Measurement of Heat Production during the Summation of ...

Japanese Journal of Physiology,30,617-629,1980

Measurement of Heat Production during the Summation of

Isometric Contraction in Frog Skeletal Muscle with

an Infrared Radiometer

Takakazu KOBAYASHI and Haruo SUGI

Department of Physiology,School of Medicine,Teikyo University,Tokyo,173 Japan

Abstract The heat production of frog skeletal muscle during isometric

contraction was measured with an infrared radiometer at room tempera-

ture(23-26•Ž),attention being focused on the heat produced during

the summation of twitches by two successive stimuli.When the amount

of heat produced by the second stimulus was plotted against the cor-

responding tension increment,the data points fell on two regression

lines of approximately the same slope except for the intermediate stimulus

intervals.One regression line started from the origin,while the other

intersected the ordinate at about 1mcal/g.If a twitch was produced at

various times after a 0.5 sec tetanus,all the data points on the heat versus

tension increment plot distributed around a single regression line starting

from the origin.These results are explained by assuming that the

relation between the tension-dependent heat and the tension increment

in a twitch produced after a preceding mechanical response remains

nearly constant irrespective of the stimulus interval,while the amount

of tension-independent heat production varies depending on the time

after the preceding stimulation.

A number of investigations have hitherto been performed on the heat pro-

duction in active muscle by use of a thermopile to obtain information about the

mechanism of chemomechanical conversion in muscle contraction(for reviews,

see WOLEDGE,1971;HOMSHER and KEAN,1978).In the thermopile experiments,

however,heat produced in muscle has to flow through the layer of physiological

saline and the film of coating material to be measured by a thermopile,producing

a considerable lag in heat measurements.Most thermopile experimentation

has,therefore,been made at 0•Žto slow down muscle contraction,thus com-

pensating for the limited time resolution.Recently,FRASER(1970,1971)devised

an infrared radiometer,which detects infrared radiation from muscle with no

thermal contact resulting in an improved time resolution,and has succeeded

in measuring heat production in frog muscle at 15•Žat which temperature frogs

Received for publication April 3,1980

小林孝和,杉晴夫

617

618 T.KOBAYASHI and H.SUGI

can move normally(FRASER,1973;FRASER and CARLSON,1973).Since the use of

this infrared radiometer seemed so interesting,we constructed a similar radio-

meter to be used for muscle heat measurements at room temperatures.

The present paper deals with the heat production in frog skeletal muscle during

isometric contraction,attention being focused on the amount of heat produced and

the magnitude of the increment of tension during the summation of isometric

twitches by two successive stimuli.The experiments were made at room tempera-

tures of 23-26•Ž,at which the tension increment by the summation of twitches

was much more marked than at low temperatures because of a large tetanus:

twitch tension ratio(GIBBS et al.,1966;RALL,1979).

METHODS

Infrared radiometer.The infrared radiometer used was essentially similar to

that of FRASER(1970,1971).The radiometer monitored infrared radiation from

a 7mm2 target area of the muscle surface,and consisted of a Golay cell(Eppley

Laboratories,Inc.),a kind of gas thermometer converting infrared radiation

into an optical signal(GOLAY,1947),and a signal processor whose output was

an accurate analog of infrared radiation from muscle.The amount of muscle heat

production was measured directly as millidegrees centigrades(•‹mC),and this value

was nearly equivalent to that expressed as millicalories per gram(mcal/g)because

the specific heat of frog muscle is about 0.86(HILL,1949).In the present study,

the heat production was expressed as mcal/g for the sake of comparison with

the values in previous reports.The rise time constant of the signal processor was

adjusted to about 5 msec,so that the noise levels in heat records was less than

0.5•‹mC.In heat measurements during single or two successive twitches,an

averaging computer was used to increase signal-to-noise ratio.The base-line drift

was less than 1•‹mC/sec,and did not significantly affect the results.No correction

was made for heat loss,since it was negligible for the time of heat measurements

(less than 1 sec).

The linearity and the response time of the radiometer were calibrated with

a black aluminium block containing an internal heater(FRASER,1970,1971).

