Neuromuscular training focuses on improving movement patterns, muscular recruitment, balance, proprioception, and agility. Coupled with strength training, it is a prevalent method used in rehabilitation and injury prevention (4,5,9,10,35,49,50). Research findings on neuromuscular training demonstrate reduced lower extremity ligament injury rates (9,10,32,44,46), improved movement biomechanics (5,43), dynamic balance (34), and functional status (34). One type of neuromuscular training is perturbation training or the use of controlled, unpredictable, and multidirectional forces to disturb balance. This article will focus on surface perturbation training, which involves directing forces to unstable surfaces (13,22,35). Perturbation forces can be applied during gait and bilateral or unilateral stance and through a variety of mediums, including rocker boards and roller boards. Rehabilitation professionals and strength and conditioning coaches can perform this training in a clinical or team practice setting.
In essence, perturbation training is an advanced form of balance training. The human body continuously combines the input of 3 sensory systems to maintain balance (25,28). With perturbation training, the somatosensory, vestibular, and visual systems are all challenged; however, the visual and vestibular systems are generally not altered, and most adaptations occur within the somatosensory system. The somatosensory system consists of various receptors that detect different sensations (Table 1). A group of somatosensory receptors, termed “proprioceptors,” identify changes in joint angle, muscle length, and tension. Understanding the function of the muscle spindle, a type of proprioceptor, is important to understand the physiological benefits of perturbation training.
Muscle spindles are found in parallel with extrafusal muscle fibers. Composed of intrafusal muscle fibers, afferent nerve endings, and gamma motor nerves, the muscle spindle functions to regulate alpha motor neuron activity and participate in the stretch reflex by responding to changes in muscle length or the rate of tissue length change (41,53). With surface perturbation training, changes in the stability of the surface elicit a quick stretch to affected musculotendinous units. Upon a quick stretch, the muscle spindle receives and sends neural input in an attempt to regain stability by contraction of stretched musculature and inhibition of an antagonistic response (45). Gamma innervation sets the threshold, or sensitivity, within a muscle spindle to respond to various intensities of stretch (1). With fatigue, proprioceptive input is delayed even further, leading to a slower reaction time (10,11,54). The purpose of perturbation training is to accelerate this response. Lowering mechanoreceptors' thresholds allows agonistic musculature to be more sensitive by responding to lower unanticipated forces with a faster reaction time. This can result in a higher state of readiness to detect and respond to destabilizing forces.
These sensorimotor adaptations, as a result of perturbation training, lead to measurable physical changes. Such responses include changes in muscular cocontraction surrounding a joint (13,35), improved muscle recruitment and activation (15,35,36), and accelerated anticipatory reactions to improve an athlete's gait status (29,35) and his or her ability to return to prior sport or functional activities (22,24,30). Although most current research shows the benefits of perturbation training during preoperative care (29,30) and nonsurgical care (13,22,23) of anterior cruciate ligament (ACL) injury, it is also used as a treatment in rehabilitation settings for various knee and ankle pathologies.
The remainder of this article will focus on a description of researched perturbation techniques (22,23,35) and supplemental modifications for an athlete's rehabilitation or conditioning program. The benefits, both physiological and functional, of perturbation training will follow. Last, uses beyond ACL rehabilitation are discussed along with future research needs.
TECHNIQUES AND PROGRESSION
First described as perturbation-enhanced rehabilitation, perturbation training has been found to be effective for the treatment of athletes with ACL tears (22), also termed “ACL deficiency” by qualified rehabilitation professionals. The challenges it can present to the visual and vestibular systems and especially the somatosensory system make it an excellent option for use with athletes for rehabilitation purposes and to simulate game situations. In the subacute phase of injury, once the athlete has achieved full range of motion, 70% quadriceps strength of the uninvolved knee, no evidence of joint effusion, and the ability to hop without pain, the athlete with ACL deficiency is put through a screening examination (Table 2) (21). If the athlete passes the examination and is able to single-leg balance for more than 60 seconds, surface perturbation training can begin 2-3 times per week. The athlete should experience pain-free training without incidence of instability. If either of the previous are witnessed, perturbation training should stop or at least be reverted to the previous pain-free stage.
Unstable support surfaces, such as a roller board and rocker board, are used to elicit perturbations. There are 3 separate conditions used: the roller board in combination with a stable surface of the same height, the roller board alone, and the rocker board alone. All 3 conditions can be initiated on the same day but are progressed independently of the other based on the varying difficulties and demands of each device. Through all stages of training, verbal cues are important to remind the athlete to keep his or her knees slightly bent and abdominal and hip musculature contracted, with emphasis on “knee-over-toe” position, indicated by minimal hip adduction, internal rotation, or knee valgus (Figure 1a and 1b) (35).
