Temperature dependence of the force‐generating process in single fibres from frog skeletal muscle

SUMMARYHummingbird flight muscle is estimated to have among the highest mass-specific power output among vertebrates, based on aerodynamic models. However, little is known about the fundamental contractile properties of their remarkable flight muscles. We hypothesized that hummingbird pectoralis fibers generate relatively low force when activated in a tradeoff for high shortening speeds associated with the characteristic high wingbeat frequencies that are required for sustained hovering. Our objective was to measure maximal force-generating ability (maximal force/cross-sectional area, P o /CSA) in single, skinned fibers from the pectoralis and supracoracoideus muscles, which power the wing downstroke and upstroke, respectively, in hummingbirds (Calypte anna) and in another similarly sized species, zebra finch (Taeniopygia guttata), which also has a very high wingbeat frequency during flight but does not perform a sustained hover. Mean P o /CSA in hummingbird pectoralis fibers was very low -1.6, 6.1 and 12.2kNm -2 , at 10, 15 and 20°C, respectively. P o /CSA in finch pectoralis fibers was also very low (for both species, ~5% of the reported P o /CSA of chicken pectoralis fast fibers at 15°C). Q 10-force (force generated at 20°C/force generated at 10°C) was very high for hummingbird and finch pectoralis fibers (mean=15.3 and 11.5, respectively) compared with rat slow and fast fibers (1.8 and 1.9, respectively). P o /CSA in hummingbird leg fibers was much higher than in pectoralis fibers at each temperature, and the mean Q 10-force was much lower. Thus, hummingbird and finch pectoralis fibers have an extremely low force-generating ability compared with other bird and mammalian limb fibers, and an extremely high temperature dependence of force generation. However, the extrapolated maximum force-generating ability of hummingbird pectoralis fibers in vivo (~48kNm -2 ) is substantially higher than the estimated requirements for hovering flight of C. anna. The unusually low P o /CSA of hummingbird and zebra finch pectoralis fibers may reflect a constraint imposed by a need for extremely high contraction frequencies, especially during hummingbird hovering. Supplementary material available online at

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Reiser

Welch

Suarez

et al. 2013

“…For instance, measurements of twitch and tetanus stress in gastrocnemius muscle from X. laevis demonstrated high thermal sensitivity between 5 and 20°C, with limited change from 20 to 30°C (Wilson et al, 2000). Previous work on Rana esculenta demonstrated that raising the temperature of single tibialis anterior muscle fibres from 2 to 12°C increased force output by a Q 10 of approximately 2 by increasing the number of cross-bridges that were in a force-producing state, without affecting the number of cross-bridges formed between the thick and thin filaments (Piazzesi et al, 2003). Such findings on single fibres help to explain the relatively large effects of temperature on whole-muscle force production during isometric activity at low temperatures in the present and previous studies.…”

Section: Isometric Forcementioning

confidence: 99%

Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adultXenopus tropicalis

James

Tallis

Herrel³

et al. 2012

SUMMARYEnvironmental temperature varies temporally and spatially and may consequently affect organismal function in complex ways. Effects of temperature are often most pertinent on locomotor performance traits of ectothermic animals. Given the importance of locomotion to mobility and dispersion, variability in temperature may therefore affect the current and future distribution of species. Many previous studies have demonstrated that burst muscle performance changes with temperature. However, less is known about the effects of temperature on sustained skeletal muscle performance. The iliotibialis muscle was isolated from eight male Xenopus tropicalis individuals and subjected to in vitro isometric and work-loop studies at test temperatures of 15, 24, 30 and 32°C. Work-loop power output (average power per cycle) was maximised at each temperature by altering stimulation and strain parameters. A series of 10 work loops was also delivered at each test temperature to quantify endurance performance. Warmer test temperatures tended to increase twitch stress (force normalised to muscle cross-sectional area) and significantly increased tetanic stress. Increased temperature significantly reduced twitch and tetanus activation and relaxation times. Increased temperature also significantly increased both burst muscle power output (cycle average) and sustained (endurance) performance during work loop studies. The increase in burst power output between 15 and 24°C yielded a high Q 10 value of 6.86. Recent studies have demonstrated that the negative effects of inorganic phosphate accumulation during prolonged skeletal muscle performance are reduced with increased temperature, possibly explaining the increases in endurance found with increased test temperature in the present study.

“…Some of the adaptations to permit this are related to calcium channel function (Wang et al, 2002; Hauton et al, 2011). However, the force from motor proteins at low temperatures is reduced (Rall and Woledge, 1990;Piazzesi et al, 2003;Woledge et al, 2009), and yet ground squirrel hearts function at near-freezing temperatures, while simultaneously supporting cardiac performance when body temperature returns to euthermy, a temperature differential of over 30°C. Second, the activity of the heart, as quantified by heart rate, ranges from over 350-400 beats min -1 prior to hibernation, to a low of 4-5 beats min -1 during torpor.…”

Section: Echocardiogram and Myosin Of Hibernatorsmentioning

confidence: 99%

Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

Nelson

Rourke

2013

SUMMARYDeep hibernators such as golden-mantled ground squirrels (Callospermophilus lateralis) have multiple challenges to cardiac function during low temperature torpor and subsequent arousals. As heart rates fall from over 300 beats min -1 to less than 10, chamber dilation and reduced cardiac output could lead to congestive myopathy. We performed echocardiography on a cohort of individuals prior to and after several months of hibernation. The left ventricular chamber exhibited eccentric and concentric hypertrophy during hibernation and thus calculated ventricular mass was ~30% greater. Ventricular ejection fraction was mildly reduced during hibernation but stroke volumes were greater due to the eccentric hypertrophy and dramatically increased diastolic filling volumes. Globally, the systolic phase in hibernation was ~9.5 times longer, and the diastolic phase was 28× longer. Left atrial ejection generally was not observed during hibernation. Atrial ejection returned weakly during early arousal. Strain echocardiography assessed the velocity and total movement distance of contraction and relaxation for regional ventricular segments in active and early arousal states. Myocardial systolic strain during early arousal was significantly greater than the active state, indicating greater total contractile movement. This mirrored the increased ventricular ejection fraction noted with early arousal. However, strain rates were slower during early arousal than during the active period, particularly systolic strain, which was 33% of active, compared with the rate of diastolic strain, which was 67% of active. As heart rate rose during the arousal period, myocardial velocities and strain rates also increased; this was matched closely by cardiac output. Curiously, though heart rates were only 26% of active heart rates during early arousal, the cardiac output was nearly 40% of the active state, suggesting an efficient pumping system. We further analyzed proportions of cardiac myosin heavy-chain (MyHC) isoforms in a separate cohort of squirrels over 5 months, including time points before hibernation, during hibernation and just prior to emergence. Hibernating individuals were maintained in both a 4°C cold room and a 20°C warm room. Measured by SDS-PAGE, relative percentages of cardiac MyHC alpha were increased during hibernation, at both hibernacula temperatures. A potential increase in contractile speed, and power, from more abundant MyHC alpha may aid force generation at low temperature and at low heart rates. Unlike many models of cardiomyopathies where the alpha isoform is replaced by the beta isoform in order to reduce oxygen consumption, ground squirrels demonstrate a potential cardioprotective mechanism to maintain cardiac output during torpor. Received 25 March 2013; Accepted 4 September 2013Key words: hibernation, MyHC, echocardiogram, atrial contraction, cardiac function. Echocardiogram and myosin of hibernatorsThe myosin heavy-chain isoforms (MyHC) are crucial determinants of contractile performance in cardiac muscle t...