|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online September 19, 2006
Journal of Experimental Biology 209, 3925-3939 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02400
Sagittal spine movements of small therian mammals during asymmetrical gaits
1 Institute of Systematic Zoology and Evolutionary Biology,
Friedrich-Schiller-University, Erbertstrasse 1, 07743 Jena, Germany
2 Museum National d'Histoire Naturelle, USM 302 / FRE 2696 CP 55, Pavillon
d'anatomie comparée, 57, Rue Cuvier, 75231 Cedex 05, Paris,
France
* Author for correspondence (e-mail: nadja.schilling{at}uni-jena.de)
Accepted 22 June 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: intervertebral joints, locomotion, vertebral column, kinematic, X-ray, spinal flexion
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Hildebrand, 1959;
Gambaryan, 1974;
Hildebrand, 1974). Mammals are
the only tetrapods that show asymmetrical gaits regularly [beside young
galloping crocodiles (Zug,
1974; Webb and Gans,
1982)].
According to Alexander et al., the gallop is suggested to be the most
efficient mode of locomotion (Alexander et
al., 1985). Sagittal spine movements are used to increase hindlimb
retraction velocity but also step length, and thereby animal's speed
via the integration of a long aerial phase and extended stance and
swing phases (Howell, 1944;
Hildebrand, 1959). In small
therian mammals, about half of the stance length is contributed by sagittal
bending movements (Fischer,
1994; Fischer and Lehmann,
1998; Schilling and Fischer,
1999; Fischer et al.,
2002). Nearly half of the metabolic costs can be saved by the
storage of elastic energy in the large thoracolumbar aponeurosis as well as in
the paravertebral musculature itself
(Cavagna et al., 1977;
Taylor, 1978;
Alexander et al., 1985;
Alexander, 1988;
Koob and Long, 2000;
Fischer and Witte, 2004;
Hackert, 2002). Additionally,
metabolic costs can be reduced by the use of natural resonance frequencies
during fast locomotion (`preferred traveling speed')
(Koob and Long, 2000).
Furthermore, sagittal oscillations of the body axis drive lung ventilation in
mammals during locomotion (`visceral piston model')
(Bramble and Carrier, 1983;
Bramble, 1989;
Bramble, 1999).
The synchronous motion and the touching down of both hindlimbs at the same
spot were suggested as characteristics that stabilize the locomotion of
asymmetrical gaits (Howell,
1944; Goslow et al.,
1973; Hildebrand,
1974; English,
1980). Furthermore, trunk movements that induce cyclic horizontal
displacements of the centre of body mass (CoM) and the strength of the back
movements can be interpreted as ways to adjust the optimal angle of attack of
forelimbs [`CoM-shifting hypothesis'
(Hackert, 2002;
Hackert et al., 2006)] and
thus using self stabilizing mechanisms [i.e. mechanical stability of a system
without the need of sensory feedback
(Wagner and Blickhan, 1999;
Blickhan et al., 2003)].
Flexions of the spine are thought to decrease vertical excursions of the CoM
and consequently reduce the need of compensatory limb movements
(Hackert, 2002).
Despite the well-known impact of trunk movements on mammalian locomotion,
only limited information is available for the kinematics of spinal movements.
It is generally accepted that all spine movements are the result of small
intervertebral movements that add up to what is called `pelvic motion'. Owing
to the rigid connection of the pelvis to the vertebral column, movements in
the iliosacral joint are restricted. No movements were observed in this joint
during locomotion in a number of small mammalian species including the species
studied herein. Therefore, we can conclude that movements in the iliosacral
joint have no influence on locomotion and do not contribute to pelvic
displacements in the species under study
(Kühnapfel, 1996;
Fischer and Lehmann, 1998;
Schilling and Fischer, 1999;
Fischer et al., 2002). In
symmetrical gaits (e.g. walk and trot), back movements are composed of lateral
movements in the horizontal plane and rotational motions around the
craniocaudal body axis [lateral bending and tilting, respectively
(Jenkins, Jr and Camazine,
1977)]. In asymmetrical gaits, spine motion is restricted to
dorsoventral flexion and extension movements in the sagittal plane.
Much information is available for back movements of walking or trotting
mammals [e.g. horses (Audigie et al.,
1999; Faber et al.,
2001; Haussler et al.,
2001; Licka et al.,
2001; Robert et al.,
2001); dogs (Tokuriki,
1973a; Tokuriki,
1973b; Tokuriki,
1974; Jenkins, Jr and
Camazine, 1977; Ritter et al.,
2001); foxes (Jenkins, Jr and
Camazine, 1977); cats (Jenkins
and Camazine, 1977; Carlson et
al., 1979; English,
1980); raccoons (Jenkins, Jr
and Camazine, 1977); skunks
(van der Graaff et al., 1982);
ferrets (Kafkafi and Golani,
1998); tree shrews (Jenkins,
Jr, 1974; Schilling and
Fischer, 1999); primates
(Shapiro et al., 2001); and
grey short-tailed opossums (Pridmore,
1992)]; however, little information is available for asymmetrical
gaits. Most studies investigated either `pelvic motion'
(Hildebrand, 1959;
Jenkins, Jr and Camazine,
1977; Fischer et al.,
2002) or X-rays of manipulated cadavers to comprehend the observed
`pelvic movement' (Alexander et al.,
1985; Fischer,
1994; Carlson,
1978). Some more detailed data were published only for the pika
(Fischer and Lehmann, 1998).
The first study analyzing intervertebral joint movements in symmetrical and
asymmetrical gaits was published for the tree shrew
(Schilling and Fischer, 1999).
This study exposed the restricted bending region between the eleventh thoracic
and the first lumbar vertebrae, reported by Jenkins, Jr
(Jenkins, Jr, 1974), as valid
only during exploratory walking.