The aluminium block was placed at the same position as that of the target area of

muscle,and a given temperature increment was produced by applying current to

the internal heater.The temperature change of the block was calculated from

the time integral of the voltage-current product,the specific heat of aluminium,

and the weight and emissivity of the block(0.95,FRASER,1970).Heat loss of the

block was negligible for the time needed for calibration.The relation between

the change in calibrator temperature and the output of the processor was linear

well over the range of heat measurements in the present study.Further details

of the radiometer and the signal processor are the same as those described by

FRASER(1970,1971).

Japanese Journal of Physiology

HEAT PRODUCTION IN FROG MUSCLE 619

Muscle mounting.All experiments were performed with the sartorius muscle

of the bullfrog(Rana catesbeiana).The muscle was isolated with the pelvic bone

attached and kept in physiological saline containing 115mm NaCl,2.5mm KCl,

1.8mM CaCl2,2.18mM Na2HPO4 and 0.85mM NaH2PO4(pH 7.2)for 1 hr prior to

the experiments.The preparation was then mounted in an acrylic experimental

chamber with its inner surface uppermost;the pelvic end was firmly clamped to

the chamber,while the tibial end was connected to a strain gauge with a jeweller's

chain to record isometric tension.The compliance and the natural frequency of

oscillation of the strain gauge were about 1ƒÊm/g and 150Hz,respectively.The

length of the preparation mounted in this way(40-60mm)was about 1.1 times the

slack length unless otherwise stated,the sarcomere length measured by He-Ne

laser light being 2.2-2.4ƒÊm at the middle part.Stimulating electrodes consisted

of two pairs of Pt wires fixed to the chamber,the heat produced by a stimulating

current having been proven negligible.To avoid movement artifacts,the fascia

along the edge of the preparation was pulled laterally and pinned at several points

to the bottom of the chamber to eliminate movement of the target area during

isometric contraction(FRASER,1970;FRASER and CARLSON,1973).

The experimental chamber was initially filled with physiological saline to

equilibrate the preparation for 30min.Immediately before each experiment,the

muscle was carefully blotted with a strip of filter paper.Then,the chamber was

placed in the radiometer in such a way that the distance between a double conical

reflector,which was attached at the aperture of the radiometer to collect infrared

radiation(FRASER,1970,1971),and the muscle surface was about 0.5mm.The

whole set-up was confined to a steel box to be shielded both thermally and electro-

magnetically.

General procedure.The preparation mounted in the radiometer was further

thermally equilibrated for about 10min.Then,it was stimulated to contract

isometrically by applying supramaximal current pulses of 0.5-1 msec duration

through the Pt wire electrodes.Single or two successive twitches were produced

at intervals of 40-60 sec,while tetani were produced with a series of repetitive pulses

given at 50Hz at intervals of more than 2min.In the case of single or two suc-

cessive twitches,four serial records were averaged in an averaging computer to be

displayed on a chart recorder.Individual heat and tension traces were also moni-

tored on a memory oscilloscope to check the reproducibility of heat and tension

responses within each series of records.After the experiments,the muscles were

cut free of their attachments,blotted and weighted to calculate the tetanic tension

per cross-sectional area as Pol/fm,where Po,l and m were the maximum tetanic

tension,muscle length and blotted weight,respectively.The calculated values

ranged from 2.0 to 2.5kg/cm2,indicating that the muscles were adequately stimu-

lated.All experiments were made at room temperatures of 23-26•‹C,at which the

tetanus:twitch tension ratio was 2.2-3.0.

Vol.30,No.4,1980


RESULTS

Heat production during isometric twitch and tetanus

General features of heat production.Figure 1 shows examples of the records

of heat production during isometric twitches(A,C)and during short isometric

tetani(B,D).The heat production and tension development took place simultane-

ously with an accuracy of a few msec.In both twitches and short tetani,the rate

of heat production was maximum at the beginning,and then decreased with time

until the muscle temperature reached a maximum level at the relaxation phase.

The above features of heat production recorded with the infrared radiometer

were similar to those reported by FRASER and CARLSON(1973) with the infrared

radiometer,and also to those obtained by previous authors with the thermopile

(cf.WOLEDGE,1971).

