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5
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Practical Biomechanics and
Physiology of Balance
Lewis M. Nashner
INTRODUCTION
Balance is a complex process involving the coordinated activities of multiple sensory, motor, and biomechani­cal components. The position of the body in relation to gravity and the surrounds is sensed by combining visual, vestibular, and somatosensory inputs. Balance movements involve motions of the ankle, knee, and hip joints, which are controlled by the coordinated actions of ankle, thigh, and lower trunk muscles. The aim of this chapter is to describe the principal biomechanical, sensory, and motor components of balance and their interactions within a systematic model of balance con­trol. Chapter 15 describes a method for assessing the sensory and motor components of balance based on this model and provides illustrative patient examples of how the information is clinically applied.
BIOMECHANICS OF BALANCE
Definition of Balance
To balance with the feet in place, the position of the body’s center of gravity (COG) must be maintained vertically over the base of support (Gurfinkel & Ose­vets, 1972; Koozekanani, Stockwell, McGhee, & Firooz­mand, 1980; Nashner, 1981). When this condition is met, a person can both resist the destabilizing influ-
ence of gravity and actively move the COG. When a person moves slowly, the in-place limits of stability are exceeded whenever the COG position has been dis­placed beyond the perimeter of the base of support. At this point a rapid step or stumble to reestablish the base of support beneath the COG, or additional exter­nal support, is required to prevent a fall. When a per­son is moving more rapidly, the definition of balance is more complex, because momentum of the body motion must also be taken into consideration. For example, if the COG is displaced only slightly forward but moving forward rapidly, the person has lost balance because the forward momentum is sufficient to carry the COG beyond the forward stability limit.
The state of a person’s balance is most simply described in terms of angular displacement of the COG from the gravitational vertical. Center of grav­ity sway is then defined as the angle formed by the intersection of a first line from the center of the base of support through the COG and a second line extend­ing vertically from the center of support, as shown in Figure 5–1. This definition of balance pertains whether the person moves about the ankles, the hips, or both joints, as well as taking height into account (Nashner & McCollum, 1985). Thus, a given sway angle indicates a comparable state of balance for all body movement patterns and heights.
This definition of balance is further discussed in the section on limits of stability. More recent studies have expanded the definition of balance to incorporate multiple joints of the body (Maurer & Peterka, 2005).
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Figure 5–1. Center of gravity (COG) sway angle in rela­tion to the “limits of stability” cone. is moving about the ankles; the figure on the right is moving about the hips. The COG sway angles of the two figures are approximately the same, although the joint motions are much larger using the hip strategy. Filled diamonds show the body C book of Balance Function Testing, Jacobson et al., 1997.
The figure on the left
OG positions. From Hand-
Base of Support
The base of support for standing on a flat, firm surface is defined as the area contained within the perimeter of contact between the surface and the two feet. The base of support area is nearly square when the feet are placed comfortably apart while the person is quietly standing. Similarly, a diagonal stance produces a parallelogram­shaped base of support extending forward on one side and backward on the other, while a tandem stance posi­tion creates a long but very narrow base of support.
When the support surface area is smaller than the feet, or when surface irregularities limit the contact between the feet and the surface, the base of support is reduced. Standing sideways on a narrow beam, for example, provides a base with a normal width but very short length. Thus, the person’s limits of stability are effectively reduced in the anterior-posterior (AP) but not the lateral dimensions.
Limits of Stability
The limits of stability (LOS) is a two-dimensional quan­tity defining the maximum possible COG sway angle as a function of sway direction from the center position (Koozekanani et al., 1980; McCollum & Leen, 1989). The
LOS depends on the placement of the feet and charac­teristics of the base of support. In normal adults stand­ing on a flat, firm surface with feet spaced comfortably apart, the LOS perimeter can best be described as an ellipse, as shown in Figure 5–1. The AP dimension of this ellipse is approximately 12.5° from the back­wardmost to the forwardmost points on the perimeter (Nashner & McCollum, 1985). While height of the COG above the surface and foot length affect the AP LOS, these two features co-vary, resulting in approximately the same AP limits for people of various heights (Dun­can, Weiner, Chandler, & Studenski, 1990).