Perturbations are introduced by the rehabilitation professional directly to the support surface using both hands for the roller board and either hands or feet for the rocker board. They begin as low-intensity, low-frequency forces in a direction predisclosed to the athlete. Instruction may be important for emphasis on muscular relaxation between perturbations. Perturbations can be elicited forward, backward, sideways, and in diagonal or rotational patterns while using the roller board. With the rocker board, forces are given in the degrees of freedom the board allows (either forward and backward or side to side). Typical parameters have perturbation sessions lasting for 60-90 seconds, with 30- to 60-second rest breaks for tissue recovery (22). The practitioner may vary the times to simulate specific sport activities. As the athlete's performance improves, perturbations are made more rapidly in random directions, with various amplitudes and time between perturbations.
A roller board (22,35) consists of a platform and 4 underlying wheels that swivel in all directions. In the first condition (Figure 2a), the roller board is used in combination with another stable surface of the same height as the roller board. The athlete is instructed to maintain good lower extremity alignment while using the involved extremity to hold the board in the same location while matching the force given by the professional. Overpowering the perturbation force may produce a strong cocontraction response and is therefore discouraged (23).
The second condition is the roller board without another surface (Figure 2b-d). The athlete is asked to stand with both feet on the roller board with good form and alignment. During perturbations, the athlete attempts to maintain controlled balance. Once good form is achieved without loss of balance for 90 seconds, the athlete is advanced to single-leg stance on the involved extremity.
Rocker boards, often called tilt boards, offer a different element to perturbation training and are used in the third condition (Figure 3) (23,35). The board is initially stationed for bilateral stance with freedom in the anterior and posterior directions to target stabilizing muscles in the sagittal plane. Perturbations are introduced, beginning with low-intensity forces in anticipated directions, while the athlete attempts to maintain balance. As good neuromuscular control is accomplished for 90 seconds with randomly applied perturbations, the rocker board is moved 90° and used in the medial and lateral directions. Once good dynamic stability is exhibited, the athlete is progressed to single-leg stance, with the rocker board used in both planes.
Various modifications can be made to the aforementioned progression based on the athlete's functional level and required sport skills. Of utmost importance is lower extremity alignment, especially in single-leg stance. If the athlete is having difficulty maintaining optimal alignment, tactile feedback can be introduced using an exercise band or tube to pull the knee into genu valgus (Figure 1c). The athlete is then instructed to pull his or her knee out against the resistance to the knee-over-toe position.
A scale can be used as the stable surface in conjunction with the roller board, as described in condition 1. Visual feedback of the amount of weight bearing ensures that the athlete maintains at least 50% of his or her body weight on the roller board throughout the duration of the exercise. Using decreased weight through the affected limb may lead to compensatory movement patterns, unwanted for return to sport.
Furthermore, the athlete can attempt training in all three positions with their eyes closed to remove visual input. With his or her eyes closed, training more specifically challenges the somatosensory and vestibular systems. Sport-specific tasks and eyes-closed situations can be added to the athlete's program if good form and balance are achieved with the previous progressions to simulate game situations. Activities such as throwing, catching, dribbling, and swinging are commonly used. Other training exercises such as squats and deadlifts can also be performed during perturbation training in either single- or double-leg stance. For athletes involved in contact sports such as football and basketball, perturbations directed not only to the support surface but also to the body will additionally simulate game situations. Furthermore, an athlete may be able to use the domed balance training device (Figure 4) with the stable platform up. Perturbation training on this device is significantly more challenging than rocker and roller boards because of the increased degrees of freedom in all planes.
BENEFITS OF SURFACE PERTURBATION TRAINING
Surface perturbation training is an excellent intervention for athletes recovering from an ACL injury. Research has shown that surface perturbation training improves hamstring recruitment (13,15,35,36) and decreases joint cocontractions (13,35). Improvements in instability episodes (21,24), gait mechanics (29,35), and athletes' abilities to return to sport without surgical management (22) are also seen.