On the other hand,a distinct cooling phase,as indicated by a period of negative

slope in the heat records(Fig.1C,D,FRASER,1973;FRASER and CARLSON,1973),

was observed only in about 50% of the muscles studied;the remaining muscles

showed no appreciable cooling phase in heat records(Fig.1A,B).This may be

due,at least in part,to the fact that the present experiments were made with

muscles slightly stretched above the slack length,because the cooling phase tends

to disappear by stretching muscles(FRASER and CARLSON,1973).The average

value of the final temperature change produced in a twitch was 3.1•}0.4mcal/g

(n=35),a value comparable to those obtained by previous authors(e.g.2.5-4•‹mC/g

A

C

B

D

Fig.1. Simultaneous records of heat production(upper traces)and isometric tension

(lower traces)in twitches(A,C)and in 0.5 sec tetani(B,D).Distinct cooling phase

indicated by arrow can be seen in C and D,but not in A and B.Records in A and C

are averages of four traces,while records in B and D are averages of two traces.Tem-

perature,24•Ž



Fig.2. Relation between the heat production and the twitch tension in a muscle stretched

to a variable extent.The initial muscle length l was 53mm.Each data point was

obtained at the following muscle lengths,reading from right,l,l+5mm,l+10mm,

l+15mm,l+20mm,l+30mm. Temperature,25℃.

at 15•Ž,FRASER and CARLSON,1973;2.7•}0.9 mcal/g at 15-22•Ž,GIBBS et al.,

1966).Meanwhile,the average temperature change attained in a 0.5 sec tetanus

was 21.3•}3.4 mcal/g(n=24).

Relation between heat production and twitch tension.The relation between

the amount of heat production and the magnitude of twitch tension was examined

by stretching the muscle beyond its initial length.In agreement with the previous

reports(SMITH,1972;HOMSHER et al.,1972;RALL,1978,1979),the heat produced

in a twitch was divided into tension-dependent and tension-independent com-

ponents as shown in Fig.2.The tension-independent component of heat produc-

tion,which was determined by the point of intersection of the regression line with

the ordinate,was about 1mcal/g,being analogous to the value obtained by

HOMSHER et al.(1972)on the semitendinosus muscle of Rana pipiens at 0•‹C.

Heat production during summation of isometric twitches by two successive stimuli

The muscle was stimulated by two successive stimuli at various intervals,

and the relation between the heat production and the magnitude of tension in-

crement in response to the second stimulus was examined.Examples of heat and

tension records of summated twitches are shown in Fig .3.The amount of

heat produced by the second stimulus was determined by algebraically subtracting

the heat produced by the first stimulus from the total heat produced by two suc-

cessive stimuli,whereas the magnitude of tension increment produced by the second

stimulus was measured by the method illustrated in Fig.4(GIBBs et al .,1966).

Vol.30,No.4,1980


A

C

B

D

Fig.3. Records of heat production and isometric tension during the summation of twitches

by two successive stimuli given at various intervals.The intervals between stimuli were

10 msec in A,30 msec in B,50 msec in C and 150 msec in D.All records are averages

of four traces.Temperature,24•Ž.

A B C

Fig.4. Schematic drawings showing an isometric twitch in response to a single stimulus(A)and the summated mechanical responses in response to two successive stimuli givenat an interval of less than the mechanical fusion interval(B)and at an interval ofmore than the fusion interval(C).The tension increment in response to the secondstimulus is indicated by arrows.

When the stimulus interval was less than the mechanical fusion interval,the

tension increment was measured by algebraical subtraction of the first twitch from

the summated response(Fig.4B).If the stimulus interval was more than the fusioninterval,the tension increment was measured from the level of tension at whichthe second twitch started(Fig.4C).

A typical result is shown in Fig.5,in which the heat production and the tension

increment in response to the second stimulus are plotted against the stimulus inter-

val.The heat produced by the second stimulus decreased with decreasing stimulus

interval,approaching zero as the stimulus interval tended to zero.Similar resultshave been reported by HARTREE and HILL(1921)and GIBBS et al.(1966),except thatHartree and Hill sometimes observed a supernormal phase in heat production



which was never seen in the present experiments.Meanwhile,the tension incre-

ment first decreased with decreasing stimulus interval to reach a minimum value

at a stimulus interval of about 50 msec,and then increased with a further decrease

in the stimulus interval,reaching a maximum at a stimulus interval of about

20 msec.At a stimulus interval of less than 20 msec,the tension increment de-

creased steeply with decreasing stimulus interval,approaching zero as the stimulus

interval tended to zero.

Fig.5. Dependence of the heat production(open circles)and the tension increment(filled

circles)in response to the second stimulus on the stimulus interval.Broken line shows

the time-course of a single twitch.Temperature,24•Ž.