The lateral LOS depends on the person’s height relative to the spacing between the feet. When the feet of a 70-inch tall person are placed 4 inches apart, for example, the lateral dimension of the LOS ellipse is approximately 16° from the left to the rightmost points on the perimeter. For taller individuals, a wider spacing between the feet is required to produce a 16° ellipse, whereas shorter people can place their feet closer together.
The biomechanical properties that determine the LOS are similar while standing in place, walking, and sitting without trunk support, as shown in Figure 5–2. During in-place standing, the COG moves randomly within an LOS perimeter determined by the base of support and the placement of the feet. During walk­ing, the COG progresses forward through the LOS in a smooth, rhythmic movement (Nashner, 1986; Nashner & Forssberg, 1986). At heel strike, LOS is established with the COG positioned slightly behind the posterior perimeter but with sufficient forward momentum to carry it to the perimeter. As the step progresses, the COG moves forward within the LOS. As the COG approaches and then exceeds the anterior perimeter of the LOS, the next step establishes a new LOS and the rhythmic process is repeated. When sitting without trunk support, the height of the COG above the support surface is considerably less and the base area is larger. Therefore, the LOS perimeter is larger in terms of COG sway angles when one is seated than in quiet standing.
Limits of Sway
It is impossible to maintain the COG motionless, because in-place standing is an inherently unstable task requiring intermittent corrections to overcome the destabilizing influence of gravity (Begbie, 1967; Diener, Dichgans, Bacher, & Gompf, 1984; Scott & Dzendolet,
1972). Thus, a person attempting to maintain balance spontaneously sways back and forth and from side to side. The limits of sway is a two-dimensional quantity defining the maximum spontaneous COG sway angle
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Figure 5–2. Limits of stability boundaries during standing, walking and sitting. From Handbook of Balance Func- tion Testing, Jacobson et al., 1997.
as a function of the sway direction, as shown in Fig­ure 5–3. A person’s limits of spontaneous sway vary with the sensory conditions and the configuration of the base of support. But, unless the person loses bal­ance, the limits of sway remain within the LOS.
Center of Gravity Alignment
A point at the center of the area contained within the limits of sway perimeter defines the COG alignment, as shown in Figure 5–3. This definition of COG alignment is based on the assumption that a person is attempting to maintain a COG position which is at the center of the limits of sway perimeter. When a normal person is asked to stand erect, the most stable position is to align the COG above the center of the base of support, since this position maximizes the limits of sway amplitude.
The limits of sway and COG alignment affect a person’s balance. When the COG is aligned over the center of the base of support, the limits of sway can be as large as the LOS before balance is lost. A person whose COG alignment is offset from the center of sup­port must reduce the limits of sway in the direction of the offset to maintain stability.
low, gravity is the only significant destabilizing force that must be overcome, and the COG can be moved within the full range of the LOS. For the average adult, COG movements within the full range of the LOS are possible when a sway oscillation cycle (front to back or side to side and then back again) takes two to three seconds or longer. By contrast, when sway oscillation cycles take less than one second, momentum is an additional destabilizing force and the LOS perimeter is reduced to as little as 3°.
Understanding the impact of COG sway fre­quency is important in assessing a person’s balance. As higher frequencies reduce the effective LOS, a per­son using fast sway movements is closer to exceeding the LOS than an individual swaying slowly through a comparable arc. This principle is further explained by a theoretical multidimensional model of postural sway which demonstrates that 92% of the variance in sway is explained by two variables, one related to sway ampli­tude and the other to sway velocity (Maurer & Peterka, 2005; Pavol, 2005).
SENSING THE POSITION OF BALANCE
Limits of Stability and Sway Frequency
In addition to the base of support, the actual LOS is influenced by COG sway velocity, which is directly related to sway frequency (Nashner, Shupert, Horak, & Black, 1989). When the frequency of COG sway is
Sensory and Motor Components of Balance
To execute the constant corrections required to resist the destabilizing effect of gravity and the perturbing effects of purposeful motor actions while standing and walking, the balance system must determine the
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Figure 5–3. Relations between the LOS, the sway envelope, and the COG alignment. The middle figure shows the COG alignment within the LOS. The right figure shows the C
OG aligned forward relative to the center. From Handbook of Balance Function Testing,
Jacobson et al., 1997.
position of the COG relative to gravity and the base of support and then execute intermittent coordinated movements to correct COG deviations. Although the neural processes for determining COG position and moving the COG are highly integrated, the two are separated here for simplifying the systematic model of balance control. From a clinical perspective, separating the sensory and motor processes of balance means that a patient may have impaired balance for one or a com­bination of two reasons: (1) the position of the COG relative to the base of support is not accurately sensed, and (2) the automatic movements required to bring the COG to a balanced position are untimely, poorly coor­dinated, or inappropriate.
