaluated by assessing balance. Balance is the process of maintaining the center of gravity within the body’s base of support. 43 Berg et al 8 defined balance in a broader sense as including the ability to maintain a position, the ability to voluntarily move, and the ability to react to a perturbation. Riemann and Guskiewicz 46 used the term postural equilibrium to define the balanced state of forces and moments acting on the body’s center of mass. To achieve balance, the body must maintain the center of gravity through equalization of forces and optimal alignment of joint segments. One means of evaluating balance is by quantitating postural sway either on a static or unstable force plate and recording sway in degrees per second. Insufficient neurologic input or improperly processing that input at either the spinal, brain stem, or cognitive centers results in an inadequate response by the motor system and can result in injury. A Charcot joint is an example of the extreme state of joint destruction resulting from insufficient sensory input.
Neuromuscular Control in Conditioning and Rehabilitation Programs
The concept of doing proprioceptive exercises to restore neuromuscular control initially was introduced in rehabilitation programs. It was thought that because ligaments housed mechanoreceptors, an injury to a ligament would alter afferent input. 36,39 Training, after an injury, would be needed to restore this altered neurologic function. More recently, neuromuscular conditioning techniques have been advocated for injury prevention. 12,25,27
To enhance proprioceptive mediated neuromuscular control, structured conditioning and rehabilitation programs in sports need to address all three levels of motor activation within the central nervous system. 10 Reflexes emanating from the spinal cord potentially can be improved by activities that necessitate reflex neuromuscular controlled response to sudden alterations in joint positioning. Postural exercises enhance motor function at the brain stem level. Repeating motor patterns to convert conscious to unconscious motor patterns also is helpful in improving neuromuscular control and feed forward processing. Feed forward processing refers to the theory that fast movements can be controlled by events previously encountered by the neuromuscular system regarding the event (advanced information or preparatory activities). The length of reaction time indicates that motor activity cannot be undertaken solely in response to environmental stimuli. To prevent injury, motor programming, a stored set of muscle commands that allows for the initiation of activity on exposure to the unfolding event, must occur. 39 Such repetition of tasks also permits the cerebral cortex to determine the most effective motor pattern for that task and potentially decrease the response time.
Isokinetic exercises can be done to enhance joint position sense such as placing the athlete’s extremity in a predetermined position and asking the athlete to reproduce this position, initially with the eyes open and then with the eyes shut to block visual cues that might aid in neuromuscular control. Improving the sense of joint motion (kinesthesia) also can be done by initiating motion in the athlete’s joint at various positions within normal the range of motion (ROM). This can be done manually or with specialized equipment. The athlete, blindfolded or with the eyes closed, signals when he or she feels the joint being moved.
Although many companies now sell fairly complex computerized equipment to help improve proprioceptive input and balance, such training also can be accomplished through various simple drills done on various surfaces with eyes open and eyes shut, progressing from a double to a single limb stance. 46
Plyometric exercises that incorporate an eccentric preload (a quick eccentric stretch) followed by a forceful concentric contraction, a combination of events used frequently in sports (the jump and the throw) also are being investigated for injury prevention. This exercise technique is thought to enhance reflex joint stabilization and may increase muscle stiffness. It has become increasingly popular as an example of a neuromuscular control exercise that integrate spinal and brain stem levels and has been an effective addition to upper and lower extremity conditioning and rehabilitation programs. 39,55
The final phases of any functional rehabilitation or conditioning program must include activities that mimic those the athlete does in day to day sports; this specificity of training improves feed forward mechanisms and reflex and consciously controlled motor functions. 10,37,39,55
In constructing programs for conditioning and rehabilitation, one should incorporate exercises that improve joint position sense, increase awareness of joint motion, enhance dynamic joint stability, and improve reactive neuromuscular control, advancing such exercises to functional sport specific activities in the final phases of the program. 10
One of the first to recognize the importance of afferent input in neuromuscular control and the significant consequences that result when such input is disrupted was Freeman in 1965. 14 He proposed the concept of functional joint stability being frequently independent of mechanical stability. He analyzed 62 previously asymptomatic patients who initially presented with an injury to the lateral ankle ligaments. Only in seven of the 24 patients who had functional instability after 1 year, did he find a possible mechanical reason for their complaints.
