J Appl Physiol 95: 455-459, 2003;
doi:10.1152/japplphysiol.00280.2003
8750-7587/03 $5.00
INVITED REVIEW
Terminology for contractions of muscles during shortening, while isometric, and during lengthening
John A. Faulkner
Institute of Gerontology and Departments of Physiology and Biomedical
Engineering, University of Michigan, Ann Arbor, Michigan 48109
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ABSTRACT
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Communication among scientists must be clear and concise to avoid ambiguity
and misinterpretations. The selection of words must be based on accepted
definitions. The fields of biomechanics, muscle physiology, and exercise
science have had a particularly difficult time with terminology, arising from
the complexity of muscle contractions and by the use of inappropriate
terminology by scientists. The dictionary definition of the verb
"contract," specifically for the case of muscle, is "to
undergo an increase in tension, or force, and become shorter." Under all
circumstances, an activated muscle generates force, but an activated muscle
generating force does not invariably shorten! During the 1920s and 1930s,
investigators recognized that the interaction between the force generated by
the muscle and the load on the muscle results in either shortening, no length
change (isometric), or lengthening of the muscle. The recognition that muscles
perform three different types of "contractions" required that
contraction be redefined as "to undergo activation and generate
force." Modifiers of contraction are then needed to clarify the lack of
movement or the directionality of movement. Despite the contradiction, for 75
years the lack of movement has been termed an "isometric
contraction." The directionality of the movement is then best described
by the adjectives "shortening" and "lengthening." The
definitions of "concentric" as "having the same
center" and of "eccentric" as "not having the same
center" are consistent with hypertrophy, or remodeling of the heart
muscle, but are inappropriate to describe the contractions of skeletal
muscles.
action; pliometric; miometric; concentric; eccentric
AMONG SCIENTISTS, THE NEED for immediate understanding requires
that communication be clear and concise. To avoid ambiguity and
misinterpretations, the selection of words must be based on accepted
definitions as to their meanings. The fields of biomechanics, muscle
physiology, and exercise science have had a particularly difficult time in the
use of terms. The difficulties have arisen partly through the complexities of
the skeletal muscle contractions themselves and partly through the
carelessness of scientists regarding the use of inappropriate terminology, as
well as the permissiveness of editors. The dictionary definition of the
transitive verb "to contract" is "to draw together, or
shorten" and specifically, for the case of muscle, "to undergo an
increase in tension, or force, and become shorter." Under all
circumstances, an activated muscle develops force. The difficulty with the
current dictionary definition is that an activated muscle does not invariably
shorten! Depending on the interaction between the force developed by the
muscle and the load on the muscle, the muscle will either shorten, remain at a
fixed length (isometric), or be lengthened.
During the 1920s and 1930s, the phenomenon of skeletal muscles
"contracting" not only during shortening but also while remaining
isometric or even during lengthening was recognized widely
(13,
21,
22,
24,
34). The recognition that
muscles make three different types of "contractions" required a
redefinition of contraction and modifiers of contraction to clarify the lack
of movement or the directionality of the movement. During the past 75 years,
various modifiers have been associated routinely with the verb contract or the
noun contraction that were either redundant with or contradictory to the
dictionary definition of the term. Despite these problems, for muscle
physiologists, contract, contraction, and contractility are the only terms
that adequately describe the phenomenon of the response of muscle fibers to
activation. As with all "living" languages, the English language
is in a constant state of revision, as the definitions of words change through
usage. Specifically for the case of muscle, many decades ago "to
contract" should have been redefined as "to undergo activation and
generate force" and not specify the directionality of the movement as
"to shorten." An additional nuance of the contractions of skeletal
muscles, first recognized by A. V. Hill
(22) and B. Katz
(30) during the 1930s, was the
observation that, even under isometric conditions of the whole muscle, the
contractile elements shorten by stretching the elastic elements. Forty years
later, advanced optical techniques indicated that, during each of the three
types of contractions, the behavior of sarcomeres in series do not necessarily
mimic those of the fiber of which they are a part
(23,
28). Such heterogeneity of
sarcomere behavior, although of great significance as a determinant of muscle
performance (9,
22,
23,
28,
30,
38,
41), is not a factor in this
context. The focus of this discourse is the change in the end-to-end length of
single fibers or whole muscles.
