Influence of temperature on mechanics and energetics of muscle contraction JACK A. RALL AND ROGER C. WOLEDGE Department of Physiology, Ohio State University, Columbus, Ohio 43210; and Department of Physiology, University College London, London, United Kingdom RALL, JACK A., AND ROGER C. WOLEDGE. Influence of experimental results is given in Refs. 3 and 59. temperature on mechanics and energetics of muscle contraction. The motives for investigating temperature effects are Am. J. Physiol. 259 (Regulatory Integrative Comp. Physiol. threefold. 1) To perturb the system and hence gain 28): R197-R203, 1990.-Results gleaned from use of temperainsight into its working. Temperature-jump studies (e.g., ture as a probe to study skeletal muscle performance and Refs. 5, 13, 26, 44) are a modern form of this type of mechanisms of activation and contraction are reviewed. Steadyexperimentation. 2) To test ideas about what controls a state and non-steady-state responses to changes in temperature are considered. Temperature sensitivities, Q10values, of me- particular aspect of muscle performance by comparing dependence in intact muscle with that in chanical and energetic parameters range from nearly 1 to >5 temperature in frog skeletal muscle. Factors that are less temperature sen- subcellular systems. Examples include Ca2+ uptake comsitive (Q105 1.5) are peak tetanic force, instantaneous stiffness, pared with rate of relaxation and cross-bridge turnover curvature of force-velocity relation, magnitude of labile heat, compared with shortening velocity. 3) To understand the and mechanical efficiency. Rates with intermediate temperaspecialization of muscle to enable poikilotherms to opture sensitivities (Q10>2 but ~3) include rate of isometric force erate over a wide temperature range, e.g., the possible development, maximum shortening velocity, and relaxation role of parvalbumin in relaxation. These topics are confrom a brief tetanus. Rates with high temperature sensitivities sidered in this review. (Q10 > 3) include cross-bridge turnover during an isometric tetanus, isometric economy, maximum power output, Ca2+ sequestration by sarcoplasmic reticulum, relaxation from a pro- EFFECTOFTEMPERATUREONMECHANICS longed tetanus, and recovery metabolism. The observation that OFMUSCLECONTRACTION the Q10for relaxation rate depends on tetanic duration can be Isometric contraction. Tetanic force is a non-timeexplained in terms of the possible role of parvalbumin as a dependent property of muscle, and so it should be, to a soluble relaxing factor. skeletal muscle; temperature jump; heat production; calcium cycling

MOST BIOLOGICAL PROCESSESproceed more rapidly at higher temperatures, including those processes observed during muscle contraction. There is plenty of scope for observing effects of temperature on muscle function, because muscles will work over a surprising range of temperatures (-30°C). Because “working” implies a coordination of different processes, a first approximation to the way a muscle’s behavior is altered by temperature is to suggest that all its time-dependent properties will be speeded up to the same extent and all non-timedependent properties will be unchanged. What makes the study of temperature effects more interesting is the departures from this pattern. In fact, temperature is often found to affect the rates of different aspects differently, and time-independent properties are themselves often temperature dependent. A full review of these This paper was presented at the symposium entitled “Influence of Temperature on Muscle and Locomotor Performance” held in two parts: at the Spring Meeting of the Federation of American Societies for Experimental Biology, New Orleans, Louisiana, March 19-24,1989, and at the meeting of the International Union of Physiological Sciences, Helsinki, Finland, July 9-14, 1989.

first approximation, temperature independent. The facts are more complicated than this. When force has been investigated over a wide range of temperatures, there appears to be a plateau, which may be near the physiologically relevant temperature (see examples shown in Fig. 1). The fall in force at higher temperatures is not due to damage caused by heating, as the fall at higher temperatures is fully reversible. However, over much of the experimental and perhaps physiological range the force does vary with temperature, and this variation can be quite steep at the lower temperatures. What is the cause of this temperature dependence of tetanic force production? Peak force development during an isometric tetanus of anuran muscle is relatively temperature insensitive with a Q1o ranging from 1.2 to 1.4 (for example, see Refs. 7,8, X,42) in the 0-20°C range. Nonetheless, with a change of temperature from 0 to 2O”C, peak tetanic force increases by 40% or more. This temperature sensitivity of force is a property of the crossbridges rather than the activation system. This conclusion is based on the observation that the Q10 for peak force in skinned frog muscle fibers under maximum activating conditions also ranges from 1.2 to 1.4 (25). According to the sliding filament-attached cross-bridge model of contraction, force depends on the number of attached cross bridges and the average force per cross bridge (36). Instantaneous stiffness of a muscle during