Often external skin markers or the body contours were used to evaluate
spinal movements. But as intervertebral movements are hidden by movements of
fur, skin and subcutaneous tissues, external marker studies are tainted with
unavoidable errors. However, 3-8 skin markers along the body were used to
represent vertebral column movements and analyze spinal motions in the studies
named above. Especially in small to medium sized mammals, cineradiography is
the only tool available to measure intervertebral movements at each segmental
level (Schilling and Fischer,
1999). Only Jenkins, Jr
(Jenkins, Jr, 1974), van der
Graaff et al. (van der Graaff et al.,
1982), Pridmore (Pridmore,
1992), Fischer and Lehmann
(Fischer and Lehmann, 1998),
Faber et al. (Faber et al.,
2001) and Haussler et al.
(Haussler et al., 2001) used
either X-ray or highly invasive bone-fixed markers and were therefore able to
resolve questions concerning segmental motions.
During the evolution of tetrapods, the non-regionalized vertebral column
was subdivided into two anatomically and functionally different regions -
thoracic and lumbar (Gadow,
1933). Sagittal spine movements are thought to be restricted to
the lumbar part only, whereas the thoracic region, as a part of the rib cage,
is thought to be rigid to secure respiration during locomotion and counteract
loading forces transmitted to the chest wall from limbs.
In order to determine how the vertebral column is involved in sagittal
spine movements, intervertebral joint movements were studied in small mammals
during asymmetrical gaits using cineradiography. Adults of five distantly
related therian species with different body forms (two `tailless' and three
with long tails) were investigated during treadmill locomotion. The aims of
the study were (1) to determine the region of the vertebral column involved in
sagittal bending, (2) to determine the amplitudes and timing of intervertebral
movements, 3) to determine the contribution of different intervertebral joint
movements to the resulting `pelvic motion', and (4) to compare the pelvic
displacement between tailed and `tailless' species to examine the influence of
the tail on spinal kinematics. Although kinematic data of `pelvic movements'
were published earlier (Fischer et al.,
2002), new data were collected for all species in order to combine
the intervertebral joint movements with the resulting `pelvic movements'.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Fischer and Lehmann, 1998;
Schilling and Fischer, 1999;
Fischer et al., 2002;
Schilling, 2005b). Out of the
same data pool, film sequences were selected for the current study (see
below). Because no differences in the kinematic parameters were observed among
the individuals of the same species in the studies cited above, data were
collected only for one individual per species for the current study (tree
shrew: 0,1; 151 g; kowari: 1,0; 145 g; grey short-tailed opossum: 1,0; 92 g;
cui: 1,0; 207 g; pika: 1,0; 250 g). The pelvic displacements, i.e. the outcome
of all additive intervertebral movements, observed in the current study
matched particularly well with previously reported results. Because of the
consistency of these results, we feel confident that the data presented here
are representative for the species although only one individual per species
has been studied. Although trunk movements have been analyzed in the tree
shrew in an earlier study (Schilling and
Fischer, 1999), new data were collected to guarantee the same
procedure of analysis for all species.
|
), we
assume that this preferred speed can be compared between the species.
Intervertebral movements were recorded by high-speed cinevideography (150
frames s-1) taken at the IWF Knowledge and Media gGmbH at
Göttingen, Germany (Fig.
1). The X-ray system consisted of an automatic X-ray source image
amplifier chain (Phillips 9807 501 800 01, Germany). Pulsed X-ray shots (57-82
kV, 200 mA) were applied. Images from running animals in lateral perspective
were recorded from the image amplifier (205 mmx150 mm) using the
high-speed video system Camsys® (Mikromak Service K. Brinkmann, Berlin,
Germany). All experiments were approved by the Committee for Animal Protection
of the State of Thuringia, Germany.
Data analysis
The analogue videotapes were converted with a video processing board
(`Screen machine I', FAST Multimedia AG, Munich, Germany). The sequences
analyzed were selected from our working group's data pool using the following
criteria. Only trials with continuous motion and at least five successive
strides were used. All landmarks had to be visible at all times. Because the
trunk length of the species investigated (up to 200 mm) was almost the same as
the size of the image amplifier and the X-ray equipment was fixed and could
not follow the animal's motion along the treadmill, the number of usable
sequences was dramatically reduced. Finally, all strides analyzed were taken
from the same film sequence and were further processed as one-motion sequences
(e.g. mean curves, filtering, etc.) but presented separately according to
their classification as gallop or halfbound (e.g. in the kowari and the grey
short-tailed opossum).
|
The accuracy of capturing the skeletal landmarks was affected by both the contrast of bones and the distances between neighbored landmarks. The shorter the distances the noisier the resulting data were. As a result, the captured coordinates were tainted by a given amount of noise due to digitizing and this propagated up to angular values. We used the Fast-Fourier transformation (FFT) to filter out high-frequency digitizing errors from the lower frequency sinusoid oscillations characterizing the intervertebral angular movements. In the signal time series, digitizing errors were represented by deviations from the `expected', real value that occurred over three consecutive frames, i.e. over a time interval of two or three sampling periods, rarely more. Digitizing errors were then included in the high frequency terms of the Fourier spectrum of the signal. At the sampling frequency of 150 Hz, errors were included in the terms corresponding to 75 Hz and 50 Hz. For a typical running frequency of four steps per second, those frequencies corresponded to oscillations which were nine times faster than the basic oscillation of the signal. In order to prepare the data for the FFT, the data series with some 210 frames, representing five locomotor cycles, were interpolated by cubic splines to become series containing a number of elements equal to a power of two. A FFT was then applied to the series. The coefficients corresponding to 75 Hz and 50 Hz were set to zero. The low frequency of the signal (up to 37.5 Hz) was preserved and transformed back using inverse FFT. The digitizing error for the pelvic landmarks was tested by repetitive digitization (five times) of five frames for each species. It ranged from 1° to 2°.