To understand the effects of perturbation training, it is important to review ACL anatomy and biomechanics. Stabilizing structures at the knee joint can be thought of as either passive or active (dynamic) stabilizers. Passive stabilizers involve the capsuloligamentous structures that have no contractile properties. Dynamic stabilizers use their ability to contract and produce muscle force for stability. The ACL is the primary passive stabilizer of anterior tibial translation, providing 85% of the total resisting force (8). Assisting the ACL, the hamstrings contract to counter anterior tibial translation by 81-94%, depending on knee angle, and can be thought of as the primary active stabilizer (2). A quick strong hamstring contraction can offset tibiofemoral instability because it dynamically posteriorly translates and stabilizes the proximal tibia (5,17,39,41,48,51). On the contrary, especially at angles of less than 45° knee flexion, the quadriceps act as an active ACL antagonist, producing an anterior pull on the tibia (17,48,51). The following will review specific neuromuscular and functional adaptations as a result of surface perturbation training.
NEUROMUSCULAR RECRUITMENT AND EFFICIENCY
Perturbation training can have an important physiological effect on muscle recruitment efficiency, especially of the hamstrings (13,15,35,36). Hamstring activation opposes anterior tibial translation in an ACL-deficient knee and complements the ACL in an uninjured knee. Various studies have found quicker hamstring activation in response to unanticipated forces after perturbation training (15,35,36). A more rapid response may enhance joint stability during unanticipated forces on the playing field.
Another neuromuscular improvement is the posttraining effect on muscular cocontractions caused by injury. Cocontractions, or the simultaneous contractions of agonist and antagonist musculature, are formed as a stiffening mechanism to protect an injured joint against joint instability (13,35). Perturbation training decreases cocontractions surrounding the knee joint (13,35). Specifically, cocontractions between the lateral hamstring and the vastus lateralis decrease in response to anterior and lateral perturbing forces (13). Mild reductions are also found in the vastus lateralis and medial gastrocnemius cocontraction. As the stiffening strategy diminishes, the joint is able to obtain its normal range of motion, preferentially activate specific muscle groups, and perform more similar to a healthy knee during functional and sport activities.
GAIT MECHANICS AND STABILITY
Stiffness associated with cocontractions is seen in the gait mechanics of athletes with ACL-deficient knees and can be positively influenced by perturbation training (29,35). Before training, patients with ACL deficiency show increased stiffness with decreased peak knee flexion angles during gait (14,19,29,35). This stiffening strategy, consisting of early quadriceps activation and a prolonged hamstring response, leads to gait asymmetry and the potential for increased compressive forces in the knee, which may result in articular cartilage degeneration or osteoarthritis (14,29). Even 3 months after ACL reconstruction without perturbation training, during gait, knees rely heavily on the quadriceps in response to any unexpected perturbation (19). After perturbation training, knee flexion angles, the onset of hamstring activity, and quadriceps-hamstring balance are significantly enhanced (29,35), which leads to improved gait symmetry and functional stability.
Another common complaint during ambulation with knee pathology is knee buckling or “giving way” (22,24,41). Buckling is proposed as a subluxation of the tibiofemoral joint that results in pain and effusion and can occur in 70-80% of ACL-deficient athletes (38). In a population with ACL injuries, perturbation training coupled with strength training produces movement patterns closer to the norm than strength training alone (7). It has commonly been thought that buckling was because of joint instability and quadriceps weakness. However, neuromuscular control appears to be the main cause. Melnyk et al. (41) showed that "giving way" symptoms are more associated with altered stretch reflex excitability than mechanical instability. As previously discussed, the stretch reflex can be improved by perturbation training and appropriate athletes can reduce the incidence of buckling (21). Buckling has also been shown to be decreased after perturbation training in other knee pathologies, including osteoarthritis (24).
RETURN TO SPORTS
With improved stability and gait mechanics, athletes may be able to return to their prior level in a quicker manner. After ACL injury, the patient and his or her healthcare team must decide between surgical and nonsurgical options. At times, nonsurgical treatment may be considered advantageous. Perturbation training is an important part in nonsurgical care for an athlete looking to return to sport. Fitzgerald et al. (22) studied athletes with less than 2 incidences of knee buckling since injury, who underwent a screening examination that consisted of hop tests and functional scales (Table 2). Forty-two percent of athletes with ACL deficiency were able to pass the screening examination (21). Potential copers participated in perturbation training coupled with strength training 2-3 times per week for 5 weeks (22). Functionally, after training, participants had reduced episodes of giving out, and 92% were able to return to their prior athletic participation level compared with 50% of athletes who solely participated in strength training. This showed a positive likelihood ratio of 4.88 (22). In other words, athletes who passed the screening examination and participated in perturbation training were about 5 times more likely to return to sport than those who did not undergo perturbation training.