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Society

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R198

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OF

co ntraction has been taken as an indicator of the number of attached cross bridges (20). Instantaneous stiffness in frog (7, 19), mammalian (26), and insect (38) skeletal muscle is less sensitive to changes in temperature than of th .is result is that the is force. The interpretation force-generating capacity of a cross bridge incre ases with increasing temperature. According to this argument, the primary explanation for an increased tetanic force with increased temperature is augmented force per cross bridge rather than an increase in the number of cycling cross bridges. Besides increasing peak force, increases in temperature also shift the isometric steady-state force vs. negative logarithm of Ca2+ concentration (pCa) relationship to higher Ca2+ concentration in skinned frog (25) and mammalian (55) muscle fibers. In other words, the pCa required for 50% of maximum force is inversely related to absolute temperature. The most likely explanation for this observation is that the affinity of the Ca2+-specific sites of troponin (TN) for Ca2+ decreases with increasing temperature, as expected, since Ca2+ binding is an exothermic reaction (47). Rates of force development and relaxation in an isometric tetanus are dramatically sensitive to temperature. In an isometric tetanus in frog and mammalian skeletal muscle, force approaches the plateau exponentially with a rate constant, which ex:hibits a Q1o of -2.5 over a wide temperature range (46, 54). Above 25OC, the Q10 for maximum rate of-change of force production is lower (17, 54). It has been observed that there is a close sim .ilarity between the rate constant for force redevelopment, measured after unloaded shortening and restretch during a tetanus, in skinned fibers from rabbit psoas muscle and adenosinetriphosphatase the maximum actomyosin (ATPase) rate in solution (6). This similarity was observed over a temperature range of 5-35OC. This result suggests that the rate-limiting step in the actomyosin 120

: u

r

40-

L? 20r

0

-5

I 0

n 5

m m I 10 15 20 TEMPERATURE,‘C

I

m

I

25

30

35

4 40

FIG. 1. Plot of isometric tetanic force normalized to maximum value vs. temperature for various skeletal muscles. Data taken from skinned fast fibers from icefish (Chaenocephalus aceratus), which experience mean sea temperature of -1°C during summer (39); skinned fast fibers from bullrout (Myoxocephulus scorpius L.), which experience seasonal variations in body temperature of 2-17°C (41); skinned white fibers from desert iguana (Dipsosuurus dorsalis), which is maximally active in the field at 3542°C (40); intact single fibers from mouse (43); whole sartorius muscles from frog (52); and intact first dorsal interosseus muscles from humans (51).

