Paradoxical Muscle Movement during Postural Control IAN DAVID LORAM1, CONSTANTINOS N. MAGANARIS1, and MARTIN LAKIE2 1

Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Manchester, M1 5GD, UNITED KINGDOM; and 2Applied Physiology Research Group, School of Sport and Exercise Sciences, University of Birmingham, B15 2TT, UNITED KINGDOM

ABSTRACT

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LORAM, I. D., C. N. MAGANARIS, and M. LAKIE. Paradoxical Muscle Movement during Postural Control. Med. Sci. Sports Exerc., Vol. 41, No. 1, pp. 198–204, 2009. Undisturbed human standing is primarily characterized by sway of the whole body about the ankle joints and is regulated primarily by the calf muscles. Traditionally, in accord with normal ideas of postural control, ankle stiffness, enhanced by spindle mediated muscle stretch reflexes, has been considered to be important for maintaining the upright human stance. This idea predicts that during forward sway, the calf muscles are stretched and the mechanoreflex response enhances muscle activity to maintain posture and balance. Muscle contractile displacement is expected to be positively correlated with bodily sway. However, recent experiments have revealed problems with these ideas. Using a new ultrasound technique for viewing and measuring the dynamic contractile displacements of the calf muscles, it has been shown that calf muscle movement is usually poorly or negatively correlated with bodily sway. The shortening of the contractile tissue during forward sway and vice versa is described as paradoxical muscle movements. This paradoxical muscle movement can be explained by the fact that the Achilles tendon, which transmits the calf muscle force, is compliant in relation the bodily load. There are two main consequences of the compliant Achilles tendon. First, the body is unstable: it cannot be stabilized by intrinsic ankle stiffness alone and thus requires modulation of muscle activity to maintain balance. Second, contractile displacement is mechanically decoupled from bodily sway, which implies that stretch-reflex mechanisms mediated by the calf muscle spindles are unable to successfully modulate muscle activity to maintain balance. This leaves uncertain the postural role of the numerous calf muscle spindles: it is predicted that they signal the effective motor output rather than bodily sway. Key Words: HUMAN STANDING, STRETCH REFLEX, SOLEUS, GASTROCNEMIUS, ULTRASONAGRAPHY, POSTURE

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different pathways are more or less influential in their relative contribution: the nervous system tends to inhibit those pathways that are inappropriate for the task (5,33). Undisturbed, quiet, human standing is primarily characterized by small sways of the whole body about the ankle joints, and forward toppling of the body is regulated primarily by the calf muscles (12,25). To gain information regarding the control of human balance, it is normally necessary to disturb the process is some way such as by rotating or translating the platform on which the person is standing. Experiments of this kind have supported the traditional idea that during quiet standing intrinsic ankle stiffness is quite high: in fact, historically intrinsic stiffness was thought to be high enough to maintain stability in the presence of the small sways of quiet standing (14,15,33) that are usually a few tenths of a degree. Experiments of this kind, with larger disturbances, normally stimulate shorter latency, peripheral feedback processes such as muscle stretch (33), and vestibular mediated reflexes (1,2,6) that provide rapid responses that are necessary to maintain balance. In so far as the ankle rotation is relevant to the maintenance of balance, the functional muscle stretch reflex mediated by the muscle spindle has a central role in enhancing and sustaining the short-range intrinsic stiffness to maintain the upright configuration (1,33,38). In combination with similar experiments, often on cats (18),

he human nervous system is complex in that there are parallel pathways available for controlling posture, balance, and movement. In a simplified conception, posture (configuration) is maintained by inner, middle, and outer control loops consisting of intrinsic joint stiffness, peripheral reflexes, and central voluntary pathways. The inner pathways, for example, intrinsic joint stiffness, generally act immediately, over a limited range of movement (13,27); the middle pathways, for example, muscle stretch (9,33) and vestibular (1,2,5) reflexes, act with shorter latency via lower-level peripheral feedback loops; and the outer pathways, for example, centrally mediated voluntary control, act with longest latency, greatest flexibility, and greatest accuracy. Depending on circumstances, these

Address for correspondence: Ian David Loram, Ph.D., Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Manchester, M1 5GD United Kingdom; E-mail: [email protected]. Submitted for publication November 2007. Accepted for publication January 2008. 0195-9131/09/4101-0198/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2008 by the American College of Sports Medicine DOI: 10.1249/MSS.0b013e318183c0ed