Visual, Vestibular, and Somatosensory Inputs
Sensing the position of the COG relative to gravity and the base of support requires a combination of visual, vestibular, and somatosensory (tactile, deep pres­sure, joint receptor, and muscle proprioceptor) inputs. Utilization of the three balance senses is reviewed in Table 5–1. Three senses are required because no single sense directly measures COG position. Somatosensory inputs provide information on the orientation of the body parts relative to one another, the support surface,
and gravity. The vestibular system measures gravita­tional, linear, and angular accelerations of the head in relation to inertial space. Vision measures the orientation of the eyes and head in relation to surrounding objects.
Under some task conditions, one or more of the senses may provide information that is misleading or inaccurate for purposes of balance control. For exam­ple, when a person stands next to a large bus that suddenly begins to move forward, momentary disori­entation or unsteadiness may result. A fraction of a sec­ond is required for the brain to determine whether the resulting visual stimulus indicates backward sway of the person or forward movement of the bus. If a down­wardly tilted support surface is encountered, the brain must determine whether the surface is tilted downward or the surface is level and the body is tilted back. Dur­ing sensory conflict situations, the brain must quickly select the sensory inputs providing accurate orienta­tion information and ignore the misleading ones.
The process of changing the combination of sensory inputs to balance is usually termed sensory “adaptation” or “reweighting.” Using signal process­ing techniques, investigators have demonstrated that under normal sensory conditions when all senses are accurate and there is more than enough useful informa­tion, subjects vary in their weighting of the three senses (Peterka & Loughlin, 2004). These same techniques have been used to show that, as the sensory conditions
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table 5–1. Utilization of the Senses for Balance
Sense Reference Conditions Favoring Use Conditions Disrupting Use
Somatosensory Support surface Fixed support surface Irregular or moving support
Visual Surrounding objects Fixed visible surrounds and
irregular or moving support
Vestibular Gravity and inertial space Irregular or moving support
and moving surrounds or darkness
change, subjects reweigh inputs, reducing the influence of misleading inputs in favor of those providing the more useful information (Asslander & Peterka, 2014; Logan, Kiemel, & Jeka, 2014).
positions and the direction of gaze. Precise head, eye, and gaze control are critical in the execution of many complex motor activities, such as running and either kicking or catching a moving ball.
The weighting of the vestibular input, however,
Somatosensory Input
is increased when both the somatosensory and visual
inputs are misleading or unavailable (Allum, Hon­Somatosensory input derived from the contact forces and motions between the feet and the support surface is the dominant sensory input to balance under normal (fixed) support surface conditions (Aggashyan, Gurfin­kel, Mamsakhlisov, & Elner, 1973; Diener & Dichgans, 1988; Diener, Dichgans, & Guschlbauer, 1986; Dietz, Horstmann, & Berger, 1989; Gurfinkel, Lipshits, et al.,
1974). When a person stands on a firm, level surface, the extent of COG sway is very small relative to the LOS. Closing the eyes to eliminate vision causes little if any functionally significant increase in COG sway. Even a well-compensated patient with a bilateral ves­tibular loss sways well within the LOS with the eyes closed (Black & Nashner, 1984, 1985; Nashner, Black, & Wall, 1982; Shupert, Black, & Horak, 1988). When the support surface is sway referenced to disrupt use­ful somatosensory inputs, subjects reduce the weight given to somatosensory inputs and increase weighting of visual and vestibular inputs (Logan, Kiemel, & Jeka, 2014; Peterka & Laughlin, 2004).
egger, & Pfaltz, 1989; Peterka & Loughlin, 2004). The
patient with a profound bilateral vestibular loss, for
example, is unsteady standing in darkness on a com-
pliant or irregular surface. Because vestibular input is
seldom if ever misleading (except in cases of disease
or other disorder and unusual motion environments),
vestibular information is critical for balance when
conflicting visual and/or somatosensory informa-
tion requires a person to identify and quickly ignore
a misleading input (Black & Nashner, 1984, 1985). This
is why patients with peripheral vestibular deficits fre-
quently complain of dizziness and/or unsteadiness
during exposure to conflicting visual and support sur-
face stimuli.