MUSCLE

FUNCTION

ATPase cycle in solution, thought to be the transition from the weak-binding conformation to the strong-binding conformation associated with release of Pi, may determine the rate of force development in the intact muscle. The Q10 of relaxation often is found to be high. For example, in experiments of Stein et al. (54) in which they used rat and mouse extensor digitorum longus muscles and measured the exponential phase of relaxation, the Q10 is -6 at temperatures below the break point (20°C) and -2.5 above this temperature. Mechanical relaxation from an isometric tetanus in frog skeletal muscle can be divided into three phases (16): 1) maintained isometric force immediately following the last stimulus; 2) slow force decay before force “shoulder;” and 3) exponential decay of force following the force “shoulder.” In isometric tetani of l-s duration, these phases exhibit a Q10 of -2.5 from 0 to 20°C (16). Rate of relaxation in frog skeletal muscle slows exponentially with increasing duration of stimulation (1). Surprisingly, the &lo for relaxation rate of frog skeletal muscle depends on tetanus duration (35). For instance, the &lo for relaxation rate between 0 and 10°C ranges from -4 for long tetani to 2.2 for short tetani (35) The dependence of the Q1o of relaxation rate on tetanic duration suggests that more than one temperature-sensitive process may be involved in determining relaxation rate. This result is expected based on the hypothesis that the intracellular Ca2+-binding protein parvalbumin (PA) acts as a soluble relaxing factor operating in parallel with the sarcoplasmic reticulum (SR) to promote muscle relaxation (24). Frog skeletal muscle has a high PA concentration (27), and the majority of PA is likely to be complexed with Mg+ at rest (59). During a prolonged tetanus, PA would bind Ca2+ continually and eventually become saturated. The time course of Ca2+ binding would be determined by the rate of Mg+ dissociation from PA. Relaxation rate under these conditions would be slow, and its Q10 would represent the temperature sensitivity of the SR Ca2+ pump alone. Relaxation from a brief tetanus would be promoted by the SR and PA and thus would be faster than after a prolonged tetanus. Furthermore, if the Q10 for Ca2’ uptake by PA is less than that for SR, the &lo of the combined processes would be less in a brief tetanus than in a prolonged tetanus, as observed. If this explanation is correct, the Q1o of Mg+ dissociation from PA would have to be ~2.2 (the lowest temperature sensitivity of the rate of relaxation in frog skeletal muscle). In agreement with this suggestion, the Q10 for the Mg+ dissociation rate from frog PA in the O10°C range is 1.9 (34). The Mg+ dissociation rate from PA at 0°C is -0.9 s-l (34). This value and the &lo of 1.9 indicate that PA may promote relaxation in tetanic contractions of frog skeletal muscle of up to -2-s and ls duration at 0 and lO”C, respectively. This mechanism might represent a means of maintaining high locomotory activity in poikilotherms at low temperatures. Isotonic contraction. The mechanical performance of contracting muscle during shortening at constant load is described over most of the load range by a hyperbolic force-velocity relationship. This relationship is charac-

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THERMAL

DEPENDENCE

OF MUSCLE

R199

FUNCTION

terized by three parameters: the maximum velocity of muscle shortening ( Vmax), and the curvature (a/PO), and 0. . hb (J/g/s) the maximum force development (PJ (29). The thermal dependence of P, already has been discussed. The curvature, which is greater in slower contracting muscle and may relate to the thermodynamic efficiency of contraction (57), is little altered by temperature in anurans, i.e., 0. Q10 of -1.2 (10,42). In the 0-20°C temperature range in frogs, Knax exhibits a Q1o of 2.3-2.7 (8, 10, 15, 37). A wider range of Q1o values is found in reptilian and mammalian skeletal muscle (40,50), with higher temperature sensitivity at lower temperatures and for slower fiber types. Given P,, V,,,, and a/PO, it is possible to calculate the maximum power output of a muscle and thus its temperature sensitivity. Maximum power output = MO P, . Vmax where 1M = [(l + G)” - l]/G and G = P,/a (see Ref. 59, p. 49). In practice, 2M2 is ~0.1, and it has about one-half the temperature sensitivity of a/PO. If the Q10 values for PO, Vmax, and a/P0 are 1.2-1.4, 2.3-2.7, and 1.2, respectively, then the Q10 for maximum power output for frog skeletal muscle in the 0-20°C range would vary from 3 0. to 4. Observed maximum power output ranges from 3.3 to 3.6 (52). Thus maximum power output is the most temperature sensitive of the mechanical parameters describing isotonic muscle performance in frog skeletal ( muscle in 0-20°C temperature range.

V&engths/s)

a

0

2. Effect of temperature on steady rate of energy liberation during an isometric tetanus (hb) and velocity of shortening under zero load ( Vo) in frog single fibers. Results from tibialis anterior muscles at 1 and 10°C from Ref. 11 and from unpublished observations of same authors. V. was determined by slack step technique of Edman (15). Solid lines connect observations made on same fibers, and dashed lines connect medians, shown by arrows. FIG.