Fig.6. Relation between the heat produced by the second stimulus and the correspondingtension increment.The data are the same as those shown in Fig.5.The stimulusinterval(in msec)is indicated alongside each data point.

Vol.30,No.4,1980


The amount of heat produced by the second stimulus was also plotted against

the magnitude of corresponding tension increment in Fig.6.At stimulus intervals

of 60-150 msec,the data points fell on a regression line which intersected the

ordinate at about 1 mcal/g as in the case of the relation between the heat produc-tion and the twitch tension in Fig.2.The first and second twitches were completelyseparated at a stimulus interval of 150 msec with no significant difference betweenthem in either heat production or tension,indicating that the above regression

line was identical with that shown in Fig.2.At stimulus intervals of less than

20 msec,the data points were found to fall on another regression line,which

started from the origin with approximately the same slope as that of the former

regression line.

At intervals between 20 and 60 msec,the data points distributed between these

two regression lines;the deviation along the ordinate of each data point from

the upper regression line increased as the stimulus interval was decreased from

60 to 20 msec.

Heat production in a twitch produced after a tetanusExperiments were also performed in which a twitch was produced at various

times after a preceding 0.5 sec tetanus(Fig.7).In these experiments,the recordswere not averaged to avoid muscle fatigue with repeated tetani.In Fig.8,theheat production and the tension increment in response to the"test"stimulus are

plotted against the interval between the termination of the preceding"conditioning"repetitive stimuli(50 Hz,for 0.5 sec)and the"test"stimulus.Both the heat

Fig.7. An example of unaveraged records of heat production and tension when a twitch

was produced after a 0.5 sec tetanus.The interval between the end of the"conditioning"

repetitive stimuli(50 Hz for 0.5sec)and the"test"stimulus was 500 msec.Temperature,

23.5•Ž.



Fig.8. Fig.9.

Fig.8. Dependence of the heat production(open circles)and the tension increment (filledcircles)in response to a"test"stimulus given after a 0.5 sec tetanus on the intervalbetween the termination of the"conditioning"repetitive stimuli and the"test"stimulus.Broken line shows the time-course of the preceding tetanus from the termination of the

"conditioning"stimuli,its magnitude being scaled down for the sake of convenience.

Temperature,23.5•Ž.

Fig.9. Relation between the heat production and the tension increment in a twitch producedafter a tetanus.The data are the same as those shown in Fig.8.The interval betweenthe"conditioning"repetitive stimuli and the"test"stimulus(in msec)is indicated at eachdata point.

production and the tension increment decreased with decreasing interval betweenthe"conditioning"and the "test"stimuli.The heat and tension measurements

were made only at stimulus intervals of more than 120-150 msec,since their values

became vanishingly small at shorter intervals to be measured accurately.The

amount of heat production by the"test"stimulus was also plotted against the

magnitude of corresponding tension increment in Fig.9.In contrast with the results

on summation of twitches(Fig.6),all the data points distributed around a singleregression line starting from the origin, irrespective of the interval between the"conditioning"and the"test"stimuli .

DISCUSSION

Explanation of heat production during summation of isometric contraction interms of two heat components.It has been shown by many investigators that.when the muscle length is increased beyond the slack length to decrease isometric

twitch tension,the heat produced in a twitch decreases with decreasing twitch

Vol.30,No.4,1980


tension,approaching a finite value as the tension tends to zero(SMITH,1972;HOMSHER et al.,1972;RALL,1978,1979).Consequently,the heat production ina twitch has been divided into tension-dependent heat(TDH)and tension-inde-

pendent heat(TIH).These two components of heat produced in a twitch werealso confirmed in the present study(Fig.2).

In the present experiments on the summation of twitches by two successivestimuli(Fig.3),it was found that the data points on the heat versus tension incre-ment plot fell on two regression lines with approximately the same slope except forthe intermediate stimulus intervals(Fig.6);the upper regression line was identicalwith the heat versus tension relation in a twitch(Fig.2),while the lower regressionline started from the origin.The above finding was facilitated by the temperature

(23-26•Ž)at which the experiments were performed,since the magnitude of tension

increment for a given stimulus interval increased with increasing temperature as

a result of increasing tetanus:twitch tension ratio.

