QUEST, 1994,46, 8-19
O 1994 American Academy of Kinesiology and Physical Education
Neuromuscular Stress
Timothy P. White and Marialice Kern
This paper focuses on exercise-induced stress that results from motor unit recruitment,
the impact of recruitment on selected systemic support systems, and some of the environmental
overlays that affect the degree of physiological stress. This topic is a component, in a global
sense, of the physiological response to stress as defined by the general adaptation syndrome
(Selye, 1976), in which three phases are characterized as the alarm reaction, resistance development, and exhaustion. As summarized by Vander, Sherman, and Luciano (1990, pp. 696704), the response to stress is necessary if health and life are to be maintained. In a more
limited sense, physiologists often consider the response to stress in regard to a noxious or
potentially noxious stimuli. The stress response is an evolutionary conserved mechanism by
which cells respond and defend against abrupt and adverse changes in their environment
(Welch, 1992). Examples often include the response to trauma, prolonged cold exposure or
heavy exercise, infection, shock, hypoxia, fright, pain, and other emotional stresses (Vander,
Sherman, & Luciano, 1990). In this context, the secretion of cortisol, a glucocorticoid hormone
from the adrenal cortex, is increased through mediation by the hypothalamus-anterior pituitary
system in a way similar to the increased release of epinephrine from the adrenal medulla.
Although these traditional responses are fundamentally important, they will not be reviewed
in any detail in the present paper.
A primary stressor of the human body comes from within-the recruitment of motor
units in skeletal muscle. In this context, stress is a positive attribute and is necessary for
performance, survival, and reproduction of a species, including human beings. Recruitment
of motor units in skeletal muscle during a single bout of exercise induces stress and leads to
the response of several key physiological systems to maintain homeostasis. Two fundamental
factors for sustained performance are energy demand by recruited skeletal muscle and oxygen
delivery. Since physiology has a high degree of redundancy, one specific underlying systemic
variable may be altered, whereas another compensates such that these factors are maintained.
Repeated exposure to stressors can induce adaptive responses, such that the subsequent exposure
to a similar absolute stress will be less on a relative scale. The adaptations that occur from
appropriate training stimuli enhance the capacity to maintain homeostasis. One can increase
the level of stress of motor unit recruitment by external and internal environmental changes
or lessen the relative level of stress with appropriate adaptations of skeletal muscle and key
systemic support systems (e.g., cardiorespiratory).
The working definition of stress for this symposium (Franks,1994) as "arousal beyond
what is necessary to accomplish the activity" (p. 4) creates an interesting challenge for the
treatment of physiological stress. There are few nonpathological circumstances under which
Timothy P. White is with the Department of Human Biodynamics at the University
of California, Berkeley, Berkeley, CA 94720. Marialice Kern is with the Department of
Kinesiology and Physical Education at California State University, Hayward, Hayward, CA
94542-3062.
NEUROMUSCULAR STRESS
9
systemic physiological responses to exercise wiU exceed those necessary to accomplish the
desired activity. For example, during single bouts of exercise, a cardiovascular or other systemic
response to exercise will become elevated under a given circumstance (such as induced by
an environmental extreme); this is an additional stress from a physiological viewpoint and
indeed necessary to accomplish the exercise.
When stressors coincidentwith a singlebout of exerciseexceed the homeostaticcapacity,
or when repetitive bouts of exercise exceed the adaptive capacity, either performance becomes
attenuated or injury, disease, or death results. Muscle injury is dealt within the current paper,
disease is the purview of Dr. Plowman's (1994) paper, and death is not addressed in the
symposium. Dr. Dishman's (1994) treatment of the biopsychology and neuroscience of stress
focuses on other physiological issues, including neuroendocrine mediators.