EFFECTS OF TEMPERATURE OF MUSCLE CONTRACTION

ON

ENERGETICS

Isometric contraction. The time course of energy liberation (heat + work) in response to muscle stimulation can be divided into two phases: 1) the initial phase, which occurs during contraction and relaxation, and 2) the recovery phase, which occurs after relaxation (for review see Ref. 48). The initial phase of energy liberation during an isometric tetanus occurs at a high transient rate during and immediately after force development and then decreases to a steady rate during force maintenance. The steady rate of energy liberation is due entirely to continuous hydrolysis of ATP by the cross bridges (-70%) and the SR (-30%) (12, 32, 33). The economy of an isometric tetanus is defined by the ratio of force maintenance to steady rate of energy liberation. The economy of muscle contraction varies across the animal kingdom by three orders of magnitude (48). The steady rate of energy liberation is highly temperature dependent. For example, a Q10 of 4.5 has been observed for frog whole muscle between 0 and 10°C (8). One possible problem in interpreting measurements on whole muscle is that one is not sure that all the fibers and thus all cross bridges are active at all temperatures. Cooling can cause inexcitability. A version of the whole muscle experiment made with single frog muscle fibers is shown in Fig. 2. In this scatter diagram, the lines connect observations made on the same fibers, whereas the dashed lines connect the medians. The Q10for median Vmax (2.0) is clearly less than the Q1o for steady rate of energy liberation (3.7). The energetics of the SR Ca2+ pump can be studied independent of cross-bridge cvcling bv inducing an iso-

metric tetanus in a muscle that has been stretched to a resting sarcomere length of ~3.6 pm, i.e., beyond myofilament overlap (8, 33). An isometric tetanus under these conditions exhibits little force development, and the steady rate of energy liberation, -30% of that at optimum myofilament overlap, represents energy utilized for Ca2+ sequestration by the SR. In frog skeletal muscle, this fraction of the’ energy liberation exhibits a Qlo of >5 in the 0-10°C range (8). This high Q1O,attributed to ATP utilization by the SR Ca2+ pump, is similar to the Q1o of 4 for relaxation rate in a prolonged tetanus in the same temperature range (Ref. 35 and see above). These results are consistent with the interpretation that relaxation rate in frog skeletal muscle from a prolonged tetanus can be explained totally by Ca2’ sequestration by the SR. Comparable observations have yet to be made on single fibers. The Q10 for cross-bridge cycling during a maintained tetanus can be calculated from these results (8) and is 3.9, which is still significantly above that for Vmax. The simplest interpretation of this observation is that the rate-limiting steps during unloaded shortening and during maximal isometric force maintenance are different. Thus conclusions about the rate of ATP splitting during isometric contractions cannot be drawn solely from measurements of Vmax. In reaching this conclusion we have assumed that essentially all the cross bridges within an active muscle are participating in the cross-bridge

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THERMAL

DEPENDENCE

cycle. As mentioned above, the primary explanation for increased force at higher temperatures is unlikely to be due to the recruitment of more cross bridges into the cycle. The transient high rate of energy liberation during an isometric tetanus in frog skeletal muscle can be explained only in part by the hydrolysis of ATP (12, 32, 59). The extra energy liberation that is not attributable to ATP hydrolysis may be due to the heat production associated with Ca2+ binding to TN and PA during muscle contraction (for recent review see Ref. 49). Quantitatively, Ca2+ binding to PA is more important than to TN, since its concentration is about seven times that of TN in frog skeletal muscle (T.-t. Hou and J. A. Rall, personal communication). This extra transient energy liberation is similar in magnitude and time course to the labile heat production measured during an isometric tetanus. Labile heat is produced with an exponential time course and is evolved in -5 s in frog skeletal muscle at 0°C (2). The amount of labile heat production in frog skeletal muscle is relatively insensitive to temperature in the 0-10°C range, &lo of 1.3-1.5 (2,8). The exponential rate constant for decay of labile heat production exhibits a &lo of -1.8 (8). The time course of Ca2+ binding to PA and TN is determined by the rate of Mg+ dissociation from PA and TN. The observed Q10 of labile heat evolution should reflect the thermal dependence of Mg2+ dissociation from TN and PA. This relatively low &lo is consistent with the observed &lo of 1.9 for Mg2+ dissociation from PA (34) and thus with the proposed role of PA as a soluble relaxing factor (see above). The emerging picture is that in frog skeletal muscle, in the temperature range of O10°C, Ca2’ sequestration by the SR pump exhibits a &lo of ~4-5, and Ca2’ binding to PA and TN may exhibit a Q10 of -1.8-1.9. Taken together these results could explain the fact that the Q10 of the rate of relaxation varies with tetanic duration from -2.2 to 4 in frog skeletal muscle (35). The economy of an isometric tetanus of frog skeletal muscle exhibits a Q10 in the 0-20°C temperature range of -3.3 (2, 8, 37). This &lo represents the combined thermal sensitivities of the cross-bridge cycle, SR Ca2+ pump, and tetanus force. The &lo for recovery metabolism for frog skeletal muscle in the 0-10°C temperature range is 3.4 (53), which is similar to the &lo observed for economy during an isometric tetanus. Isotonic contraction. The energetic cost of an isometric contraction is usually characterized by the measurement of economy. The energetic cost of work production is characterized by measurement of efficiency (56). Intuitively, efficiency can be thought of as the amount of work (W) obtained from a process divided by the maximum amount of work ( VVmax)obtainable. This thermodynamic efficiency is not readily measurable experimentally. Instead, the mechanical efficiency defined as work divided by heat plus wor ‘k produced during the contraction is measured. Th .ese measurements, und .er conditions chosen to maximize the ratio, have been made for relat #ively few species. The value in frog skeletal muscle is 0.45 (31) There is some evidence, however, that the value may* be different in different species (58). (For a more