The heat versus tension increment relation in response to the second stimulusshown in Fig.6 can be explained by assuming(1)the TDH versus tension incrementrelation in the second twitch remains nearly constant irrespective of the stimulusinterval(except for the refractory period of muscle action potential,3.5-4 msec

at 23-26•Ž,Kobayashi and Sugi,unpublished),and(2)the amount of TIH pro-

duced by the second stimulus changes depending on the stimulus interval.Thus,

when the second stimulus is given within 20 msec after the first,it produces a

tension increment above tne nrst twitcn ana tne corresponding amount or tun

while the amount of TIH production is very much reduced or eliminated,and asa result the points on the heat versus tension increment plot should fall on a straight

line starting from the origin(the lower regression line in Fig.6).If the secondstimulus is delivered more than 60 msec after the first one,it produces not onlythe tension increment and the corresponding TDH,but also the full TIH of about1 mcal/g(see Fig.2),so that the points should fall on a straight line intersectingthe ordinate at about 1 mcal/g(the upper regression line in Fig.6).At stimulusintervals between 20 and 60 msec,the second stimulus produces both TDH and TIHas well as the tension increment,and the amount of TIH production increases asthe stimulus interval is increased above 20 msec to reach the maximum value ot-about 1 mcal/g at an interval of 60 msec.

Recently,RALL(1979)showed that the slope of the TDH versus tensionrelation in a twitch remained unchanged irrespective of whether the twitch tensionwas varied by changing muscle length or by changing temperature.Similarly,the

present results may be stated so that the slope 01 the"TDH versus tension relationmay also remain nearly constant when the twitch tension is varied by producing

a twitch at various times after the preceding mechanical response, implying that

the tension increment determined as illustrated in Fig.4 is a valid measure of

the magnitude of the second twitch preceded by the first one.

On the other hand,when a twitch was produced at various times after a



preceding 0.5 sec tetanus(Fig.7),both the heat production and the tensionincrement in response to the"test"stimulus were vanishingly small when it wasapplied within 120-150 msec after the termination of the"conditioning"repetitivestimuli(Fig.8),and all the data points on the heat versus tension increment plotwere observed to distribute around a single regression line starting from the originirrespective of the stimulus interval(Fig.9).These results indicate that the TIH

production is markedly reduced for a much longer period after a series of repetitivestimuli than after a single stimulus.

Possible source of tension-independent heat.Though the heat productionduring summation of isometric contraction can be accounted for on the basis ofthe two heat components,the source of the TIH,the amount of which changesdepending on the previous stimulation,remains to be determined.The tension-independent heat is generally referred to as activation heat,in the sense that it isindependent of the interaction between the thick and thin filaments to produceisometric tension(cf.HOMSHER and KEAN,1978).In the present experiments,theamount of TIH production in response to the second stimulus was very muchreduced for the first 20 msec after the first stimulus,and the full recovery of TIHtook place in about 60 msec(Fig.6).Meanwhile,the amount of TIH in a twitch

preceded by a 0.5 sec tetanus was markedly reduced for the first 120-150 msecafter the preceding tetanic stimulation(Fig.8),and the presence of a single re-

gression line in the TDH versus tension increment plot(Fig.9)implies that thefull recovery of TIH takes place gradually in about 300 msec.

At present,the most probable sources of activation heat(or TIH)are theenergy dissipated during Ca2+cycling(HOMSHER et al.,1972)and the enthalpychange for Ca2+binding to troponin(YAMADA et al.,1976;POTTER et al.,1977).Concerning the Ca2+cycling,the Ca transients during an isometric twitch reacha peak at the early phase of tension rise,and then decay nearly to zero shortly afterthe peak of twitch tension(BLINKS et al.,1978),roughly corresponding to the time-course of the initial marked reduction and the subsequent recovery of TIH in re-sponse to the second stimulus.The decay of Ca transients after a tetanus,how-ever,precedes the relaxation of tetanus tension,and cannot be compared with thelong-lasting effect of a tetanus in markedly reducing the TIH response to the sub-sequent stimulus(Figs.8 and 9).

With respect to the Ca2+binding to troponin,it has been shown that the ac-companying enthalpy change is sufficient to account for the activation heat

(YAMADA et al.,1976;POTTER et al.,1977).Though the Ca transient experimentsgive no direct information about the actual amount of Ca2+bound to troponi,it seems possible that the binding of Ca2+to one or more of the Ca2+-bindingsites of troponin may be related to the effect of the preceding stimulation in reduc-ing the amount of TIH production in response to the subsequent stimulus.