Exposure to zero gravity or to a simulation of zero gravity is believed to cause changes in the way the brain interprets orientation input from the vestibu­lar system. The utricular otoliths normally sense both the linear acceleration of the head and the tilt angle of the head with respect to gravity. Under zero-gravity conditions, the brain must adapt to an absence of the
Vestibular Input
tilt angle component of the otolith input. The adaptive changes in interpretation of the vestibular input fol-
When functionally useful somatosensory and visual inputs are available, vestibular inputs play a minor role in controlling COG position (Bles, deJong, & deWit, 1984; Nashner et al., 1982; Shupert et al., 1988). This is because the somatosensory and visual inputs are more sensitive to body sway than the vestibular sys­tem (Nashner et al., 1989). The primary role of vestibu­lar input under these conditions is most probably to allow independent and precise control of head and eye
lowing zero-gravity exposure may be viewed as a tem­porary, environmentally induced pathologic condition (Paloski, Reschke, Doxey, & Harm, 1992; Young, Oman, Watt, Money, & Lichtenberg, 1984). These maladaptive changes are most potent immediately after return to normal terrestrial conditions and are most pronounced when the returning astronauts are exposed to conflict­ing visual conditions (Parker, Reschke, Arrott, Hor­mick, & Lichtenberg, 1985).
Moving surrounds, darkness
Unusual motion environments
92 BAlAnCE FunCtion AssEssmEnt And mAnAgEmEnt
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Visual Input
Among the three balance senses, vision is without doubt the richest and most varied in providing ori­entation and motion information. A comprehensive summary of visual orientation perception has been described by Gibson (1979). Understanding the nature of visual perception is important for posture control, because the advent of modern computer animated vir­tual reality techniques allows assessment and training of the full range of visual influences on balance. Some of the key elements of visual motion perception that influence balance include visual field flow and changes in object size, both of which are influenced by the dis­tance of objects from the observer, parallax effects influ­enced by the relative distances between near and far objects, and the spatial frequencies and contrast dif­ferences among objects in the surround. Recent virtual reality research demonstrates that individual elements of visual orientation perception differ in their influ­ences on balance (Keshner & Kenyan, 2009; Streepey, Kenyan, & Keshner, 2007). For example, flow within the peripheral visual field has a stronger influence on balance control than the changing sizes of objects in the central visual field.
Vision plays a significant role in balance, especially when the support surface is unstable (Begbie, 1967; Die­ner et al., 1986; Lee & Lishman, 1975; Paulus, Straube, & Brandt, 1984, 1987). For example, when toes-up and toes-down tilting of the surface in direct relation to the AP sway disrupts somatosensory input useful for bal­ance, COG sway is significantly less with eyes open than with eyes closed (Black & Nashner, 1984, 1985; Nashner, Black, & Wall, 1982). The stabilizing effect of vision is also illustrated by comparing eyes-open and eyes-closed sway while a person stands on a compli­ant foam rubber pad. Vision also influences COG align­ment. When a person is exposed to a constant linear or rotational movement of the visual field, for example, the alignment of the COG over the base of support shifts in the direction of the visual field motion (Brandt, Paulus, & Straube, 1986; Lestienne, Soechting, & Berthoz, 1977).
The reader may have experienced the effect of vision on balance, for example, at the seashore when a wave causes a large area of the surrounding water to move in or out at constant velocity. If a person is attending to the moving water, there is a tendency to sway and sometimes even stumble in the direction of the moving water. Alterations in body alignment also occur when subjects are exposed to a room with tilted walls. Similar visual illusions are sometimes used in carnival fun-houses to throw participants off balance.
MOTOR CONTROL OF BALANCE
Anatomy and Physiology of Movement
During erect standing with the arms at the sides or folded at the waist, the COG is located in the area of the lower abdomen, with the exact position at any given moment dependent on the relative positions of the ankle, knee, and hip joints (McCollum & Leen, 1989). Because there are three principal joint systems — ankles, knees, and hips — between the base of support and the COG during standing, a wide variety of different pos­tures can be assumed with the COG over the center of the base of support, as illustrated in Figure 5–4. For similar reasons, a wide variety of active ankle, knee, and hip movement patterns can be used to produce similar shifts in COG position. Examples of this diver­sity of postures and balance movement patterns can be observed in individuals performing highly trained dance or martial arts routines.