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TERMINOLOGY
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Biophysicists or muscle mechanicists primarily interested in the mechanisms
of the actual contraction itself have tended to stay with accurate but wordier
constructs such as "stimulated muscles stretched during the active phase
of the contraction," "stretching a muscle during a tetanus"
(1), "forcible
lengthening of active muscles," or "lengthening of a stimulated
muscle" (35). For muscle
physiologists describing conditioning
(5) or contraction-induced
injury (40) protocols or
biomechanicists assessing contractions during human movements
(13,
24), a more concise
terminology is required. In an editorial in Biomechanics Journal in
1988, Peter Cavanagh (6)
recommended the replacement of the term "muscle contraction" with
"muscle action." His basic premise was that the great majority of
experiments in the "grand era" of muscle mechanics really were
concerned only with "shortening," and consequently these
investigators were not challenged by the concepts of contracting muscles being
stretched. In fact, throughout the grand era, presumably the 1920s and 1930s,
Levin and Wyman (34) and Hill
(21,
22) investigated the relation
between force and velocity during shortening and lengthening of stimulated
dog-fish and frog muscles in vitro. Fenn
(11–13),
Hill (22), and Katz
(30) investigated force and
heat production during shortening and the increase in force development and
the production of heat when stretches of constant velocity were applied to
sartorius muscles of frogs and toads during twitches or tetani. Concurrently,
Hill (20,
22), Fenn
(13), and Hubbard and Stetson
(24) performed sophisticated
experiments that correlated the three types of muscle contractions with the
movements of humans during walking and running. Consequently, the concept that
"lengthening contractions are as common as isometric, or shortening
contractions" was common knowledge to the muscle physiologists of the
1920s and 1930s
(10–12,
20–22,
31).
Furthermore, the premise that the term contraction is an outmoded term that
should be discarded and that the substitution of "action" or
"activation" for contraction would serve as "a signal of the
modern acceptance, derived from the biomechanical study of human
movement," of the need for a change in terminology
(6) has not happened. The
recommendation of any change from contraction has met with widespread
resistance, and few, if any, muscle physiologists have adopted such a change.
In everyday usage, action does not differentiate between the quiescent and the
activated states of muscle with the same clarity as contraction does. The
clarity is based on well over a century of consistent usage in scientific
journals that, when activated, the activated muscles undergo a sequence of
events termed contraction! The activation of muscle fibers is an all-or-none
phenomenon and is independent of the directionality, or lack of
directionality, of the subsequent contraction that the activation elicited.
Regardless of the external factors acting on the muscle, physiologically and
mechanically, during "shortening, isometric and lengthening
contractions," the sequence of events after activation of muscle fibers
is similar but not identical. With activation, muscle fibers contract:
globular heads of myosin attach to actin sites, undergo a transition to strong
binding, and then depending on the load proceed through some form of the
cyclical interactions between the myosin heads and the actin binding sites,
termed the "working stroke"
(26). During shortening, cross
bridges cycle through their working stroke, and energy expenditure is a
function of load and shortening velocity
(26). At loads greater than
muscle force, the stretch produces a reversal in the force-generating working
stroke, and energy expenditure is reduced
(35,
36). The conclusion is that
neither action nor activation provides an adequate substitute for
contraction.
Because the dictionary definition of "to contract" is "to
generate force" and "to shorten," a number of investigators
have modified the terms action
(15) and condition
(24) to signify the type of
contraction that occurred. Fick
(15) employed the terms
"isometric" and "isotonic" to describe the actions of
a contracting heart muscle when the muscle remained at a fixed length or
shortened with a fixed load. In 1938, Fenn
(12) noted that shortening,
isometric, and lengthening more accurately represented the three types of
contractions that muscles make than the terms proposed by Fick, but Fenn was
careful to dissociate the directionality of the muscle movement from the term
contraction. The same year, in correlating the contractions of muscles of
humans with the movements of the limbs during walking and running, Hubbard and
Stetson (24) recognized that
muscles underwent contractions during three different
"conditions." The three conditions were termed
"miometric," "isometric," and
"pliometric," by coupling the Greek prefixes "mio"
(shorter), "iso" (same), and "plio" (longer) to the
noun "metric," defined as "pertaining to measures or
measurement." Consequently, the noun condition was used with the
appropriate adjective to differentiate among the three conditions under which
the muscles "contracted."