In connection with the long-lasting effect of a tetanus on the reduction ofTIH production,it is of interest that,in a twitch produced shortly after a preceding

Vol.30,No.4,1980


tetanus,the magnitude of Ca transient decreases markedly as compared to thecontrol in spite of a marked potentiation of twitch tension(BLINKS et al.,1978).In addition,YAGI et al.(1977)reported that the intensity ratio of two equatorialreflections(I1,0/I1,1),which is normally regarded as a measure of the cross-links

between the thick and thin filaments (HASELGROVE and HUXLEY,1973),returnedto the resting value at many seconds after a tetanus.These phenomena seemvery likely to originate from the same underlying mechanism as that for effect ofthe previous stimulation in reducing TIH in response to the subsequent stimulus.

We wish to thank Dr.A.Fraser for giving us valuable information about the infrared

radiometer and Professors H.Mashima and K.Yamada for their encouragement,advice andkind cooperation in constructing the radiometer.

REFERENCES

BLINKS J. R., RUDEL R., and TAYLOR, S. R.(1978) Calcium transients in isolated amphibianskeletal muscle fibres: Detection with aequorin. J. Physiol.(Lond.), 277: 291-323.

FRASER, A.(1970) Myothermic radiometry and muscle heat production: Length dependenceof transients during isometric twitches in. frog sartorius muscle. Ph. D. Thesis, The JohnHopkins University.

FRASER, A.(1971) Myothermic radiometry. Rev. Sci. Instrum., 42: 22-26.FRASER, A.(1973) Comments on activation heat and its relation to activation. Cold Spring

Harbor Symp. Quant. Biol., 37: 627-628.FRASER, A. and CARLSON, F. D.(1973) Initial heat production in isometric frog muscle at

15•Ž. J. Gen. Physiol., 62: 271-285.

GIBBS, C. L., RICCHIUTI, N. V., and MOMMAERTS, W. F. H. M.(1966) Activation heat in frog

sartorius muscle. J. Gen. Physiol., 49: 517-535.

GOLAY, M. J. E.(1947) Theoretical consideration in heat and infrared detection with partic-

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HARTREE, W. and HILL, A. V.(1921) The nature of the isometric twitch. J. Physiol.(Lond.),55: 389-441.

HASELGROVE, J. C. and HUXLEY, H. E.(1973) X-ray evidence for radial cross-bridge movementand for sliding filament model in actively contracting skeletal muscle. J. Mol. Biol., 77:549-568.

HILL, A. V.(1949) Energetics of relaxation in a muscle twitch. Proc. R. Soc. Lond.(Biol.),136: 211-219.

HOMSHER, E. and KEAN, C. J.(1978) Skeletal muscle energetics and metabolism. Annu.Rev. Physiol., 40: 93-131.

HOMSHER, E., MOMMAERTS, W. F. H. M., RICCHIUTI, N. V., and WALLNER, A.(1972) Activationheat, activation metabolism and tension-related heat in frog semitendinosus muscle. J.Physiol.(Lond.), 220: 601-625.

POTTER, J. D., HSU, F., and POWNALL, H. J.(1977) The thermodynamics of Ca2+ binding totroponin-C. J. Biol. Chem., 252: 2452-2454.

RALL, J. A.(1978) Dependence of energy output on force generation during muscle contraction.Am. J. Physiol.: Cell Physiol., 4: C20-C26.

RALL, J. A.(1979) Effects of temperature on tension, tension-dependent heat, and activationheat in twitches of frog skeletal muscle. J. Physiol.(Lond.), 291: 265-275.

SMITH, I. C. H.(1972) Energetics of activation in frog and toad muscle. J. Physiol.(Lond.),220: 583-599.



WOLEDGE, R. C.(1971) Heat production and chemical change in muscle. Prog. Biophys. Mol.Biol., 22: 37-74.

YAGI, N., ITo, M. H., NAKAYAMA, H., IzUMI, T., and MATSUBARA, I.(1977) Return of myosinheads to thick filaments after muscle contraction. Science, 197: 685-687.

YAMADA, K., MASHIMA, H., and EBASHI, S.(1976) The enthalpy change accompanying thebinding of calcium to troponin relating to the activation heat production of muscle.Proc. Jpn. Acad., 52: 252-255.

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