A detailed description of the large number of muscles controlling ankle, knee, and hip joint motions is beyond the scope of this chapter. Instead, this sec­tion focuses on the key muscle groups involved in balance and on the general physiologic principles gov­erning coordination of these muscles during postural movements.
Motions about a given joint are controlled by the combined actions of at least one pair of muscles working in opposition. All leg and lower trunk joints have multiple pairs of opposing muscles. Furthermore, many leg muscles act about two neighboring joints. At the ankle joint, the gastrocnemius and tibialis anterior are the major extensor (plantar flexor) and flexor (dor­siflexor) muscles, respectively. The quadriceps is the major knee extensor, while the hamstrings and gas­trocnemius are both knee flexors. The hamstrings and lower back muscles are hip extensors, while hip flexion is controlled by quadriceps and abdominals.
An isolated muscle acts like a spring, tending to resist attempts to stretch the muscle beyond a resting length (Hill, 1953). The degree of the muscle’s resis­tance to stretch is called muscle stiffness. Both the rest length of the muscle and the muscle stiffness vary depending on how strongly the muscle is being acti­vated. An inactive muscle has an extended rest length and offers little resistance to stretching. The rest length of a highly active muscle is shorter, and the muscle vigorously resists stretching. When muscles acting in opposition about a joint co-contract, stiffness increases without associated joint motion.
5. PRACTICAL BIOMECHANICS AND PHYSIOLOGY OF BALANCE 93
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Figure 5–4. Examples of the variety of different postures during which the body C Handbook of Balance Function Testing, Jacobson et al., 1997.
OG is centered over the base of support. From
Stretch Reflex Movement
When the forces exerted by pairs of opposing muscles about a joint are combined, the effect is to resist joint rotation like a compliant spring. How compliant the joint is in resisting rotation is called joint stiffness. The resting position and the stiffness of the joint are each altered independently by changing the background activation levels of one or both muscles. The myotatic stretch reflex is the earliest mechanism for increasing the activation level of the muscles of a joint following an externally imposed rotation of the joint. This response component is initiated by inputs from muscle spindles, tiny stretch sensitive receptors embedded within the muscle. Output fibers from the muscle spindles enter the spinal cord and, by way of single synapses within the cord, activate muscle fibers within the same muscle originating the spindle inputs (Houk, 1979). Myotatic stretch reflexes are thought to improve the nonlinear stiffness properties of muscle (Houk, 1979).
Recent advances in computer modeling of bal­ance control suggest that leg joint stiffness is an impor­tant component of balance control and that, like the reweighting of senses, the system actively also modi­fies leg joint stiffnesses depending on the conditions of the task (Suzuki, Nomura, Casadio, & Morasso, 2012). For example, forces generated by ankle joint stiffness in response to rotations of the support surface are desta­bilizing and therefore inappropriate for balance control (Nashner, 1976).
Automatic and Volitional Movement Systems
The influences of joint stiffness, automatic movement system, and volitional movement system on standing balance are reviewed in Table 5–2. As described previ­ously, the active regulation of joint stiffness provides assistance but is insufficient to maintain postural sta­bility (Casadio & Morasso, 2005; Gurfinkel, Lipshits, & Popov, 1974).
Automatic postural movements are the earliest actively generated force responses helping to main­tain stability when a standing individual’s balance is perturbed (Nashner, 1976, 1977; Nashner, Woollacott, & Tuma, 1979). Automatic postural movements resem­ble both reflexive and voluntary movements. Like reflexes, they are triggered by external stimuli, occur at fixed latencies, and are relatively stereotyped. Like voluntary postural movements, automatic responses involve the coordinated actions of many leg and trunk muscles, and the amplitudes and patterns of automatic responses adapt to the task conditions. Although the pathways mediating automatic postural movements have not been fully elucidated, the 90 to 100 msec laten­cies of electromyographic (EMG) responses are suffi­cient to include significant brainstem and subcortical involvement (Evarts & Tajii, 1974; Marsden, Merton, & Morton, 1973; Melville Jones & Watt, 1971).
Voluntary postural movements can occur either in the presence or absence of external stimuli and the