Freeman attributed this functional instability for the “tendency of the foot” to give way to an “unknown pathologic process” and in a subsequent article it was proposed that an articular deafferentiation is sustained at the time of injury leading to “motor incoordination” or functional instability on the basis of inadequate proprioceptive input for proper neuromuscular control. He proposed that not only must one treat the mechanical cause of instability, but rehabilitate the injured ankle to improve not only the ROM and strength but also to restore the ability to balance. 15
To this end, Freeman had patients train initially on a flat board with a block underneath that permitted side to side motion, but then advanced them to a board with a spear underneath necessitating balance be achieved at a wide variety of ankle angles. He also had patients train on both legs, and then one leg and concluded that patients trained with such exercises had less functional instability than patients not trained in this manner. He thought this was attributable to improvement in proprioceptive defects. Others have substantiated these findings although some controversy still exists. 9,17,26,28,45,47
If exercises to enhance proprioception can improve functional stability after an injury, it seems logical that such programs enhancing detection of foot motion and making postural adjustments, also should be appropriate in initial conditioning programs to prevent ankle injuries. Balance training begun on a flat board, advancing to a wobble board, and then to an unstable surface such as a foam pad, now is advocated by several authors as an essential component of conditioning. 33,45,47 Exercises can be done initially with two legs and then with one leg, and with the eyes open followed by the eyes closed. The athlete also should be encouraged to practice balancing after single hop drills and progress to various patterns of hopping on stable and unstable surfaces, first with both legs, then with one leg, and with the eyes open followed by the eyes closed.
Whether such training improves afferent input, motor output, or the coordinated processing of same in the uninjured athlete is not clear. However, currently, several authors would agree that although the specifics of how balance and agility training improve functional stability are not clear, such exercises should continue to be an essential part of athletic training, conditioning, and rehabilitation programs. 13,18,20,25,27,33
The anterior cruciate ligament, the ligaments of the ankle, has mechanoreceptors within it. 3,5,32,44,48,49 After injury to the anterior cruciate ligament, proprioceptive defects have been reported. 4,34 Reconstructing the anterior cruciate ligament seems to improve afferent input needed for functional joint stability, and histologic studies have shown a repopulation of mechanoreceptors in anterior cruciate ligament graft tissue. 6,19,38
Exercises to enhance motor control therefore are essential after an anterior cruciate ligament reconstruction. In the past several years, there also has been a heightened awareness of the need for preseason sport conditioning to focus on lower extremity balance and conditioning in an attempt to diminish the incidence of knee ligament injuries. A significant number of noncontact anterior cruciate ligament injuries occur in athletes who have pursued a traditional program of developing muscle strength, endurance, and flexibility. 1 One of the proposed causes for such a high injury rate in athletes considered to be wellconditioned is thought to be the lack of adequate neuromuscular training. 20,27,41 Landing, cutting, and stopping in an off balance position with the hip and knee extended, can result in an anterior cruciate ligament injury. 21,31,41 Therefore, neuromuscular training incorporating plyometrics and agility drills and stressing the need for proper technique for pivoting, stopping, and landing, has been advocated to decrease the incidence of anterior cruciate ligament injuries particularly in women athletes. 21,24 Existing programs based on these principles have been tried with early success including the Henning Program, 21 the Sportsmetrics Program, 24,25 the Caraffa Program, 11 and the Santa Monica Program (oral and written communication, B Mandelbaum, MD, 2000).
The program of Griffis et al 21 is based on the “quad-cruciate interaction.” When the knee is straight during weightbearing, the anterior cruciate ligament acts as a major restraint of forward movement of the tibia on the femur. However, when the knee is near full extension, a powerful quadriceps contraction can strain the anterior cruciate ligament. If the quadriceps contracts when the knee is flexed 60° or more, the anterior displacement of the tibia on the femur and, therefore, the anterior cruciate ligament is less. As a result, drills were in which athletes practiced neuromuscular control when stopping quickly, cutting, or landing in a position of hip and knee flexion with the body balanced over the lower extremity. To meet this end, athletes do drills changing three components: the “plant and cut” was changed to an accelerated rounded turn in a bent knee position, straight knee landings to landings with the knee bent, and one step stops with the knee extended to multiple step stops with the knee bent. Preliminary data from Division I basketball players during a 2-year period showed an 89% decrease in anterior cruciate ligament injury when players practiced his prevention techniques. 21
The program of Caraffa et al 12 is a five-phase proprioceptive program based on increasingly difficult skills done initially without a balance board and progressing through a series of balance boards of various design. Athletes participate in the program 20 minutes a day beginning 30 days before the beginning of the season. In early limited trials, injury reduction from 1.15 injuries per team in the untrained groups to 0.15 injuries per team in the trained group was seen.
The Sportsmetrics program developed in Cincinnati is a three-part prevention program consisting of stretching, plyometrics, and strengthening drills designed to address potential deficits in the neuromuscular strength and coordination of the stabilizing muscles about the knee. 25 Early trials of this program showed a marked reduction of severe knee injuries in the trained group. 24 Additionally, athletes trained with this program had a decrease in peak landing forces, a decrease in varus and valgus movements of the knee, and an increase in hamstring power and strength, and an increase in hamstring to quadriceps peak torque ratios. 25
Recently, a sport specific anterior cruciate ligament neuromuscular prevention program was developed on the West Coast and currently is being field tested. (written communication, B Mandelbaum MD, 2000). This five-part program is designed to help improve strength, flexibility, injury awareness, plyometrics, and agility skills. Emphasized throughout the program is the use of proper form and technique. Athletes are encouraged to keep their hip and knee bent and the body balanced over the lower extremity while cutting, pivoting, and stopping.