Skeletal Muscle Recruitment
Indeed, it is the recruitment of motor units in skeletal muscle that provides the basis
for all physical activities. Muscle contraction results from the activation of contractile and
regulatory proteins within fibers (Faulkner, Green, & White, 1994). The resulting type of
contraction depends on the balance between the external load applied and the force developed
by the muscle fibers. During contraction, fibers may shorten, remain at the same length, or
lengthen, depending on the balance between external load and force development. Thus, the
term contraction is used by convention and is not meant literally.
Muscle fibers are functionally organized into motor units, which consist of the cell
body, the motor nerve and its branches, and the skeletal muscle fibers that are innervated by
the nerve terminals (Burke, Levine, Zajac, Tsairis, & Engle, 1973). In medial gaslrocnemius
muscle of cats, the motor units have been classified as slow (S), fast fatigue resistant (FR),
and fast fatigable (FF) (Burke et al., 1973). This classification scheme is based on functional
data, including contraction time, a "sag" in the force record during unfused tetanus, and a
fatigue test. Other prominent schemes of classification of mammalian fibers are based on the
activities of oxidative enzymes (Peter, Bamard, Edgerton, Gillespie, & Stemple, 1972), and
the differential sensitivity of myofibrillar adenosin triphosphatase (ATPase) activity to altered
pH (Pette & Staron, 1990). Although there are some ambiguities, there is a reasonable
correlation between classifying motor units as Type I, IIA, W, (Brooke & Kaiser, 1970), or
slow (S), fast-oxidative-glycolytic (FOG), and fast-glycolyhc (FG)(Peter et al., 1972), and
those classified by contractile properties (S, FR, FF) (Burke et al., 1973). The primary attributes
of fibers that determine classification under these schemes typically constitute a continuum
(Faulkner & White, 1990), and thus the classification of fibers into distinct types based on
qualitative determination of "low" and "high" activity for various enzymes has shortcomings.
The maximum strength of muscle groups may be obtained by maximum voluntary
contractions, and maximum isometric force by electrical stimulation of the motor nerve or
directly of muscle fibers (Merton, 1954). Voluntary recruitment follows, in most cases, the
principles set out by Hememan and colleagues (Hememan & Olson, 1965; Hememan,
Somjen, & Carpenter, 1965), and the regulation of force is influenced by the number and
size of motor units recruited and the frequency of their stimulation. With supramaximum
stimulation frequency, the maximum isometric force is a function of the total cross-sectional
area of the contracting fibers and the length of the fibers relative to optimum on the lengthtension relationship (Close, 1972; Kandarian & White, 1990). The product of the force and
velocity at which muscle lengthens or shortens determines the power absorption or output,
respectively. The maximum absolute velocity of fiber shortening is determined, when there
is minimal preload and afterload, by the myosin ATPase activity (Barany, 1967) and the
WHITE AND KERN
10
length of the muscle fibers. When muscles are loaded, which is the usual case in exercise,
the velocity attained is slowed by the magnitude of the load (Wilkie, 1950). Alterations in
force and power output almarise from architectwd influences, such as the angle of fiber
pinnation (Gans, 1982).
Exercise involves innumerable combiitions of shortening, isometric, and lengthening
contractionsby the activated motor units (Luhtanen & Komi, 1980).The shorteningcontractions
generatethe power necessary for limb movement and the consequent locomotion and movement
of external objects. Compared to other types of contraction, shortening contmctions are the
most demanding from a metabolic perspective Wesser, Linnarsson, & Bjurstedt, 1977).During
most forms of exercise, energy will also be expended by isometric contractions that provide
joint stability and by other muscles that contract concurrently in an antagonistic function to
decelerate limb movement, which results in lengthening contractions. Other muscles will be
recruited to retum the involved limbs to their original position during repetitive movements
(Luhtanen & Komi, 1980). The energy expended to perform the isometric and lengthening
contractions, or to retum limbs to original position in repetitive tasks, is not expressed as
external work in a Newtonian sense. The more complex the exercise, the greater the discrepancy
between caloric expenditures and the amount of external work performed (Eaulkner et al.,
1994).