Only data of the intervertebral joints involved in sagittal bending indicated by frequencies similar to that of `pelvic movements' were further processed. Mean touch-down and lift-off angles, effective angular movements, maximum and minimum angles during stance and swing phases, and maximum angular movements of intervertebral joint angles as well as of `pelvic movements' were determined for trailing and leading limbs, separately, or for both hindlimbs (halfbound) and compared among the species (for definitions see Table 1). In the example of the galloping pika and the grey short-tailed opossum, mean curves of the intervertebral movements of five or six typical gait sequences were calculated in order to show the characteristics of intervertebral movements (see Fig. 4). For this, stance and swing phases were normalized to the same period using the method of linear interpolation.
|
|
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
In the kowari and the tree shrew, the tenth trunk vertebra is the so-called
`diaphragmatic' vertebra. At this vertebra, the orientation of the
zygapophyseal facets changes from a horizontal, `tangential' to an upright,
`radiär' orientation (Virchow,
1907). The diaphragmatic vertebra is situated more caudally in the
pika and the cui (eleventh and thirteenth thoracic vertebra, respectively).
The grey short-tailed opossum exhibits a diaphragmatic region, i.e. the change
of the facet orientation involves more than one vertebra
(Pridmore, 1992) (this study).
The orientation of the spinous processus changes at the anticline vertebra,
which is the tenth in the tree shrew, the twelfth in the pika and the grey
short-tailed opossum, and the thirteenth in the cui. In the kowari, the ninth
and the tenth thoracic vertebrae are involved in the change of the inclination
of the spinous processus (Table
2).
Gaits and `pelvic movement'
Altogether, 23-25 skeletal landmarks were captured in 862 frames for the
current study. Because left and right limbs cannot be identified in
cineradiography, trials were only categorized as either gallop or half-bound
without further classification (e.g. as transverse or rotatory gallop). The
pika, the tree shrew and the cui presented gallops defined by clearly
distinguishable trailing and leading hindlimbs. Time between the touching-down
of trailing and leading limbs ranged from one to three frames (6.7 ms to 20.0
ms) in the pika and one to four frames (6.7 ms to 26.7 ms) in the tree shrew
and the cui. Both metatherian species, showed transitions from gallop to
half-bound back and forth within the same film sequence. In the kowari, three
strides were halfbounds defined by the synchronous touching down of the
hindlimbs. In the other four strides, a time lag of one frame between the
touch-down of trailing and leading limbs was observed but only three of these
strides retained the lag until lift-off. In one stride, the lift-off of both
hindlimbs was synchronous. In the grey short-tailed opossum, six strides were
half-bound and four had a duration of 6.7 ms to 13.4 ms (1-2 frames) between
the touch-downs of both hindlimbs but no time between their lift-offs (except
for one stride with a time lag of 13.4 ms;
Fig. 3). The mean speeds for
the trials analyzed were: kowari, 0.92±0.06 m s-1; grey
short-tailed opossum, 1.15±0.19 m s-1; tree shrew,
1.48±0.15 m s-1; pika, 1.18±0.05 m s-1;
and the cui, 1.14±0.12 m s-1.
|
; Fischer and Lehmann,
1998; Schilling and Fischer,
1999; Fischer et al.,
2002).
Independent of the body form (tailed or `tailless'), effective angular movements of the pelvis during stance phase were of a comparable magnitude in all species (29° to 44°; Table 3). In the gallop, the effective `pelvic movement' was larger in leading than in trailing limbs in all species but the cui. Effective angular movement of the pelvis in the halfbound was similar to that of the leading limbs in the gallop within the same species (kowari, gray short-tailed opossum).
|
In general, maximum cranial displacement of the pelvis (protraction, minimum of stride) was reached within the last quarter of swing phase (i.e. before touch-down of the trailing limb in the gallop or before touch-down of both hindlimbs in the halfbound) (Fig. 3). Thus, the pelvis was already in retraction at touch-down. Maximum caudal displacement (retraction, maximum of stride) was usually observed between lift-off of the leading hindlimb (gallop) or of both hindlimbs (halfbound) and during the first quarter of swing phase. Thus, neither maximum cranial nor caudal displacements of the `pelvic movements' were strictly coupled with touch-down or lift-off events and both maximum pro- and retraction were observed during the swing phase. Mean amplitude of `pelvic movement' during swing phase was comparable between all species (40° to 51°; Table 3) and independent of the existence or absence of a long, external tail.
During stance phase, maximum cranial displacement of the pelvis occurred primarily at touch-down of the trailing limbs in the cui and at the touch-down of leading limbs in the kowari and the gray short-tailed opossum. Thus, the pelvis is briefly in protraction after touch-down of the trailing limbs in the two metatherians. A comparable protraction of the pelvis but after the touch-down of the leading limbs was observed in half of the strides of the pika (Fig. 4). In all other strides, minimum value during stance phase corresponded to the touch-down of the leading limbs. In the tree shrew, maximum protraction was observed either between the touch-down of trailing and leading limbs or at the touch-down of the leading limb. Consequently, maximum protraction during stance phase is not coupled with trailing or leading limbs. Furthermore, interspecific differences were observed. Subsequently, the pelvis was retracted continuously during stance phase in all species. Owing to the continuous retraction into the swing phase, maximum caudal displacement during stance phase corresponded to lift-off angles of trailing and leading limbs, respectively. In the halfbound, minimum and maximum values of `pelvic movement' during stance phase corresponded mostly to touchdown and lift-off angles, and therefore amplitudes were approximately the same as the effective angular movements. In all gaits, the pelvis was consecutively retracted after lift-off until the maximum caudal displacement during the swing phase was reached. The following protraction of the pelvis ended by reaching the maximum cranial displacement shortly before touch-down.
Despite comparable ranges of effective `pelvic movements' during stance phase and amplitudes during stance and swing phases, those ranges were covered by strikingly different pelvic positions. Mean touch-down angles were particularly low in the pika with a nearly vertical pelvic position (109° for leading limb; Table 3) and were higher in all other species (127° to 135°). At lift-off, the pelvis was almost horizontal in the gray short-tailed opossum, the tree shrew and the cui (168° to 176°), slightly more inclined in the kowari (160° to 164°), but most inclined in the pika (147° and 151° for trailing and leading limbs, respectively). Thus, the pelvis of the pika was oriented vertically at the beginning of stance phase and reached a more inclined position at the end of stance phase, whereas the other species started with a less protracted pelvis and ended by a nearly horizontal position at lift-off (Figs 1 and 3).
