First published online February 29, 2008
Journal of Experimental Biology 211, 873-882 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.006031
Dynamic properties of a locomotory muscle of the tobacco hornworm Manduca sexta during strain cycling and simulated natural crawling
William A. Woods, Jr*,
Steven J. Fusillo and
Barry A. Trimmer
Tufts University, Department of Biology, Dana Laboratories, 163 Packard
Avenue, Medford, MA 02155, USA
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Fig. 1. (A) Lateral view of M. sexta showing location of the ventral
interior lateral muscle (VIL) of the third abdominal segment. (B) VIL and
other body wall muscles of the larva of the moth Hyalophora cecropia,
with the innermost muscles shown frontmost in the drawing. From Beckel
(Beckel, 1958 ).
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Fig. 2. Time course of force development by the ventral interior lateral muscle
(VIL) under tetanic stimulus at resting length. An example is shown of a
typical force response to a 30 V, 20 Hz stimulus train for 2 s, beginning at 1
s in the figure. Peak stress of 138.6±74.2 kPa (mean ± s.d.) was
reached in 2.22±1.33 s (N=19); individual muscle preparations
reached 80% of their peak force in 0.56±0.24 s.
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Fig. 3. Peak tetanic force of the ventral interior medial muscle versus
length. Different symbols represent four different muscle preparations. Fitted
curve is a four-parameter Weibull nonlinear regression
(r2=0.48, P<0.0001). Peak force increased
linearly by more than threefold as strain increased from about 60 to 108% of
in vivo resting muscle length. Optimal length for force production
(Lo) was about 108% of resting length. Muscles produced
90% or more of maximum force at lengths from about 80 to 135% of
Lo, and 60% or more at lengths from about 60 to 160% of
Lo.
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Fig. 4. Work loops of the ventral interior lateral muscle under sinusoidal cycling
from 80% to 120% of in vivo resting muscle length. Broken lines are
for passive muscle and solid lines are for muscle under sustained stimulation.
Data shown are for the fourth of five strain cycles at each cycling
frequency.
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Fig. 5. The ratio of passive to active work loop area of VIL (see
Fig. 4) was associated with
sinusoidal strain cycling frequency [ratio=0.0425 log(cycling
frequency)+0.220; N=4, r2=0.99]. Data used are of
the fourth of five concurrent strain cycles at each cycling frequency.
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Fig. 6. Resilience of active ventral interior lateral muscle during sinusoidal
strain cycling rose exponentially to a maximum at cycling frequencies from 0.5
to 16 Hz (single time constant three-parameter model,
r2=0.98, P<0.01). Frequencies of 0.5–2
Hz produce length change velocities representative of those observed in
vivo.
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Fig. 7. (A) The time course of force increase and decay as the ventral interior
lateral (VIL) muscle is stretched from 90 to 110% of in vivo resting
length at 0.4 lengths s–1 and held. Force decays
exponentially at completion of stretching (see
Fig. 8). (B) Detail of A
showing the transition in the rate of force increase during the constant
velocity stretch.
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Fig. 9. Mean stress during the transition (st; see
Fig. 7B) was associated with
stretch velocity (v) of the ventral interior lateral muscle by the
relationship st=0.0161v+0.0158 (N=5,
P<0.001). Values are means ± 1 s.e.m. Despite considerable
variation between individual muscle preparations, r2
values of the stress vs stretch velocity relationship for individual
muscles were all >0.90 and averaged 0.97.
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Fig. 10. (A) Length (broken trace) and instantaneous spike frequency (ISF; solid
trace) of the third abdominal segment ventral interior lateral muscle during
horizontal crawling. The ISF represents the frequency of excitatory junction
potential events as characterized by EMGs of stimulated muscles obtained from
in vitro preparations. (B) Differentiated voltage from which the ISF
values in A were obtained.
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Fig. 11. (A) Time course of force and length of a 4.6 mm third abdominal segment
ventral interior lateral muscle subjected to a simplified concensus crawling
strain cycle and stimulus. The muscle is shortened by 28% in 0.95 s and
re-lengthened in 0.87 s. Time course of force development by the same muscle
preparation under tetanic stimulus is shown in
Fig. 2. (B) Work loop during
the crawling cycle in A. The loop does not close during strain cycling, but
force returns to nearly starting values during a time interval representative
of that seen between strain cycles in Fig.
10A.
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Fig. 12. The effect of varying stimulus phase or duration during in vitro
crawling cycles. (A) Varying the timing of the 0.68 s stimulus by as little as
0.2 s, about 10% of the strain cycle duration, resulted in no positive work
being done by the same muscle preparation as in Figs
2 and
11. (B) Varying stimulus
duration from 0.28 to 1.08 s for a 3.6 mm VIL while holding the timing of the
stimulus midpoint at the same value as in A and in
Fig. 11 resulted in positive
work being done for a portion of the strain cycle in both cases, as well as
for intermediate stimulus duration values (not shown).
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© The Company of Biologists Ltd 2008
) of force decay from the peak values shown in A with the muscle held at
110% of resting length was associated with stretch velocity (v) by
the relationship