A STEP FORWARD FOR LOCOMOTOR MECHANICS
Brown University Thomas_Roberts{at}Brown.edu
|
Manter's study was built on a novel experimental tool, ingeniously applied.
From the earliest studies, researchers recognized that an accurate measurement
of forces produced by a runner or walker against the ground might yield
insight into how muscles power movement (Marey, 1874;
Fenn, 1930;
Elftman, 1939
). Marey's clever
pneumatic devices were the first force platforms, followed by Fenn's
spring-based device and arrays of deformable rubber pyramids used by H. O.
Elftman. Working with Elftman, Manter designed and built a spring-based
platform, with a lever system to magnify small deflections as the platform was
loaded by an animal's weight. They visualized and measured the displacement of
these levers in the same high-speed film images used to record the positions
of the animal's limbs. Manter's elegant force plate design stands out from
others because it was the first to record forces in three axes
vertical, foreaft and lateral and therefore is the prototype of
the modern force plate used in biomechanics research as well as clinical
orthopedics. It is only recently that an analogous tool has become available
for those interested in forces produced by swimming and flying animals.
Particle image velocimetry is currently providing the same kind of fundamental
insights into movement in fluid media that force plates have provided into
terrestrial locomotion over the past century (Lauder and Drucker, 2004;
Tobalske et al., 2005).
The real power of Manter's work resulted not from the design of his force
plate, but from its application as a tool for measuring mechanical work. From
the early 20th century, oxygen consumption measurements quantified the
metabolic energy used by muscles during walking and running. A better
understanding of running and walking mechanics promised to reveal, as H. O.
Elftman summarized, `the use to which this energy is put'
(Elftman, 1940). Early studies
of the mechanical work of running relied on high-speed film measurements of
the movements of the body and limbs. Each step a runner takes involves cyclic
fluctuations in the kinetic and potential energy of the body and limbs, and
these energy changes can be calculated from known limb dimensions and
movements. Film-based measurements, however, suffer from the fact that the
body's center of mass cannot be identified by an obvious anatomical landmark,
and its location varies with changes in posture.
Manter recognized that his force plate could provide an alternative to film
as a method for measuring body movement. The forces on the body are related to
its acceleration according to Newton's second law
(force=massxacceleration), and velocities and positions can be
determined by integrating accelerations. From body position and velocity,
changes in potential and kinetic energy can be calculated. Manter applied this
approach to walking cats, and concluded that it was superior to film-based
methods. This approach was ultimately developed rigorously and dubbed
`force-plate ergometry' by Cavagna and coworkers
(Cavagna et al., 1964;
Cavagna, 1975
). This method has
been an essential tool for investigating how the mechanical work of walking
and running relates to metabolic energy consumed, a topic that continues to
motivate locomotor research today (e.g.
Taylor, 1994
;
Marsh et al., 2004
;
Griffin et al., 2003
).
It turns out that relating the mechanical work of walking and running to
the metabolic energy muscles consume is not so easy, primarily because much of
the work is done not by muscles but by passive mechanisms. Manter recognized
one of the most important of these when he observed that not all of the
increases in the body's kinetic energy in each step had to be supplied by
muscle work, but could instead result from a transfer of energy from potential
to kinetic. This kind of exchange explains how a pendulum maintains a lot of
motion without much energy input. Since walkers vault over the limb with each
step, the cyclic exchange of the body's potential and kinetic energy has been
termed the `inverted pendulum' mechanism
(Cavagna et al., 1977). Studies
including a diverse assemblage of animals, from rams and turkeys
(Cavagna et al., 1977
) to crabs
(Full, 1989
) and frogs
(Ahn et al., 2004
), have
demonstrated that this mechanism is nearly universal among walkers. Recent
studies of slightly unusual walkers provide exceptions that prove the rule:
penguins pendulum in a side-to-side waddle
(Griffin and Kram, 2000
), and
Galapagos tortoises are the first documented examples of animals that walk
without any pendulum mechanism at all
(Zani et al., 2005
). Our
understanding of the inverted pendulum mechanism has not only informed
biologists. A pendulum-like mechanism has been incorporated into many robots
that walk. Robot designers have found that mimicking nature's walkers
simplifies control and improves energy efficiency
(McGeer, 1990
; Collins et al.,
2004).
Manter's study appears to be the first to combine simultaneous measurements
of individual foot forces and film to use the modern inverse dynamics approach
to estimate the muscle forces acting at individual joints. This non-invasive
method of determining muscle function is still used in clinical gait analysis.
As a research tool, it has provided a wide range of insights into locomotor
function, including the change in limb posture with size in mammals
(Biewener, 1990), the
mechanical role of biarticular muscles
(van Ingen Schenau, 1992
;
Jacobs et al., 1996
), and the
motor coordination of movement (Zajac et al., 1981; Winter, 1990). Manter's
inverse dynamics analysis of cat walking led him to conclude that some muscles
may act isometrically to effectively produce high forces, an idea that has
recently received renewed interest (Taylor et al., 1994;
Roberts et al., 1997
;
Fukunaga et al., 2001
).
Manter's study includes elegant diagrams and a clear description of the
force-plate-based inverse dynamics calculations. It is unclear why Elftman's
paper published the following year is usually cited as the definitive inverse
dynamics paper (Elftman, 1939).
Elftman's subjects were human rather than feline, but adapting the approach
from cats to humans requires only a change in the constants used for the mass
and dimensions of the limbs.
Is Manter's paper a forgotten classic? A survey of modern citations of Manter's paper suggests that his work has been cited extensively in some fields but left behind in others. Citations to this paper are well-represented in the physical anthropology literature, spotty in the comparative locomotor mechanics literature, and almost completely absent from the extensive literature on human locomotor mechanics and inverse dynamics. For both its technical prowess and its insights into questions still under debate today, this JEB classic is worth a second look.
Footnotes
Thomas Roberts writes about J. T. Manter's classic 1938 study of the dynamics of quadrupedal walking.
A PDF file of the original paper can be accessed online: http://jeb.biologists.org/cgi/content/full/208/22/4191/DC
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