Intervertebral movements
Independent of their regional classification as `lumbar' or `thoracic', six
to eight presacral intervertebral joints were involved in the additive
sagittal spine movements in all species but the cui
(Table 3). Therefore, sagittal
intervertebral joint movements were observed in the caudal thoracic and the
lumbar parts of the pika (up to T14/15), the tree shrew (up to T11/12), and
the gray short-tailed opossum (up to T13/14), and were restricted to the
lumbar region in the kowari (up to L2/3) and the cui (up to L3/4). In general,
effective angular movements of the intervertebral joints craniad from PS3
ranged between 1° to 9° in all species. Slightly higher values were
often found in the second presacral joint (PS2). In the gallop, the highest
effective angular movements occurred in the first presacral joint in all
species (PS1: 7° to 22°). Among the species, the highest values were
observed in the tree shrew and the kowari (17° to 22° for trailing and
leading limbs) and the lowest values in the pika (7° and 8° for
trailing and leading limbs, respectively).
The timing of intervertebral movements during galloping was highly similar among the species. In general, maximum spinal flexion was not connected to the touch-down events, furthermore, it was observed between the last third of swing phase and touch-down events. Therefore, extension of the vertebral column started in the late swing phase. More cranial parts of the vertebral column often extended earlier than more caudal ones (Figs 3 and 4), but no strict craniocaudal order between adjacent intervertebral joints was observed. However, toward the caudal end of the trunk, the described timing pattern was increasingly pronounced. At touch-down of trailing and leading limbs, all intervertebral joints were still essentially flexed in all species as indicated by intervertebral joint angles of less than 180° (Table 3, Fig. 4). Only in the cui, the first presacral intervertebral joint (PS1) was still slightly extended (181°-183°).
During stance phase, the vertebral column was extended continuously in all involved presacral intervertebral joints (Table 3). Maximum angular excursions of the first up to the sixth presacral joints were comparable to the effective angular movements, respectively, because maximum extension of this region is reached after lift-off. Therefore, maximum values of stance phase and lift-off angles often corresponded to each other. But, amplitudes of more cranial intervertebral joints (craniad from PS6) were higher than effective angular movements during stance phase due to craniocaudal progression of extension. At the moment of lift-off of trailing and leading hindlimbs, the more caudal intervertebral joints were often flexed dorsally as indicated by values above 180° (Table 3). After lift-off of leading limbs and within the first quarter of swing phase, the vertebral column was extended until maximum extension was reached. In some species, the back was clearly extended dorsally (lordosis; e.g. in the kowari, Fig. 1). Synchronously, ventral flexion started in the more cranial parts of the vertebral column. Caudal parts of the trunk were flexed in the second quarter of swing phase. In general, maximum angular excursions were higher during swing phase than during stance phase. Again, the highest values were observed in the first presacral joint in all species. The closer touch-down or lift-off events of both hindlimbs became, i.e. the more synchronously both hindlimbs moved (up to halfbound) the more stereotypic the described motion pattern became.
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Hildebrand, 1959;
Gambaryan, 1974). A number of
studies have shown that sagittal bending movements have a major impact on
mammalian locomotion and that asymmetrical gaits are the most efficient mode
of locomotion (Howell, 1944;
Slijper, 1946;
Hildebrand, 1959;
Gambaryan, 1974;
Hildebrand, 1974;
Taylor, 1978;
English, 1980;
Pridmore, 1992;
Alexander et al., 1985).
According to Hildebrand, sagittal spine movements occur typically in fast
carnivores, lagomorphs and rodents
(Hildebrand, 1985). As this
study shows, as well as previous investigations, sagittal bending is more
widespread among eutherian and also metatherian mammals
(Pridmore, 1992;
Schilling and Fischer, 1999)
(this study). This is clearly in contrast to Reilly and White
(Reilly and White, 2003), who
argued that some metatherians, including the gray short-tailed opossum studied
herein, do not exhibit asymmetrical gaits because of their epipubic bones
which are part of a kinetic linkage. This cross-couplet kinetic connection
between the hindlimb and the abdominal body wall is presumed to restrict the
animals to symmetrical gaits (Reilly and
White, 2003). But the use of asymmetrical gaits in the gray
short-tailed opossum has been reported earlier and its locomotor parameters
have been analyzed quantitatively
(Pridmore, 1992;
Kühnapfel, 1996;
Fischer et al., 2002).
However, the investigated marsupials showed both gallops and half-bounds in
the recent study and they switched between these gaits within the same running
trial back and forth several times. This phenomenon of changing gaits
frequently has been observed earlier in a number of small- to medium-sized
therian mammals in symmetrical and in asymmetrical gaits
(Fischer and Lehmann, 1998;
Schilling and Fischer, 1999;
Fischer et al., 2002;
Schilling, 2005b). That means
that in the named studies the experimenters either always happened to end up
at the animal's `transition speed' (i.e. the speed at which they change gaits)
or this is a characteristic inherent to smaller mammals. Since it was observed
in many species and at different speeds it may be a feature of smaller therian
mammals. This is supported by the observation that small mammals often use
different gaits at the same velocities, which results in a large overlap
between speed and used gaits
(Kühnapfel, 1996;
Fischer and Lehmann, 1998;
Schilling and Fischer, 1999;
Fischer et al., 2002). Being
close to the `transition speed' might actually be an advantage for the animal
in order to make use of the gait that is to be preferred for the next strides.
Because for a small animal the environment is highly irregular and structured
in relation to its body size (Jenkins, Jr,
1974) adjustments in the locomotor parameters have to be made more
frequently than in larger animals.