OTHER REHABILITATION AND CONDITIONING USES
Although effective in the rehabilitation of ACL-deficient athletes, surface perturbation training may also prove beneficial in other areas of rehabilitation and injury prevention and can be used by all strength and conditioning specialists. Perturbation training is performed in the closed kinetic chain and may affect neuromuscular control at other joints. Also, because of its effects on muscular recruitment, perturbation training may be useful for injury prevention purposes. The following will outline further uses of perturbation training, which, in the author's experience, have led to successful clinical outcomes and avenues for future research.
ANKLE REHABILITATION AND CONDITIONING
Ankle instability is caused from a combination of ligamentous laxity and articular deafferentation, which negatively impacts neuromuscular control (24). In many cases, instability may be more functional than mechanical (24). Patients with chronic instability ambulate with increased inversion of the ankle at heel strike (16) and have slower peroneal reaction time to unanticipated inversion forces (37). This can lead to further injury or repetitive sprains, especially when ambulating on uneven surfaces. Therefore, sensitizing the muscle spindle's threshold and training the limb with destabilizing forces improve the functional stability. Treatment for ankle instability often consists of closed chain strengthening and proprioceptive training (27,28). Although effective, this training is generally controlled and anticipated but not functionally consistent with return to sport.
As seen at the knee, perturbation training can help improve soft tissue reaction times to destabilizing forces (26). Single-leg balance activities with perturbations on the rocker board in the medial and lateral directions may lead to improved timing and recruitment of the posterior tibialis, peroneals, and other ankle stabilizers. Using a domed balance training device will further challenge the ankle musculature in all planes. If perturbation training improves peroneal recruitment as hypothesized, improved response time may have an effect on dynamic ankle stability and reduce injury rates of traumatic ankle sprains. When combined with sport-specific activities, perturbation training may be an excellent intervention for injury prevention of ankle ligament sprains and musculotendinous strains in high-risk sports, such as basketball and volleyball.
REHABILITATION AND CONDITIONING OF THE HAMSTRINGS
Perturbation training has a positive effect on hamstring recruitment and efficiency. Noncontact hamstring strains are a common sports injury (31,47). After hamstring strain, the injured location of the muscle shows increased scar tissue formation and overall shorter length and decreased girth of the muscle belly (6,47,52). These factors may lead to decreased force production and slower recruitment. Reduced hamstring force or slower onset can elevate the risk of injury by promoting dominance of the quadriceps, leading to increased forces pulling the tibia anteriorly. Perturbation training can help reduce these undesirable mechanics.
ANTERIOR CRUCIATE LIGAMENT INJURY PREVENTION
It is widely accepted that the etiology of ACL injury is multifactorial (3,18). Elements that play a role in ACL injury include anatomical, hormonal, environmental, neuromuscular, and biomechanical factors (42,51). ACL injury prevention should address risk factors that are modifiable. Of particular interest in looking at ACL injury rates is the elevated rate of knee ligament injuries in women compared with men. Among other factors that vary between men and women (anatomical and hormonal), neuromuscular imbalances such as quadriceps dominance, leg dominance, and ligament dominance (20) can contribute to the increased injury rate.
Quadriceps dominance is a state of imbalance during sport activities, when athletes preferentially activate the quadriceps as the primary stabilizer of the knee, and is commonly seen in female athletes (40). Women preferentially activate the quadriceps before the hamstrings compared with men (12). This underutilization of the hamstring musculature is in part because of the fact that women show less hamstring force relative to body size than men (33). Quadriceps dominance, especially in women (35) and athletes with ACL deficiency (19), leads to higher rates of injury. Efficient hamstring recruitment and force production are imperative to counterbalancing quadriceps dominance and reducing ACL injury. As previously discussed, surface perturbation training is able to impact these neuromuscular characteristics of the lower extremity.
Perturbation training for injury prevention can be used by all strength and conditioning professionals in their conditioning and prevention programs. Typically, progressions for these athletes are similar as for rehabilitation but may move faster for those without a previous injury. Perturbation training can be used in a practice environment, with ample education to all coaches and players. Teammates can pair up and perform these activities during warm-up and cool-down sessions.
Further benefits of perturbation training may be linked to effects with muscle groups other than those surrounding the knee. Proximal lower extremity musculature including the hip adductor and gluteal muscle groups should be studied. Future research should also be conducted for evidence of improvements at the foot and ankle. Furthermore, upper extremity closed chain activities on perturbed surfaces may show benefits for joint stability and rotator cuff recruitment.
Perturbation training is an excellent and simple way to rehabilitate lower extremity pathologies and may reduce the risk of athletic injuries. It can easily be incorporated into rehabilitation or practice settings. Both physiological and functional improvements have been found with perturbation training that lead to enhanced joint stability and neuromuscular control.
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