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In an early series of experiments (21), we applied very small rotations to the ankle joint while participants were standing naturally or balancing an equivalent inverted pendulum using their feet. These ankle rotations were much smaller (0.055-) than perturbations used to challenge balance (typically 0.5-–10-) (34,39) and were intended to measure the intrinsic ankle stiffness applicable to the small sways (mean 0.13- [25]) of quiet standing. Intrinsic stiffness is created by the muscles and ligaments surrounding the joint and is the stiffness that does not depend on reactive, neural modulation. It is defined as the mechanical change in joint moment per unit change in joint angle. The key question was whether the intrinsic ankle stiffness was sufficient to stabilize the human inverted pendulum such that neural modulation is not required to maintain balance. Understanding this question requires some knowledge of the inverted pendulum model. For an inverted pendulum (Fig. 1C), the gravitational moment changes approximately linearly for small angular deviations (less than 5-) from the mean position. The ratio of change in gravitational moment to change in angle (the gravitational toppling moment per unit angle) is a constant known as the load stiffness (10), which depends on the mass (m), height of center of mass (h) of the participant, and the gravitational acceleration (g) where load stiffness = mgh. If the intrinsic ankle stiffness is greater than the load stiffness, then for small sways the mechanical restoring moment is greater than the gravitational destabilizing moment

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there has been a prevailing traditional view that appropriately tuned peripheral feedback processes including muscle stretch reflexes are central to postural regulation (7–10,18, 35,36). It has been assumed that this applies to the modulation of calf muscle activity during normal, human standing (7–10,12,36,37). For a standing human, when the supporting platform is translated, for example, backward, the ankles are dorsiflexed, the calf muscles are stretched, the sensory organs in the muscles (spindles) register elongation of contractile tissue, and the spindles appropriately stimulate increased calf muscle activity (33,39). Likewise, when a forward acting disturbance is applied at waist level, the body is pulled forward, the ankle is again dorsiflexed, the calf muscles are stretched, and the muscle spindles simulate increased muscle activity. It has been assumed that the same relationship between ankle angle and muscle length applies during natural standing. The assumption is that as the person sways forward, the calf muscles are elongated, and as a person sways back to the vertical, the calf muscles are shortened, thus providing the appropriate stimulus for the mechanoreflex mechanism. This article summarizes a series of observations (3,21–25, 27,28) which show that unlike the perturbation experiments described above, during undisturbed standing calf muscle contractile length is not driven by bodily sway, and hence it is predicted that the calf muscle spindles do not register bodily sway. Rather, the calf muscles actively generate the necessary tension via a compliant Achilles tendon and therefore contract paradoxically. Rather than being a mechanical signal that conveys bodily sway, active contractile displacement reflects balance-related modulation of muscle activity. Thus, for humans, normal standing balance is unlikely to utilize the generic stretch-reflex mechanism.

EXPERIMENTAL METHODS The upright human configuration is well described as having a high center of mass in relation to a small base of support and a multijointed structure. Controlling this structure in movement and posture is a complex process, neurologically and biomechanically. It is clear that the ankle mechanisms and the ankle strategy are only a small part of the wider process of maintaining balance (1,4). Nonetheless, in an attempt to investigate underlying principles, we have found it helpful to reduce the upright human balance problem to a simpler problem in which rotation occurs about only one joint, the ankle joint, and in which only one muscle group, the agonist calf muscles, is actively involved in the process of maintaining balance (Fig. 1). Hence, we have investigated either human balancing of a real inverted pendulum using the feet (20–22) (or hands) (16,17,19) or quiet, unperturbed standing (21,23–25), where bodily sway can be closely approximated by the inverted pendulum model (12,40) that portrays standing as bodily rotation solely about the ankle joint.

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FIGURE 1—Anatomy of human standing. A, The calf muscles soleus and gastrocnemius connect the Achilles tendon to the back of the lower leg bones and the back of the knee respectively. B, Sonograph of the gastrocnemius medialis and soleus muscles taken from the medial aspect. Proximal aponeurosis of gastrocnemius medialis (A), distal aponeurosis of gastrocnemius (B), distal aponeurosis of soleus (C), and proximal aponeurosis of soleus (D). Panels B and C are morphologically distinct but moved as a unit and were tracked using a single set of markers. The size of the image is 4.5  4.5 cm. C, The body is represented by an inverted pendulum with its center of mass (CoM) indicated. For simplicity, the gastrocnemius and soleus muscles together are represented by a single, uniarticular contractile element (CE). These muscles act through a spring-like element that connects them to the ground through the foot. The total stiffness of this elastic link is represented by K. The system operates by dynamically altering the length of the CE, thus altering the position of the proximal end of K. Reproduced with permission from Blackwell Publishing, Oxford; Figure 1 (24).