In the current study, the sagittal bending was investigated at preferred
speed of the animal because animals prefer certain speeds to make use of
natural resonance frequencies [`traveling speed'
(Koob and Long, 2000)]. We
assume that this preferred traveling speed can be compared between the
species. Therefore, the analysis was performed on running sequences at
whatever speed the animal chose; no effort was made to analyze either
increasing or decreasing velocities or different speeds. Whereas larger
mammals increase their speed by increasing step length
(Heglund and Taylor, 1988),
which results in a speed sensitivity of locomotor parameters such as
kinematics and kinetics, small mammals accelerate by increasing their step
frequency. In particular, the species studied herein increased velocity at
asymmetrical gaits by increasing their step frequency and prolonging their
suspension period. Touch-down and lift-off positions of the limbs as well as
stance length were independent of speed and therefore, the same kinematics can
be expected at different velocities. Speed independency of limb kinematics has
been shown for a tenfold range of speed in more than 300 strides for the pika
(Fischer and Lehmann, 1998).
In addition, speed independency of kinematic parameters was reported for the
kowari and the gray short-tailed opossum
(Kühnapfel, 1996), for
the tree shrew (Schilling and Fischer,
1999), and for the guinea pig, a close relative of the cui
(Rocha-Barbosa et al., 1996;
Rocha-Barbosa et al., 2005).
In particular, the detailed study on speed sensitivity of limb kinematics in
the guinea pig showed that, although most joint angles were affected as speed
increased, only a few angles were correlated to speed. In the hindlimb, only
the flexion amplitude and the extension angular velocity of the knee joint was
related to increasing speed (Rocha-Barbosa
et al., 2005). Because of speed independency of limb kinematics
including the pelvic motion (i.e. the outcome of all sagittal spine
movements), we can expect the same trunk kinematics at different speeds for
the species under study.
Timing of the sagittal spine movements
Hildebrand suggested that spinal flexions and extensions are coupled in
their timing to the trailing limb
(Hildebrand, 1959). This is in
contrast to the results of the current study. In all species, maximum dorsal
or ventral flexions were usually observed in the swing phase and they were not
coupled with touch-down or lift-off events. Hildebrand's observation on the
cheetah (Hildebrand, 1959) was
drawn from a Walt Disney video (60 Hz). Therefore, the observed coupling of
spinal motions to the trailing limb could be the result of the low temporal
resolution. Our results confirm Gambaryan's observations
(Gambaryan, 1974), who
reported the maximal flexion of the spine before touch-down and the maximal
extension shortly after lift-off of the hindlimbs. In the galloping cat, a
marked flexion of the spine was observed during E1-phase of the step (=first
extension phase of the knee-joint, i.e. second half of swing phase) and the
following extension continued during E3 (i.e. second half of stance phase) and
into the following F epoch (=flexion, i.e. first half of swing phase)
(English, 1980). The timing in
the galloping cat is therefore similar to the timing found in smaller
mammals.
Although for none of the species investigated in the recent study airflow
measurements exist, our observations of the timing of the vertebral column
movements are in accordance with airflow measurements in galloping mammals.
Surprisingly, these descriptions of the timing of the ventilatory cycle were
based on the timing of forelimb's support, although it is well known that lung
ventilation is driven by oscillations of inner organs and thus by those of the
spine (e.g. Bramble, 1989;
Bramble and Jenkins, Jr, 1993;
Simons, 1999). However,
expiration was generally observed during stance phase and inspiration during
swing phase of the forelimbs in several galloping mammals
(Attenburrow, 1982;
Bramble and Carrier, 1983;
Bramble, 1989;
Young et al., 1992;
Simons, 1999). Inhalation
began after lift-off of the leading forelimb
(Bramble, 1989) and thus
shortly before the touch-down of the hindlimbs. At the same time, maximum
flexion of the spine was reached and the extension of the vertebral column
started (Fig. 1). Exhalation
onset was observed shortly after the impact of the trailing forelimbs [hard
contact (Bramble, 1989)].
Synchronously, hindlimbs were at lift-off or within the first quarter of swing
phase and the maximum extension of the spine was reached, i.e. flexion
movements just started (Fig.
1). Thus, the timing of maximum flexion and extension of the back
corresponds to that of the ventilator cycle in mammals and supports the
`visceral piston model' (Bramble and
Carrier, 1983).
Spinal extensions started before touch-down, resulting in a retraction of
both hindlimbs prior to ground contact. Retraction of fore- and hindlimbs
prior to touch-down was shown by several studies to be a common feature of
mammalian locomotion (Fischer,
1994; Fischer and Lehmann,
1998; Schilling and Fischer,
1999; Schmidt and Fischer,
2000; Fischer et al.,
2002; Schmidt,
2005) and was observable in different gaits and even during the
first postnatal steps (Schilling,
2005b). Using a conservative spring-mass model as well as a
biomechanical model for fast, quadrupedal locomotion, studies have examined
the effect of the limb's retraction in order to test its influence on running
stability (Herr et al., 2002;
Seyfarth et al., 2003). In all
models, pre-stance leg retraction enhanced stability significantly. Therefore,
the spinal extension prior ground contact of either trailing and leading limbs
at the gallop or both hindlimbs at the halfbound can be interpreted as a
feature that stabilizes the motion.
Sagittal bending and regionalization of the trunk
It is generally accepted that spinal movements are the result of small
additive movements between adjacent intervertebral joints. Due to the less
flexible thoracic (rib-bearing) region in comparison to the lumbar (ribless)
region (Rockwell et al.,
1938), dorsoventral flexions and extensions of the vertebral
column are generally thought to be restricted to the lumbar region of the
vertebral column (Slijper,
1946; English,
1980; Hildebrand,
1985; Fischer and Lehmann,
1998). The thoracic region is assumed not to be involved in
sagittal spine movements in order to allow the respiratory function of the
thorax. However, the current study showed that the caudal thoracic
intervertebral joints were involved in sagittal bending movements in at least
some species.
Independent of their regional classification as lumbar or thoracic, 7±1 presacral intervertebral joints contributed to sagittal spine movements in the therian mammals under study (except the cui). Whereas in the kowari and the cui, sagittal spine movements were restricted to the lumbar region (up to L2/3 and L3/4, respectively), the last caudal thoracic intervertebral joints were involved in sagittal bending movements in the gray short-tailed opossum (up to T13/14), the tree shrew (up to T11/12) and the pika (up to T14/15). Thus, the number of intervertebral joints taking part in sagittal bending was not correlated with the transition of the thoracic to the lumbar region in the species under study. Furthermore, the comparison of the number of thoracic intervertebral joints to the number of free ribs occurring in the caudal thoracic region in the different species, does not point to a simple relationship between the morphology of the skeleton and the observed sagittal bending.