OF

MUSCLE

FUNCTION

complete discussion of efficiency see Refs. 48, 56, and 58.) Unlike economy, the maximum mechanical efficiency of anuran muscle in the lo-20°C temperature range is essentially insensitive to temperature (21). These results emphasize the fundamental difference between economy and efficiency of muscular contraction. The economy is determined primarily by the rate of cross bridge and Ca2’ cycling, whereas the efficiency is determined by the fraction of chemical free energy converted to work during a cross-bridge cycle. This fraction does not appear to be dramatically sensitive to the speed of the cross-bridge cycle. EFFECTS OF RAPID TEMPERATURE CHANGES ON MECHANICS OF MUSCLE CONTRACTION

Thus far the steady-state responses of muscle to temperature ch anges have been considered. A nother strategy is to consider the transient approach to a new steady state after a rapid or step change in temperature. This general area in chemistry is called relaxation kinetics (4). Examination of transient responses can provide information about the rates and thermodynamics of the reactions under consideration. The approach is as follows: 1) let a system come to equilibrium or a steady state; 2) perturb the system sudden ly and sligh .tly; and 3) determine exponen tial decay time consta .nt(s) (“relaxation times”) that characterize adjustment of concentrations of one species to the new equilibrium or steady state (45). Because chemical equilibrium . constants generally vary with pressure, temperature, el.ectric field ., and concentration, effects of rapid changes in any of these parameters can be studied. The perturbation of in terest here is temperature, i.e., temperature jump(T-jump), and the resultant transient mechanical responses. A variety of techniques have been employed to increase muscle temperature rapidly: 1) joule heating of a fiber in air (5), 2) dielectric heating (microwave radiation) (44), and 3) optical heating [infrared holmium laser (26) or infrared iodine photodissociation laser (l3)]. As applied to muscle, this approach is still in its infancy, but the most promising technique seems to be optical heating. With this technique, -5’C temperature steps can be induced in cl50 ps (13, 26). The following mechanical responses to T-jumps have been observed in glycerol-extracted muscle fibers from rabbit psoas (26). When a fiber is at rest, either under small or large passive tension, force did not change after T-jumps. When in rigor, force decreased abruptly, indicating normal rather than rubberlike thermoelasticity. The rigor result confirms previous mechanical and myothermic measurements on rigor muscle (22). Thus when temperature is increased, rigor muscle responds by thermal expansion and a resultant decrease in force. Rubberlike materials would respond with contraction and increase in force (for discussion of thermoeleasticity see Ref. 59). Because the fiber was in rigor, this normal thermoelasticity must be a property of the myofilaments. Based on a decrease in stiffness of rigor muscle to a Tjump, it has been concluded that the cross bridges also exhibit normal rather than rubberlike elasticity (5). The force responses to T-jumps with muscle at rest or in rigor

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DEPENDENCE

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R201

FUNCTION

an instantaneous increase in force due to the negative thermal expansion of the random coil (18). The opposite was observed (26). It could be argued that this effect might have been missed if the normal thermal expansion of the filaments outweighs the predicted rubberlike thermoelasticity of the cross bridges. However, it has recently been shown, based on a transient stiffness decrease in response to a T-jump in Ca2+-activated muscle, that the cross bridges exhibit normal thermoelasticity during contraction (5). I