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and neural reaction is not required to maintain balance. If the intrinsic ankle stiffness is less than the load stiffness, then neural reaction is required to modulate the ankle moment appropriately to maintain balance. The results (below) from these experiments led us to predict that the calf muscles, that is, the contractile tissue, were not behaving in an orthodox manner during human standing. It was predicted that rather than lengthening during forward sway and shortening during sway back to the vertical (orthodox muscle movements), the opposite was happening; namely, the contractile tissue was shortening during forward sway and lengthening during backward sway (paradoxical muscle movements). At the time, it was unknown whether this prediction was correct. Verification required observation and recording of small displacements of contractile tissue during postural sway. Ultrasound imaging of muscle and tendon was well established as a technique for measuring displacements in

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FIGURE 3—Involuntary postural sway. Shown are records of a subject standing quietly and symmetrically with eyes open. A, Combined ankle torque from both legs. B, Left ankle angle (solid ) and estimated COM angle (dotted ). C, Muscle length, gastrocnemius medialis (solid ) and soleus (dotted ). D, Predicted changes in muscle length using the dynamic bias model with moment arm of 5 cm and best fit stiffness of 48%. E, integrated EMG, gastrocnemius medialis. F, Integrated EMG soleus. For both EMG, T = 200 ms. The increase in angle and torque corresponds to forward sway. Muscle lengths are shown relative to typical mean muscle belly lengths of 320 and 220 mm, respectively, for soleus and gastrocnemius. Reproduced with permission from Blackwell Publishing, Oxford; Figure 2 (24).

FIGURE 2—Exaggerated sways. Slow continuous sways of representative subject showing ankle angle (A), left ankle torque (B), muscle length (C ), gastrocnemius medialis (solid ) and soleus (dotted ), and integrated EMG (D), gastrocnemius medialis (solid ) and soleus (dotted ). For all EMG, T = 100 ms and the background noise signal is around 0.04 V. The increase in angle and torque corresponds to forward sway. Muscle lengths are shown relative to typical mean muscle belly lengths of 320 and 220 mm, respectively, for soleus and gastrocnemius. Reproduced with permission from Blackwell Publishing, Oxford; Figure 2 (23).

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tendon attachments during changes in static load and thus for establishing the length-tendon properties of tendon and aponeurosis (29–32). Although it was possible to measure large changes in muscle fascicle length occurring for example during gait (11) or caused by changes in static load (29), there was no technique for measuring contractile displacements barely visible or invisible to the human eye or for tracking those changes through time. To solve this problem, we developed a simple, automated method for calculating changes in contractile displacement of the soleus and gastrocnemius muscles from the videos acquired using an ultrasound scanner (23,26). We used this technique initially to observe contractile displacements during exaggerated standing sways (23) in which the ultrasound tracking could be verified visually and in which the main prediction of paradoxical muscle movements could be tested. Subsequently, we verified this tracking technique

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FIGURE 4—Correlation between muscle contractile length and body sway. All three panels show the normalized cross-correlation function between CoM angle and contractile length. The cross-correlation function shows the correlation between these two signals at different values of time shift between the two quantities. A positive time shift would indicate that the muscle length was in advance of the CoM angle. A, Soleus contractile length. B, Gastrocnemius medialis contractile length. C, Predicted correlations using the dynamic bias model. Predictions are for spring stiffness expressed relative to the toppling torque per unit angle of the pendulum (load stiffness). The values are 60%, 80%, 90%, 100%, 110%, 120%, and 160%. Reproduced with permission from Blackwell Publishing, Oxford; Figure 3 (24).

for very small contractile displacements (26) and used the technique to observe the largely invisible contractile displacements during involuntary postural sway to test whether the prediction of paradoxical muscle movements was correct (24,25).

Intrinsic ankle stiffness is insufficient for stability. By applying very small ankle rotations to standing subjects, we established that the intrinsic ankle stiffness was on average slightly less (mean T SD = 91% T 23%) than the load stiffness of the human inverted pendulum (21). This means that when the human sways slightly forward, the mechanical increase in ankle moment that occurs without neural modulation does not match the increase in gravitational moment. Thus, the human is biomechanically unstable. Without appropriate modulation of muscle activity, balance would not be possible. Using a simple conception of the calf muscles as a contractile tissue component in series with an elastic tendon (Fig. 1C), the stiffness of the two parts cannot exceed the stiffness of the most compliant element. The measured intrinsic ankle stiffness changed only weakly with ankle moment, which was more consistent with tendon than active muscle. We concluded that the ankle stiffness was determined by the passive series elastic component of the calf muscles, namely, the Achilles tendon in series with the foot (21). As we explain below, this implies that to generate sufficient tension in the compliant tendon to support the human inverted pendulum, the contractile component