Although the trunk vertebrae of mammals are usually classified into
thoracic and lumbar groups, they can also be divided according to their
orientation of the zygapophyseal facets into pre- and postdiaphragmatic
vertebrae. Additionally, the vertebral column has been divided according to
the inclination and width of the spinous processus into a region anterior and
a region posterior to the anticline vertebra
(Virchow, 1907;
Fick, 1911;
Rockwell et al., 1938;
Slijper, 1946;
Gambaryan, 1974;
Boszczyk et al., 2001).
According to Slijper (Slijper,
1946), the diaphragmatic vertebra or the diaphragmatic region
(i.e. when the change of the facet orientation involves more than one
vertebra) is of major importance for the axes of motion along the vertebral
column. In the anterior, prediaphragmatic region, the vertebrae possess more
or less horizontally oriented zygapophyseal facets [`tangential' after
(Virchow, 1907)], whereas in
the postdiaphragmatic part, the facets are more upright and lie in an
approximately parasagittal plane [`radiär' after
(Virchow, 1907)]. Virchow
referred to a `Wechselwirbel' that points to the junction of fore- and
hindlimbs' impact on the vertebral column
(Virchow, 1907). However,
several authors have pointed out that the horizontal orientation of the facets
in the anterior trunk allows for lateral bending and tilting movements but
restricts sagittal bending, whereas the parasagittal orientation of the facets
in the postdiaphragmatic region permits sagittal bending but restricts lateral
bending or tilting (Rockwell et al.,
1938; Slijper,
1946; Washburn and
Buettner-Janusch, 1952). According to Fick, the size of the
zygapophyseal articular surface points to the amount of intervertebral joint
movements (Fick, 1911).
If the zygapophyseal orientation influences the trunk bending, sagittal
bending should only be observed in the postdiaphragmatic region. In all
species, sagittal spine movements clearly occurred in the postdiaphragmatic
region, but in none of the species was there a simple relation to the
zygapophyseal facetation. The diaphragmatic, as well as the anticline vertebra
is situated clearly more anterior than the intervertebral joints involved in
sagittal spine movements. That means, neither the change of the facet
orientation nor the change in the spinous process orientation were related to
the region of the vertebral column used for sagittal bending. Although
Pridmore (Pridmore, 1992) did
not analyze the trunk movements in the gray short-tailed opossum
quantitatively, he pointed out that trunk bending during locomotion cannot be
related simply to the zygapophyseal facetation.
Our observation that sagittal bending can involve caudal thoracic parts is
in contrast to Fischer and Lehmann
(Fischer and Lehmann, 1998),
who reported a restriction of sagittal bending in the lumbar region in the
pika. However, they used only five skeletal landmarks along the vertebral
column to analyze its motion and did not therefore investigate intervertebral
movements. A restricted region of sagittal flexions and extensions between
Th11 and L1 was reported for the tree shrew
(Jenkins, Jr, 1974) and has
been validated for exploration walks only
(Schilling and Fischer, 1999).
The observation that also the caudal thoracic part of the vertebral column is
involved in sagittal bending movements was reported earlier for the tree shrew
(Schilling and Fischer, 1999)
and was confirmed by the current results. Furthermore, it was demonstrated for
other therian species as well by the recent study.
The amplitude of intervertebral joint movements varied slightly between the
joints, the species, and between gaits, but the highest values were always
observed in the last presacral joint. The highest mobility was also found in
the presacral joint during manipulation of the anesthetized cat
(Carlson, 1978) and the rock
hyrax (Fischer, 1998). Despite
the different directions of movements at symmetrical gaits in comparison to
asymmetrical gaits (tilting and lateral bending versus sagittal
bending), the largest motion was also measured at the lumbosacral junction in
horses (Haussler et al.,
2001).
Sagittal spine movements and its engine - the paravertebral musculature
The mammalian paravertebral musculature is organized in long muscle tracts
that enable the high mobility of the vertebral column especially in the
horizontal and sagittal planes. Particularly, the longissimus and the
iliocostalis tracts were strengthened and gained importance in axial motion in
mammals. Neither epaxial nor hypaxial muscles are restricted exclusively to
the thoracic or the lumbar region of the vertebral column, furthermore they
form long, fused muscle tracts that extend between the head and the pelvis.
Long back muscles dorsal to the vertebrae, such as the sacrospinalis muscle
(mm. longissimus lumborum et iliocostalis), are responsible for extensions of
the vertebral column, whereas longitudinal muscles ventral to the vertebral
column, such as the psoas muscles and the rectus abdominis muscle, are
involved in flexions of the back (Slijper,
1946; English,
1980; Alexander,
1988).
The sacrospinalis muscle originates via the large thoracolumbar
fascia from the spinous processus, the sacrum and the pelvis. It inserts onto
the caudal, free ribs and the transverse processus of the vertebral column
(Slijper, 1946;
Cooper and Schiller, 1975;
Alexander, 1988;
Schilling, 2005a). Thus, it
spans over the complete lumbar region to the caudal thoracic portion of the
vertebral column. Therefore, it is not surprising that the observed sagittal
spine movements were not obligatorily restricted to the lumbar region of the
vertebral column but rather involve 7±1 intervertebral joints
independent of their classification as thoracic or lumbar vertebrae.
The long, multisegmental muscle tracts found in amniotes fused from the
ancestral, segmental organization of the paravertebral musculature in basal
vertebrates, e.g. fishes and amphibians, but the plesiomorph segmental
organization is still recognizable by the innervation of the muscle tracts in
mammals (Schilling et al.,
2005). Therefore, a tendency of craniocaudal progression of
dorsoventral flexions of the vertebral column was observed in the current
study but because of the fusion of the muscle fibers no strict craniocaudal
sequence of consecutive intervertebral joints was found. This supports the
observation of English, who recorded the activity along the m. longissimus
dorsi in galloping cats at four different lumbar vertebrae levels (L1, L3, L5,
L7) (English, 1980). Although
the muscle activity at more cranial levels was slightly ahead of more caudal
levels (English, 1980)
(Fig. 4), there was not a
significant difference in timing.