Systemic Responses to Single Bouts of Exercise
Primary Metabolites
With muscle contraction, there is a small decrease in adenosine triphosphate (ATP)
and increase in adenosine diphosphate (ADP) and inorganic phosphate (Faulkner et al., 1994).
This process results in an accelerationin the hydrolysis of creatine phosphate to rephosphorylate
ADP to ATP and leads to a cascade of enzymatic events that activate the glycolytic and
oxidative phosphorylation pathways. A single bout of exercise involving repeated contractions
is influenced by a host of factors that are intrinsic and extrinsic to the muscle fibers (Eaulkner
et al., 1994). Intrinsic factors include the types of fibers and the substrate concentrations,
particularly ATP and glycogen. Important extrinsic factors include the delivery of oxygen,
removal of metabolites, and regulation of muscle temperature and pH.
Cardiovascular Response
Dynamic activities elicit the greatest response f m the cardiovascular system exemplified by 4- to 9fold increases in cardiac output, 3- to 3.5-fold increases in heart rate, and 1.5to 2-fold increases in systolic blood pressure. Strength exercises result in relatively large
increases in systolic and diastolic blood pressure, with moderate increases in heart rate and
cardiac output (Brooks & Fahey, 1984).
Coincident with muscle contraction, autoregulatory mechanisms increase muscle blood
flow and increase the delivery of oxygen and metabolic substrates in the anticipation of
sustained power output (Armstrong & Laughlin, 1984; L a u w & Ripperger, 1987). In a
single bout of exercise, the type and magnitude of the support response by the cardiovascular
system depends on the type of activity and the intensity at which it is being performed
Metabolic Responses
The metabolic responses are specific to exercise intensity and duration as well. Dynamic
activities can result in over a 20-fold increase in oxygen consumption (VO*),increased free
fatty acid levels in the blood, 10-to 15-foldincreases in blood andmusclelactate concentrations,
NEUROMUSCULAR STRESS
11
and increased glycogenolysis and liver gluconeogenesis (Brooks & Fahey, 1984). Static
exercises are short in duration and primarily utilize readily available fuels. As a result, available
ATP, creatine phosphate, blood glucose, and glycogen will be utilized. This results in transient
changesin the active muscle's level of these substrates, with little change in substrate concentration observed in the circulation.
Sustained Power
The power that can be sustained over time is dependent on the person's maximum
capacity to develop power and on the degree to which the individual is trained for the repetitive
activity. As one example, consider the systemic response to a moderate-intensity exercise.
Moderate-intensity exercise requires approximately 10% of the maximum power capable of
being developed in a single contraction in vitro, and would be equivalent to "easy" jogging
for moderately active adult (Faulkner et al., 1994). At 10% of maximum power (equivalent
to approximately 20 W/kg of active muscle and approximately 140 Watts on a bicycle
ergometer), the metabolic requirement is approximately 9.0 Mets. During moderate-intensity
activity, some loss of averageforce will occur over time during each of the repeated contractions.
Throughout moderate physical activity, ATP concentration is maintained relatively
constant, initially by hydrolysis of locally stored high-energy phosphates. During a transition
period of several minutes' duration, energy output will remain constant as a result of varying
contributions of different metabolic pathways (Brooks & Fahey, 1984). After the transition
period, oxygen consumption willplateau and oxidativephosphorylation will be the predominant
means by which energy flux is maintained throughout the remainder of the activity. The
magnitude of the power sustained during moderate activity is controlled by the balance between
energy output and enagy input. Although a steady rate of metabolism is achieved, this intensity
of activity can typically be performed for a period of hours. Beyond that, fatigue would be
very evident and blood glucose and muscle glycogen concentrations would be nearly exhausted
(Conlee, 1987).