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EXPERIMENTAL EVIDENCE

has to be shorter to support the human at more forward angles and be longer to support the human at angles closer to the vertical (24). Paradoxical muscle movements are the shortening of the calf contractile tissue as the person sways forward and vice versa. Paradoxical muscle movements during exaggerated standing sways. Using ultrasound analysis of the contractile displacements, we observed subjects performing slow, inverted pendulum-like sways of several degrees forward from and back to the normal standing position. As predicted, the calf muscles contractile tissue shortened several millimeters during forward sway of 3and lengthened during backward sway (Fig. 2) (23). This confirmed that the participants were generating active tension through an Achilles tendon that was less stiff than the load stiffness of the human inverted pendulum. Paradoxical muscle movements are the norm during involuntary standing sway. Subsequently, we observed participants standing normally and performed ultrasound analysis of the contractile displacements associated with involuntary standing sways (Fig. 3) (24). Normal standing is typically associated with unidirectional sways of a few tenths of a degree over a duration of a few seconds (25) and with positional drift of up to a degree over a duration of 35 s (Fig. 3B). This low-frequency drift is associated with paradoxical changes in contractile length such that the contractile tissue lengthens as the person sways back to the vertical (Fig. 3C). Generally, the sway pattern is associated with a corresponding paradoxical (negatively correlated) pattern of contractile displacement although the higher frequency content of

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contractile displacement is more pronounced than the sway pattern (Fig. 3C). The fluctuations in contractile displacement can be predicted using the simple model of a compliant Achilles tendon in series with an actively modulated tension generating muscle, and it can be seen that this simple model captures the contractile displacements surprisingly well (Fig. 3D). The fluctuations in contractile displacement are highly correlated with the fluctuations in muscle activity (Fig. 3C vs. Figs. 3E and 3F), reflecting the fact that the contractile displacements are a consequence of active modulation of muscle activity (24). In general, the soleus contractile displacement is negatively correlated with bodily sway, and the correlation ranges from low to strongly negative (Fig. 4A). Gastrocnemius contractile displacement is usually negatively correlated with bodily sway, ranging from weakly positively correlated to strongly negatively correlated (Fig. 4B). Paradoxical muscle movements are the norm during standing postural sway, meaning that generally, calf muscle displacements are negatively correlated with bodily sway. This contrasts with the orthodox expectation that muscle displacements are positively correlated with bodily sway. Paradoxical muscle movements are consistent with a simple model in which the calf muscles generated the active tension necessary for bal-

FIGURE 5—Consequences of reducing ‘‘tendon’’ stiffness. A large inverted pendulum (P) was supported on ball races mounted on a very substantial trunnion (Tr). Pendulum inclination was measured by a Hall effect potentiometer attached to its base. End stops (not shown) limited its range of movement. The subject controlled the pendulum by flexion/extension movements of the forearm. The upper arm was secured in a cradle (C). The forearm was coupled to the pendulum by an armlet (A), which was linked by an adjustable spring (K) to a load cell (LC) mounted on the pendulum rod. Arm movement was recorded by an infrared optical rangefinder (R), which was aimed at a lightweight reflective target (Ta). A positive signal was produced by a rise in force and by a movement toward the right in this figure of the hand and pendulum. Reproduced with permission from Blackwell Publishing, Oxford; Figure 1 (16).