Independent of the gait, the timing of sagittal extension in the small
mammals of the current study was similar. Extension of the back normally
started around touch-down of the trailing or leading hindlimb and lasted into
the first third of swing phase, i.e. after lift-off of both hindlimbs. These
results are in accordance with the muscle activation pattern of the major
extensor muscles of the trunk. In the galloping cat, the multifidus, the
longissimus, and the iliocostalis muscles were activated around the touch-down
event of the hindlimbs and clearly turned off after lift-off within the first
20% to 35% of the swing phase (English,
1980).
Although the amplitudes of intervertebral joint movements varied slightly
among the species, maximum angular excursions seemed to be dependent on the
craniocaudal position along the vertebral column. Towards the caudal
direction, amplitudes of intervertebral movements increased and the highest
angular excursion was observed in the last presacral joint in all species.
This increase in the amplitude (i.e. the intensity of sagittal bending
movements) towards the caudal direction is supported by the proportion of
various muscle fiber types within the paravertebral musculature. In the pika,
the cui and the tree shrew, the percentage of oxidative fibers decreased in
the caudal direction while the percentage of glycolytic fibers increased
(Schilling, 2005a) (personal
observations). Since metabolic profiles of muscles relate to their function
(Burke, 1981;
Fischer, 1999;
Scholle et al., 2001), the
craniocaudal gradient in fiber type distribution suggests a functional
transition along the longitudinal body axis. Because of its higher percentage
of glycolytic fibers, the more caudal part of the back is best suited to be
more involved in the more extensive, fast, and forceful sagittal bending
movements than more cranial regions of the back.
The resulting `pelvic movements'
A decisive difference between tailed and `tailless' species in touch-down
and lift-off positions of the pelvis, but the same amplitude of `pelvic
movement' was described in a previous study
(Fischer et al., 2002) and
confirmed by the current results. Whereas `tailless' species showed a nearly
vertical touch-down (100° to 111° for trailing and leading limbs) and
a more protracted lift-off position of the pelvis (131° to 151° for
both hindlimbs), the tailed species presented a more retracted touch-down
(127° to 142° for both hindlimbs) and an almost horizontal lift-off
position of the pelvis (160° to 178° for both hindlimbs). Only the
`tailless' cui behaved more like the tailed species in its pelvic course
(Fischer et al., 2002) (this
study). Despite this, for its close relative the guinea pig, comparable values
of touch-down and lift-off positions, as with the other `tailless' species
investigated here, were reported
(Rocha-Barbosa et al., 1996).
However, of the species under study, the cui's asymmetrical gaits were the
most difficult to record. It seemed to avoid the use of gallop or halfbound,
which may be related to its natural subterranean habitat
(Koch, 1978;
Künkele and Hoeck,
1987).
We hypothesize that the more retracted touch-down and a more or less
horizontal lift-off position of the pelvis is ancestral for therian mammals.
Fossils of the mammalian stem lineage were of a comparable body size to the
species investigated here and possessed long tails
(Jenkins, Jr and Schaff, 1988;
Krebs, 1991;
Luo et al., 2001;
Vasquez-Molinero et al., 2001;
Ji et al., 2002). In order to
prevent a ground contact of the tails during touch-down, we suppose that they
used a similar range of pelvic movements during asymmetrical gaits as
described here for tailed species. Owing to their lack of a long tail,
`tailless' species such as the pika
(Fischer and Lehmann, 1998)
(this study) as well as the rock hyrax
(Fischer et al., 2002) were
able to shift their range of `pelvic motions' craniad. In this position,
displacements of the pelvis result in relatively higher contributions to step
length than in the more retracted `pelvic motion' described for tailed
species.
Despite the different touch-down and lift-off positions of the pelvis, the
amplitude of `pelvic movements' during stance phase was comparable amongst all
species under study (29° to 44° for trailing and leading hindlimbs)
and similar to species of comparable body size [Shaw's jird, 28° for
trailing and 23° for leading limbs
(Gasc, 1993); guinea pig,
approx. 35°; taken from fig. 9
(Rocha-Barbosa et al., 1996)].
It is slightly higher in medium-sized mammals like the rock hyrax [49° for
trailing and 46° for leading limbs
(Fischer, 1994;
Fischer et al., 2002)] and
clearly higher in larger, fast running mammals [dog, 50°
(Alexander et al., 1980);
cheetah, 65° (Hildebrand,
1959)] than in small mammals. In relatively dorsostabile mammalian
species, `pelvic movements' are reduced [horse, 20°
(Hildebrand, 1959)].
Sagittal bending
Sagittal bending is more widespread in therian mammals than suggested by
earlier studies and did not correspond to the traditional subdivisions of the
trunk vertebrae such as the possession or lack of ribs (thoracic
versus lumbar region), the number of free ribs, or the position of
the anticline or the diaphragmatic vertebra (pre-versus
postdiaphragmatic region) in the species under study. Therefore, no prediction
for the trunk region involved in sagittal bending can be made from these
skeletal characters. Furthermore, other morphological characters such as the
insertion or origin of the major flexors or extensors of the back did not
coincide with the region of the vertebral column oscillating during
locomotion. Thus, the skeletomuscular characters cannot be simply related to
the particular part of the trunk that contributes to sagittal spine movements
during asymmetrical gaits in small mammals.