The introduction of a second term, either action or condition, in
conjunction with contraction simply begs the issue as to what is actually
happening to the muscle during the contraction. Clearly, if an isometric or
lengthening action or condition occurs, the muscle cannot be shortening during
the contraction and any reference to shortening is simply redundant. In
actuality, investigators have been modifying contraction with adjectives that
are at odds with a definition of shortening continuously since 1927
(13,
21,
22,
30,
34), particularly with the use
of "isometric contraction"
(1,
13,
22,
30). After decades of ignoring
the problem, the only rationale conclusion is that the dictionary definition
of "to contract" specifically as pertaining to muscle must be
"to undergo activation and generate force."
An equally contentious issue is what adjectives should be applied to the
term contraction to best describe the lack of movement or the directionality
of the movement. Despite their early introduction, the terms miometric and
pliometric (24) have never
gained wide acceptance. In 1963, Fenn
(14) followed the lead of
Hubbard and Stetson (24); in a
comparison of the contractions of respiratory and limb muscles, he used
miometric, isometric, and pliometric as adjectives to modify contraction.
Following Fenn's lead, several unsuccessful attempts have been made to
reintroduce these terms (4,
25,
37,
39,
47). An additional deterrent
to the use of the term pliometric is the increased use of the term
"plyometrics" for conditioning with high-power jumps that involve
repeated, rapid, and forceful shortening and lengthening actions during almost
maximum activation of large muscle groups. Despite suggestions for other
terminology for this type of conditioning by Komi
(33) and later by Knuttgen and
Kraemer (26), the popularity
of "plyometrics" and the use of the term have increased
dramatically (7,
43).
Of greater concern has been the introduction and spread of inappropriate
adjectives to modify contraction. During the 1950s, the terms
"concentric" and "eccentric" contractions appeared
first in textbooks (29,
44) and later in the exercise
science literature (32). The
dictionary defines concentric as "circles with the same centers"
and eccentric as either "circles with different centers" or
"off-center." "Weird" or "unusual" as
other definitions of eccentric adds a further complication. Several efforts
have been initiated to discourage the use of these completely inappropriate
terms. In 1962, during a discussion on muscle performance chaired by D. B.
Dill (44), Erling Asmussen
used the terms concentric and eccentric and B. J. Ralston made the perceptive
comment that these terms led to confusion and should be eliminated from the
literature. Asmussen conceded that the terms miometric and pliometric might be
better, but Ralston responded that he preferred simply shortening or
lengthening. A poster by Faulkner and his associates at the American College
of Sports Medicine Meeting (1998) made a similar argument against the use of
concentric and eccentric and advocated miometric, isometric, and pliometric.
Presently, isometric is universally accepted, but shortening and lengthening,
miometric and pliometric, and concentric and eccentric are all in use in the
physiological, biomechanics, sports medicine, and sports science literature.
Despite their inappropriateness, the most commonly used expressions in the
conditioning and sports exercise papers are concentric and eccentric
contractions (31).
The misuse of the terms concentric and eccentric to describe the types of
contractions (3,
42) has extended to the type
of work (8), exercise
(10,
17), load
(16), training
(46), strength
(48), and actions
(6). A serious problem arises
from the use of concentric and eccentric as synonyms for shortening and
lengthening contractions of skeletal muscles. With either conditioning or
disease, the heart may undergo concentric or eccentric hypertrophy,
adaptation, or remodeling (2).