Several other anterior cruciate ligament prevention programs also are being developed. Most aim at increasing injury awareness and enhancing neuromuscular control through agility and proprioceptive drills. More data are needed to ascertain the essential elements necessary for a reliable, easy to implement, and effective anterior cruciate ligament prevention program.
As in the ankle and knee, the shoulder ligaments and capsule have been found to enhance dynamic joint stability through static stabilization of the joint and through serving as a source of afferent input for muscular reflex arcs needed to protect the joint. 37,40
In 1995, Guanche et al 23 showed the neurologic function of the capsule and ligaments about the shoulder when reporting a reflex arc from the mechanoreceptors in the glenohumeral capsule to the surrounding muscles controlling this joint in the feline. Stimulation of the anterior and inferior axillary articular nerves elicited electromyographic activity in the biceps, subscapularis, supraspinatus, and infraspinatus. Stimulation of the posterior axillary nerve elicited electromyographic activity in the acromiodeltoid muscle.
Since then, others have shown that capsuloligamentous injury as sustained in traumatic anterior shoulder dislocation results in sensory deficits. 37,40,51,57 Lephart and coworkers 40 reported that surgical stabilization of previously dislocated shoulders normalizes proprioceptive awareness as detected by reproduction of passive positioning and threshold to detect passive motion techniques.
However, Tibone et al 52 found no significant difference between the reflex arcs of patients with clinically stable and unstable shoulders, suggesting that in anterior dislocation of the shoulder, the neurologic elements do not undergo gross injury. They recorded somatosensory cortical evoked potentials using scalp electrodes after stimulation of the inferior glenohumeral ligament, the middle glenohumeral ligament, subscapularis, biceps tendon, supraspinatus rotator cuff capsule, glenoid labrum, and humeral head with a monopolar electrode probe found no difference between normal shoulders, shoulders with anterior instability with a Bankart lesion, and shoulders with anterior instability and a loose capsule. This would suggest therefore, that capsular laxity, not trauma to the mechanoreceptors, alters proprioceptive responses leading to functional instability after anterior shoulder dislocation.
There is some evidence that exercises that address neuromuscular deficits improve functional stability of the shoulder. Core strengthening and flexibility exercises for scapular stabilizers and the muscles of the glenohumeral joint are an initial step in rehabilitation and conditioning programs, but these must be followed by exercises that enhance proprioceptive function reestablishing neuromuscular control. 37,53,54 Such programs, just as seen in the ankle and knee, must integrate peripheral somatosensory, visual, and vestibular afferent input and improve motor control through spinal reflex, brain stem, and cognitive programming.
Joint position sense in the shoulder can be accomplished through the use of the isokinetic dynamometer or by active and passive repositioning of the shoulder with the aid of the therapist. 53 Weightbearing on unstable platforms (partially inflated balls, foam pads, or wobble boards) enhances reactive neuromuscular control. 39 Additionally, the unstable platform provides sudden unpredictable changes in position and altered loads on the joint. These exercises can be done with the athlete prone on the floor or up on his or her toes with arms extended. Initially balancing can be done on both hands eventually progressing to having only the injured extremity on the unstable surface. 37
As with the ankle and the knee, plyometric exercises are added after near-normal strength in all targeted muscles has been achieved. In the shoulder, plyometric exercises frequently are done using balls of known weight, thrown or bounced and caught at various angles using stable and unstable rebounding boards or tossed in a various angles and at varying speeds by a therapists. 54 Finally, functional activities using motor patterns specific for the sport are added to improve feed forward processing and reflex and cognitive control. 42
The current article is an introduction to the concept of neuromuscular control and functional joint stability as components of conditioning and rehabilitation programs for sports. It also is intended to remind those involved in sports, either as participants or as directors of conditioning and rehabilitation programs, that, to prevent injuries in sports, one must think more broadly than merely developing strong, flexible, powerful, and enduring muscles; one must add to the athlete’s traditional training, conditioning, and rehabilitation program, activities to improve neuromuscular control and therefore, functional joint stability.
The concept of improving proprioception and neuromuscular control to prevent injuries is not unique to sports. Multiple studies have shown age-related alterations in propioception 7,50 and some authors think that impaired proprioception may be a contributing factor to falls in the elderly. 30,44 Computerized balance training has been found to improve postural stability in elderly individuals 56 as has postural control exercises. 29 More data are needed on this intriguing association.
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Maureen A. Finnegan, MD—Guest Editor