Thus, other variables than locomotory demands must have had an impact on
the evolution of sagittal mobility in therian mammals. Rewcastle
(Rewcastle, 1981) pointed out
that the ability to gallop may be closely related to the faculty of sagittal
vertebral flexion-extension. Reconstructions from the fossil record suggest
that sagittal bending abilities may have evolved in the stem lineage of
therian mammals (Vasquez-Molinero et al.,
2001; Ji et al.,
2002) and were added to the plesiomorph abilities of lateral
bending and long-axis torsion (Pridmore,
1992). Ancestral therian mammals were of a similar body size as
the species under study (Jenkins, Jr and
Parrington, 1976). Fischer speculated that sagittal mobility has
evolved in the context of homoeothermy
(Fischer, 1998). Necessities
like rolling up, and thereby reducing the exposed body surface but also
self-grooming in order to clean the fur from parasites and maintain its
insulatory function are highly probable circumstances for the development of a
highly mobile spine. On the other hand, other non-locomotor activities such as
high accelerations while evading predators or jumping performances may
additionally have had a major impact on morphological characters of the
skeletomuscular apparatus. Therefore, we suggest that these non-locomotory
conditions have the same impact on vertebral characters than locomotory ones.
It follows that, predictions on trunk bending during locomotion concluded only
from morphological characters may be misleading and non-locomotory functions
of the spine have to be taken into account.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alexander, R. M. (1988). Why mammals gallop. Am. Zool. 28,237 -245.
Alexander, R. M., Jayes, A. S. and Ker, R. F. (1980). Estimates of energy cost for quadrupedal running gaits. J. Zool. Lond. 190,155 -192.
Alexander, R. M., Dimery, N. J. and Ker, R. F. (1985). Elastic structures in the back and their role in galloping in some mammals. J. Zool. Lond. 207,467 -482.
Attenburrow, D. P. (1982). Time relationship between the respiratory cycle and limb cycle in the horse. Equine Vet. J. 14,69 -72.[Medline]
Audigie, F., Pourcelot, P., Degueurce, C., Denoix, J. M. and Geiger, D. (1999). Kinematics of the equine back: flexion-extension movements in sound trotting horses. Equine Vet. J. Suppl. 30,210 -213.[Medline]
Blickhan, R., Wagner, H. and Seyfarth, A. (2003). Brain or muscles? In Recent Research Developments in Biomechanics. Vol. 1 (ed. S. G. Pandalai), pp. 215-245. India: Trivandrum.
Boszczyk, B. M., Boszczyk, A. A. and Putz, R. (2001). Comparative and functional anatomy of the mammalian lumbar spine. Anat. Rec. 264,157 -168.[CrossRef][Medline]
Bramble, D. M. (1989). Axial-appendicular dynamics and the integration of breathing and gait in mammals. Am. Zool. 29,171 -186.
Bramble, D. M. (1999). Pulmonary assisted locomotion in galloping mammals: locomotory-respiratory coupling. Abstracts Edinburgh Meeting,44 .
Bramble, D. M. and Carrier, D. R. (1983).
Running and breathing in mammals. Science
219,251
-256.
Bramble, D. M. and Jenkins, F. A., Jr (1993).
Mammalian locomotor-respiratory integration: implications for diaphragmatic
and pulmonary design. Science
262,235
-240.
Burke, R. E. (1981). Motor units: anatomy, physiology, and functional organization. In Handbook of Physiology: Section I -The nervous system II. Motor Control, Part I. Vol.10 (ed. J. M. Brookhart and V. B. Mountcastle), pp.345 -422. Bethesda: American Physiological Society.
Carlson, H. (1978). Morphology and contraction properties of cat lumbar back muscles. Acta Physiol. Scand. 103,180 -197.[Medline]
Carlson, H., Halbertsma, J. and Zomlefer, M. (1979). Control of the trunk during walking in the cat. Acta Physiol. Scand. 105,251 -253.[Medline]
Cavagna, G. A., Heglund, N. C. and Taylor, C. R. (1977). Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. Am. J. Physiol. 233,R243 -R261.[Medline]
Cooper, G. and Schiller, A. L. (1975). Anatomy of the Guinea Pig. Cambridge, MA: Harvard University Press.
English, A. W. (1980). The functions of the lumbar spine during stepping in the cat. J. Morphol. 165, 55-66.
Faber, M., Christopher, J., Schamhardt, H., van Weeren, R., Roepstorff, L. and Barneveld, A. (2001). Basic three-dimensional kinematics of the vertebral column of horses trotting on a treadmill. Am. J. Vet. Res. 62,757 -764.[CrossRef][Medline]
Fick, R. (1911). Handbuch der Anatomie und Mechanik der Gelenke unter Berücksichtigung der Bewegenden Muskeln. 3. Teil. Spezielle Gelenk-und Muskelmechanik. Jena: Gustav Fischer Verlag.
Fischer, M. S. (1994). Crouched posture and high fulcrum, a principle in the locomotion of small mammals: the example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea). J. Hum. Evol. 26,501 -524.
Fischer, M. S. (1998). Die lokomotion von Procavia capensis (Mammalia: Hyracoidea): zur evolution des bewegungssystems bei säugetieren. Abh. Naturwiss. Verein Hamburg 33,1 -188.
Fischer, M. S. (1999). Kinematics, EMG, and inverse dynamics of the therian forelimb - a synthetic approach. Zool. Anz. 238,41 -54.
Fischer, M. S. and Lehmann, R. (1998). Application of cineradiography for metric and kinematic study of in-phase gaits during locomotion of pika (Ochotona rufescens, Mammalia: Lagomorpha). Zoology 101,148 -173.
Fischer, M. S. and Witte, H. F. (2004). Evolution of vertebrate locomotory systems. In Walking: Biological and Technological Aspects (CISM Courses and Lecture Notes, Course no. 272) (ed. F. Pfeiffer and T. Zielinska), pp.51 -79. Wien, New York: Springer Verlag.
Fischer, M. S., Schilling, N., Schmidt, M., Haarhaus, D. and
Witte, H. F. (2002). Basic limb kinematics of small therian
mammals. J. Exp. Biol.
205,1315
-1338.
Gadow, H. F. (1933). Evolution of the vertebral column. In Evolution of the Vertebral Column (ed. J. F. Gaskell and H. L. H. H. Green), pp. 1-356. London: Cambridge University Press.
Gambaryan, P. P. (1974). How Mammals Run. New York: John Wiley.
Gasc, J.-P. (1993). Asymmetrical gait of the saharian rodent Meriones shawi shawi (Duvernoy, 1842) (Ro