I

3. Schematic summary of effects of temperature on nonsteady- (open blocks) and steady-state (solid blocks) tetanic force production in frog skeletal muscle. Force is on vertical axis and time on horizontal axis. Tetani are in chronological order from left to right. Vertical broken lines indicate a change in temperature. A: non-steadystate force is intermediate in terms of peak force and force maintenance compared with steady-state force at previous and new temperatures. B and C: non-steady-state force is independent of duration of rest interval at new temperature. D: non-steady-state force is elicited by exposure to a second temperature without contractile activity at that second temperature (D. M. Burchfield and J. A. Rall, unpublished observations). FIG.

are observed with either slow or rapid temperature changes. Rubberlike thermoelasticity can be observed in rigor fibers at temperatures >4l”C (14). A fiber under maximum Ca2+ activation responds to a T-jump in several phases (26): 1) force decreases abruptly, suggestive of normal thermoelasticity during contraction as established by Hill (30);2) then force recovers rapidly to the pre-T-jump value with a rate constant of 400s-l, which is temperature independent; and 3) finally, force approaches a new, higher force plateau exponentially with a rate constant of 20 s-l at 2O”C, which exhibits a &lo of 1.4 (26). The final force obtained is the same as that observed in steady-state experiments where temperature is changed. The time course of the rapid force recovery after a T-jump bears a remarkable similarity to the quick recovery of force after length steps (length jumps by analogy with T-jumps) during active contraction (19, 26). Goldman et al. (26) have argued that this rapid recovery in force after a T-jump indicates that the process(es) involved is (are) endothermic in nature. By analogy with the results of length steps, this process is the redistribution of attached cross bridges. This conclusion is in agreement with recent results using conventional myothermic techniques (23). Thus T-jump experiments can provide information about kinetic processes in the cross-bridge cycle and their thermodynamic nature. The results of these experiments also bear on a hypothesis for the mechanism of force generation. This hypothesis states that the force of contraction is the result of melting of the a-helical coiled coil of myosin subfragment 2 (S2) to the random coil form with a concomitant decrease in end-to-end distance of the peptide chain and thus development of relative sliding force (28). This melting is thought to occur when myosin attaches to actin in a cross-bridge cycle, thus releasing the S2 link from the stabilizing environment of the thickfilament surface and triggering the rapid helix-coil transition. This helix-coil transition model predicts that the response to a T-jump during active contraction would be

EFFECTS OF TEMPERATURE ON NON-STEADY-STATE

CHANGE MECHANICS

IN

MUSCLE

Frog muscles can exhibit curious non-steady-state mechanical responses to temperature changes, even if those changes occur slowly (9). Non-steady-state mechanical responses are observed in the first two to four tetanic contractions at a new temperature. The characteristics of non-steady-state isometric tetani are distinct at a given temperature and depend on whether the new temperature is approached from a higher or lower temperature. The characteristics most clearly demonstrating these differences are peak force and maintenance of force. For example, at lO”C, non-steady-state tetani develop less force but maintain force more effectively if the preceding temperature was 0°C than if it was 20°C. The steady-state response at 10°C in terms of peak force and force maintenance is intermediate between the two nonsteady-state responses. Characteristics of the steadystate tetani are not dependent on previous temperature. Thus the characteristics of the non-steady-state response are influenced by the preceding temperature as well as the new temperature (Fig. 3A). The non-steady-state response is independent of the duration of rest prior to the first tetanus at a new temperature (Fig. 3, B and C). Furthermore, the muscle need not be activated at the preceding temperature to elicit the non-steady-state response at the new temperature (Fig. 30). Also, if a muscle is rested for a long time after attaining a steady state at a given temperature, subsequent stimulation elicits the steady-state response again. This result verifies that the non-steady-state response does not result from prolonged inactivity but requires a change in temperature. This non-steady-state response may be a property of all fibers or a property of a subpopulation of fibers, which results either from changes in the pattern of activation and/or cross-bridge cycling. Studies with single fibers, with intact membranes and skinned, are needed to resolve these possibilities. CONCLUSIONS