Unexplained Oxygen Consumption
The systemic response to a single bout of physical activity can also provide an example
of "excess" oxygen consumption. This is a salient example of how the enhanced energetic
cost may seem, at first glance, to result from stress in the context of an arousal beyond that
necessary to accomplish the activity. The metabolic cost of an activity is relatively constant,
and there is a rapid increase in V02 with the initiation of activity, followed by a constant,
steady state level of V02 presumably necessary to meet the energy demands of the work.
During dynamic exercise performed at levels of intensity greater than the individuals lactate
threshold, V02 slowly increases and has been termed excess oxygen consumption (Barstow &
Molt5, 1991; Poole et al., 1991; Roston et al., 1987). This is a component to the total V02
that is above that needed as estimated from lower intensities, or noted earlier in the exercise
bout.
What drives this "excess VOz" is an interesting question and falls under the working
definition of stress, as to date the cause remains elusive. Central factors, such as increased
body temperature and liver metabolism, have been evaluated and dismissed (Linnarsson, 1974;
Molt5 & Coulson, 1985). Local factors, specifically increased muscle temperature (Brooks,
Hittelman, Faukner, & Beyer,l971) and increased recruitment of Type IIB fibers (Barstow &
Mol6,1991; Vollestad & Blom, 1985), resulting in an increasein blood lactate concentration,
seem to be reasonable working hypotheses to explain this phenomenon. Although the V Q
appears as an excess, in fact it is unexplained, and we submit that it uxdoubterlly exisrs for
a bona fide physiologicat reason.
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NEUROMUSCULAR STRESS
13
Adaptations to Sustained Changes in Physical Activity
Adaptations to repeated increases in physical activity are characterized by changes in
morphological,biochemical, and molecular properties of skeletal muscle that alter the functional
attributes of fibers in specific motor units (Faulkner et al., 1994; Salmons & Hendrickson,
1981).Additionally, there are adaptiveresponsesto the support systems, primarily cardiorespiratory, that allow for sustained contractions (Brooks & Fahey, 1984). Neurophysiological adaptations can be observed during the early stages of a strength-training program when large
improvements in strength and power emerge, which presumably reflects the optimization of
motor unit recruitment (Sale, 1988). Muscle adaptations can include a higher capacity to
generate power following strength-power training or an enhanced capacity to sustain power
over time following endurance training. Adaptations to strength and endurance activities may
occur independently or concurrently (Holloszy & Booth, 1976). For example, the addition of
resistance training to endurance training has no deleterious impact effect and enhances endurance performance under some circumstances (Hickson, Dvorak, Gorostiaga, Kurowski, &
Foster, 1988).
A training stimulus occurs when a change in the habitual level of physical activity is
of sufficient magnitude and duration to produce a measurable adaptive response. During
skeletal-muscle-adaptation-increased physical activity, some metabolic adaptations may be
observed within days (Green et al., 1992). However, most improvements in biochemical
(Green et al., 1992; Holloszy & Booth, 1976) and contractile properties (Jones & Rurtherford,
1987) require weeks or months of sustained activity.
Most adaptations that occur beyond the early training directly influence the contractile
and metabolic properties of skeletal muscle fibers (Holloszy & Booth, 1976). These adaptations
may be either in the muscle group directly involved in the movement, in antagonistic muscles,
or in fixator muscles that provide the force platform for the movement (Faulkner et al., 1994).
The criterion for an adaptive response is a qualitative or quantitative alteration in one or more
specific muscle proteins: contractile, regulatory, shuctural, metabolic, or transport (Faulkner
et al., 1994). Adaptations occur in response to a specific training stimulus, and the adaptive
response is regulated at multiple sites that are controlled by negative feedback The adaptive
responses result in an enhanced capacity for work output and the maintenance of homeostasis.
A high degree of adaptive specificity results in unique modifications of specific morphological,
biochemical, and molecular properties of skeletal muscle fibers in response to a given training
stimulus (Faulkner et al., 1994). Fibers within motor units recruited during training are the
fibers primarily affected, and only those elements that are stimulated beyond a threshold will
adapt. Adaptations of muscle fibers in vitro appear to be mediated predominantly by the
frequency and duration of stimulation and by the external load (Faulkner & White, 1990),
with trophic factors playing at most a minor role.