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ance through an Achilles tendon that is less stiff than the load stiffness of the human inverted pendulum (Fig. 4C) (24). DISCUSSION To understand the cause and implications of the paradoxical muscle movements, we constructed an analog experiment in which participants manually balanced a real inverted pendulum via a compliant linkage (Fig. 5) (16). The real inverted pendulum represents the human body. The spring represents the Achilles tendon in series with the foot. The hand represents the contractile tissue. Hand movements toward the pendulum represent contractile lengthening, and the pendulum shown topples to the right (Fig. 5). The stiffness of the spring was varied from very stiff (746% of load stiffness) to very compliant (58% of load stiffness). The appropriate stiffness for a standing human is thought to be around 80–95% mgh (21,24,25,28). In this analog experiment, sway of the pendulum stretches the ‘‘tendon’’ via the distal attachment of the ‘‘tendon.’’ When the ‘‘tendon’’ is very stiff (746%), the hand is mechanically tightly coupled to the pendulum, and hand movements are mechanically constrained to reproduce pendulum sways while the subjects modulates the tension required to maintain balance (Fig. 6A) (16). This represents the orthodox expectation for normal standing and reality of platform translation experiments that contractile displacements are positively correlated with bodily sway. When the ‘‘tendon’’ stiffness is reduced (249%), the hand is mechanically less coupled to the pendulum (Fig. 6B). Sways of the pendulum do not dictate hand movement because the stiffness of the ‘‘tendon’’ is now less than the intrinsic stiffness of the hand–arm–elbow. Hand movements are more determined by voluntary command independent of pendulum movement. However, because, the ‘‘tendon’’ stiffness is greater than the load stiffness, generating appropriate ‘‘tendon’’ tension to balance the pendulum will cause the hand movements to be positively correlated with the pendulum at low frequency. When the ‘‘tendon’’ stiffness is 100%, that is, equal to the load stiffness, sway of the pendulum stretches the ‘‘tendon’’ and causes changes in ‘‘tendon’’ tension that (after converting to moments) equal changes in gravitational moment. For small oscillations, no hand modulation of spring tension is required: the system is stable—although at the limit of stability. Moreover, pendulum sways do not cause the hand to move because the spring is much less stiff than the intrinsic hand–arm stiffness. Thus, the participant cannot register pendulum movement via pendulum imposed movement of the hand (although they may be sensitive to an increase in tension in the spring). For human standing, this represents the case of limiting stability beyond which neural modulation is required to correct even small bodily sways. Moreover, it is also the case, and perhaps surprising to many, that during involuntary standing sways, the tendon stiffness is much lower (10 times lower [28]) than the intrinsic stiffness

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FIGURE 6—Representative traces from one subject. Each record is 10 s long. The records are of pendulum position, hand position, and force with springs of four different relative stiffness: 746% (A), 249% (B), 94% (C), and 58% (D). The increase in pendulum position and hand position corresponds to the movement of the pendulum and hand away from the body of the subject. Force represents the tension in the spring. The gain is identical in all records to facilitate direct comparison. The movement of the pendulum is generally less with the greatest intrinsic stiffness. The pendulum and the hand move mainly in phase in panel A and in antiphase in panel D. The force record reflects both pendulum position and hand position. Force is clearly predominantly in phase with pendulum position. Movements of the hand are more frequent than movements of the pendulum. Reproduced with permission from Blackwell Publishing, Oxford; Figure 3 (16).

with bodily sway are a consequence of the fact that the nervous system has some other source of information regarding body position and is successfully maintaining balance. In conclusion, these observations of paradoxical muscle movements in soleus and gastrocnemius demonstrate that the standing human is biomechanically unstable, thus requiring appropriate modulation of muscle activity that in turn requires knowledge of bodily sway. These observations and subsequent analysis also lead to the prediction that the calf muscle spindles do not register bodily sway during undisturbed quiet standing; rather, they register the effective motor output, a kind of ‘‘efference copy,’’ of the neural controller. Thus, the generic, autogenic stretch reflex is not useful to maintain normal human standing. Moreover, because the ankle muscles alone can provide bodily sway information (7), the proprioceptive source of this information is an open question. Are these conclusions specific to standing or are they more general? We think that generally, spindle registration of joint movement is disadvantaged by high tendon compliance and that this is exacerbated when the load is unstable. The results reported in this article do not constitute endorsement by ACSM.

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of even passive muscle, and thus sways of the body produce negligible effect on contractile displacement in relation to the neurally modulated changes in contractile length. Thus, bodily sways are predicted to be invisible to the calf muscle spindles. When the spring stiffness is reduced to 94% (Fig. 6C), the hand movements are uncorrelated with pendulum position such that the increase in pendulum angle shown is not associated with a corresponding change in hand position. Rather, changes in hand position reflect the voluntary modulation involved in maintaining balance. When the spring stiffness is reduced to 58% (Fig. 6D), generating the ‘‘tendon’’ tension necessary to maintain balance causes the hand position to be strongly negatively correlated with pendulum position. Note that this negative correlation between active hand movements and pendulum position is not a mechanical consequence of pendulum movements. Visual knowledge of pendulum position is required to produce the correct spring tension required for balance (16,17), and a consequence of the ‘‘tendon’’ stiffness is that hand movements are negatively correlated with pendulum position. By analogy, for human standing, it is predicted that bodily sway cannot be registered from the changes in calf muscle contractile length. The paradoxical muscle movements that are negatively correlated

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