Temperature perturbation can be used as a probe to gain further understanding of skeletal muscle activation and contraction. The principal conclusions reached with this technique that are discussed in this review include the following. 1) The thermal dependence of mechanical and energetic parameters of muscle contraction is complex, with observed Q10 values ranging from nearly 1 to >5. 2) The maximum force developed per cross bridge probably varies with muscle temperature. 3) The rate of

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THERMAL

DEPENDENCE

force development in intact muscle may be controlled by the rate-limiting step observed in the actomyosin ATPase cycle in solution, i.e., the transition from the weakbinding conformation to the strong-binding conformation associated with release of Pi. 4) The temperature dependence of the rate of cross-bridge cycling during force maintenance and during unloaded shortening is different, and this result suggests that the rate-limiting step during the cross-bridge cycle is load dependent. 5) The temperature dependence of the rate of frog muscle relaxation depends on tetanic duration. This result implies that there may be two factors with different ternperature sensitivities operating in parallel to promote relaxation. Evidence suggests that these factors are the sarcoplasmic reticulum and the intracellular Ca2+-binding protein parvalbumin. 6) Temperature-jump techniques can be employed to examine cross-bridge kinetics in muscle. Results to date do not support the proposed helix-coil transition model of muscle contraction. 7) Frog skeletal muscle exhibits unusual non-steady-state mechanical responses to changes in temperature. The origin of these responses is obscure. Address for reprint requests: J. A. Rall, Dept. of Physiology, Ohio State University, 333 W. 19th Ave., Columbus, OH 43210. REFERENCES B. C. The heat production associated with the maintenance of a prolonged contraction and the extra heat produced during large shortening. J. Physiol. Lond. 112: 438-445, 1951.

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Brussels: Editions Arscia, 1956, p. 1-315. 3. BENNETT, A. F. Thermal dependence of muscle function. Am. J. Physiol. 247 R229,1984. 4. BERNASCONI,

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p. l-288. S. Y., AND A. K. TSATURYAN. Effect of joule temperature jump on tension and stiffness of skinned rabbit muscle fibers. Biophys. J. 56: 809-816, 1989. 6. BRENNER, B., AND E. EISENBERG. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution.

5. BERSHITSKY,

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neous stiffness of amphibian range of 0 to 20°C. Can. J. Physiol. PharmacoZ. 59: 8. BURCHFIELD, D. M., AND J. A. RALL. Temperature the crossbridge cycle during unloaded shortening isometric tetanus in frog skeletal muscle. J. Muscle

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OF MUSCLE

FUNCTION

K. A. P. The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J. Physiol. Lond. 291: 143-159, 1979. l6 EDMAN, K. A. P., AND F. W. FLITNEY. Laser diffraction studies of sarcomere dynamics during ‘isometric’ relaxation in isolated muscle fibres of the frog. J. Physiol. Lond. 329: l-20, 1982. 17=ELMUBARAK, M. H., AND K. W. RANATUNGA. Temperature sensitivity of tension development in a fast-twitch muscle of the rat.

15. EDMAN,

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18. FLORY, P. J. Theory of elastic mechanisms in fibrous proteins. 19. 2. ’ 21* 22. 23. 24

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R. M. SIMMONS. Tension responses to sudden length changes in stimulated frog muscle fibres near slack length. J. Physiol. Lond. 269: 441-515, 1977. FORD, L. E., A. F. HUXLEY, AND R. M. SIMMONS. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J. Physiol. Lond. 311: 219-249, 1981. GIBBS, C. L., AND J. B. CHAPMAN. Effects of stimulus conditions, temperature, and length on energy output of frog and toad sartorius. Am. J. Physiol. 227: 964-971, 1974. GILBERT, S. H., AND L. E. FORD. The thermoelastic effect in rigor muscle of the frog. J. Muscle Res. Cell Motil. 7: 35-46, 1986. GILBERT, S. H., AND L. E. FORD. Heat changes during transient tension responses to small releases in active frog muscle. Biophys. J. 54: 611-617,1988. GILLIS, J. M., D. THOMASON,

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Influence of temperature on mechanics and energetics of muscle contraction.

Results gleaned from use of temperature as a probe to study skeletal muscle performance and mechanisms of activation and contraction are reviewed. Ste...
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