Mechanical forces imposed on embryonic muscles cells growing in vitro appear to
enhance muscle growth by soluble growth factors (Vandenburgh, Karlisch, Shansky, &
Feldstein, 1991), but the role of growth factors in vivo has not been determined. The specificity
of adaptations may result in improved performance in one physical activity, with no change
or even an impairment in another activity (MacDougall & Davies, 1984). Twelve weeks of
heavy-resistance strength training leads to a 5% incmse in quadriceps muscle cross-sectional
area as measured by computerized tomography (Jones & Rutherford, 1987). As muscle length
likely does not change, the circumference values provide an estimate of the gain in muscle
mass. The increase in muscle mass following power lifting results from comparable incxaws
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NEUROMUSCULAR STRESS
15
intracellular calcium appears to be a common mediator (Armstrong, 1984, 1990). Polyethylene
glycol-superoxidedismutase (PEGSOD)administered before lengthening contractionsreduced
the subsequent degree of degeneration and regeneration (Zerba, Komorowski, & Faulkner,
1990). PEG-SOD is a free radical scavenger that likely interrupts the free-radical-induced,
calcium-mediated phospholipase breakdown of membranes. Successful regeneration requires
revascularization, cellular infiltration,phagocytosis of necrotic muscle fibers, proliferation and
fusion of muscle precursor cells, reinnervation, and recruitment and loading (White & Devor,
1993).
Exercise to exhaustion can cause muscle damage (AppeU, Soares, & m e , 1992;
Armstrong, 1984; Ebbeling & Carlson, 1989; Evans & Cannon, 1991). This damage is
temporary and is typically fully repairable. Mitochondrial swelling and dis~ptionhave been
reported (Frieden, Seger, & Ekblom, 1988), resulting in compromised performance levels.
After an endurance activity, inNtration of inflammatory cells, increased connective tissue,
necrotic fibers, and fiber phagocytosis have been reported, while other fibers are undergoing
regeneration (Armstrong, 1984; Sjostrom, Friden, & Ekblom, 1987).These changes have been
atbibuted to hypoxic conditions and elevated free radicals, resulting in increased lysosomal
activity.
Myotendimus Junction Injury
The complex myotendinous junction is in its early stages of understanding (Tidball,
1991). The myotendinous junctions are the sites of force transmission between muscle fibers
and tendons and are often the site of tears and other injuries under experimentally loaded
conditions. Furthermore, this is a very common site for lesions (ie., tears) in clinical practice
(see Kibler, Chandler, & Stracener, 1992; Tidball, 1991).
Stress Proteins
When cells are exposed to an adverse change in their environment, gene expression
of certain proteins is often increased (Welch, 1992). This response was originally r e f d to
as the heat shock response, as the original experiments used thermal stress to induce the
proteins. However, the so-called heat shock proteins are expressed by so many insults in
addition to heat that they are more properly considered stress proteins (Linquist, 1986; Welch,
1992). The two major groups of stress proteins are (a) the so-called heat shock proteins with
molecular weights of 8,28,58,72,73,90, and 110 kDa and (b) the glucose-regulated proteins
that respond to glucose deprivation and have molecular weights of 78,94, and 170 kDa. In
general, these proteins are present in normal "unstressed" cells but increase their expression
under stress. The physiolkgical sigruficance of stress proteins is currently not well d e f i
but they may help mediate adaptations or facilitate protein maturation.
Following an exhaustive bout of exercise, induction of stress proteins has been reported
in rats (Locke, Nobel, & Atkinson, 1990). Salo, Donovan, and Davies (1991) studied the 70
kDa proteins in skeletal muscle, heart, and liver following an exhaustive bout of exercise,
and concluded that induction of these proteins was a physiological response to the heat shock
and oxidative stress of exercise.
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