Subsequently, the heart makes contractions that are under concentric (on
center) or eccentric (off center) conditions. Despite the concentric or
eccentric condition under which the contractions occur, the activation of the
heart muscle would still produce a shortening contraction, an isometric
contraction, or possibly under unusual circumstances a lengthening
contraction. The inappropriate use of the terms concentric and eccentric in
muscle physiology, biomechanics, sports medicine, and sports science
literature and meetings makes any meaningful dialogue with cardiovascular
physiologists or cardiologists extremely difficult.
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RECOMMENDATION
|
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- The verb "to contract" and the nouns
"contraction" and "contractility" need to be defined
correctly in terms appropriate with long-term usage as "specifically for
muscle, to undergo activation and generate force." For 75 years,
muscle physiologists (13,
22,
34), biophysicists
(35), and biomechanicists
(24,
27) have utilized the terms
contract, contraction, and contractility successfully and unambiguously,
despite misleading dictionary definitions stipulating "to shorten"
or "to draw into a more compact form." The references to "to
shorten, or a drawing together and thickening" should be deleted from
the definitions, and the terms contract, contraction, and contractility should
be preserved by accurate and precise usage.
- To clarify the type of contraction, the adjectives that provide the
greatest clarity are "shortening," "isometric," and
"lengthening." One might argue for "fixed-end"
contraction rather than isometric, but slightly less than a century of usage
weighs heavily in favor of isometric. The adjectives shortening, isometric,
and lengthening convey immediately and without equivocation even to the
uninitiated the type of contraction that is occurring within the skeletal
muscle. The adjectives miometric, isometric, and pliometric have a certain
appeal based on their long-term usage and their Greek heritage, but
understanding their meaning requires a knowledge of the Greek prefixes mio,
iso, and plio. Although dictionaries define the prefixes as denoting shorter,
the same, and longer measures, respectively, dictionaries do not provide the
complete term with the exception of isometric. Clarity in the usage of
contraction requires an indication of the immediate outcome of the interaction
between the force generated by the muscle and the load against which the
muscle is "attempting to shorten" that result in either a
shortening, an isometric, or a lengthening contraction.
- The adjectives "concentric" and "eccentric" are
misleading and inappropriate and should not be used to describe the
contractions of skeletal muscles. The definitions of concentric as
"having the same center" and of eccentric as "not having the
same center" and consequently being "off center" are
consistent with the two different types of hypertrophy, adaptation, or
remodeling observed for the heart muscle
(2,
18,
19,
45). After concentric or
eccentric hypertrophy, adaptation, or remodeling of the heart muscle, the
totality of the heart will undergo a contraction under concentric or eccentric
conditions. If concentric and eccentric are used appropriately for the
condition of the heart, the terms make no sense when applied to contractions
of either heart or skeletal muscles.
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ACKNOWLEDGMENTS
|
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I acknowledge the many contributions of my colleagues and coworkers, Susan
V. Brooks and Dennis R. Claflin, for their extensive contributions, thorough
wide-ranging discussions, and innumerable readings of the manuscript extending
over many years. Gordon S. Lynch, now at the University of Melbourne,
Australia, was an enthusiastic discussant during his 2.5 yr in the laboratory
and beyond and also provided key textbook references on eccentric contractions
(27,
29,
44). Carol S. Davis assisted
with invaluable library and Med-Line searches for the wide range of
references.
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FOOTNOTES
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Address for reprint requests and other correspondence: J. A. Faulkner,
Institute of Gerontology, Univ. of Michigan, 300 North Ingalls Bldg., Rm. 960,
Ann Arbor, MI 48109-2007 (E-mail:
jafaulk{at}umich.edu).
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T. R. Bai, J. H. T. Bates, V. Brusasco, B. Camoretti-Mercado, P. Chitano, L. H. Deng, M. Dowell, B. Fabry, L. E. Ford, J. J. Fredberg, et al.
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M. A. Schrager, S. M. Roth, R. E. Ferrell, E. J. Metter, E. Russek-Cohen, N. A. Lynch, R. S. Lindle, and B. F. Hurley
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S. V. Brooks
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Copyright © 2003 by the American Physiological Society.
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