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Propagation of impulse in the heart of the beetle allomyrina dichotomus
0300-9629/90$3.00 + 0.00 cm 1990 Pergamon Press plc
Camp. Biochem. Physiol. Vol. 97A, No. 4, pp. 60-605, 1990 Printed in Great Britain
PROPAGATION OF IMPULSE IN THE HEART BEETLE ALLOMYRINA DICHOTOMUS ARINOBU
EBARA, HATSUMI
Institute of Physics,
AKIYAMA,*
HIROSHI YAMAGlsHIt
and
OF THE
HISASHI OHSHIMA
Science University of Tokyo, Kagurazaka, Shinjuku, Tokyo 162, Japan (Receiued 19 April 1990)
Abstract-l. Propagation of impulse is studied electrophysiologically in the heart of an adult armed wrestler beetle. 2. The velocity of propagation shows extensive range of values, for example, from 5.2 cm to 2100 m/set in a specimen at a temperature of 26.5% 3. The propagation is considered to be the result of the alignment behavior of pacemakers as represented
by a phase-response curve. 4. The propagation may be derived from sequence of impulses generated spontaneously and successively from one pacemaker to an adjacent one with a short delay, the length of which may vary widely.
INTRODUCTION
RESULTS No nervous element at all could be found in the action potential of the heart muscle from extracellular recording, even in the intracellular results. When a suction electrode was impaled through the body cavity avoiding the heart, rapid spike potentials were often observed sporadically and intermittently, clearly varying from the electrocardiogram in their time course. These rapid deflections might be nerve action potentials.
The contractile wave in the heart of an adult moth Hyalophora is peristaltic in nature and usually proceeds from the caudal toward the cephalic region at low velocity (about 25 mm/set) (McCann and Sanger, 1969). It appears that conduction velocity increases with heart rate in insects (McCann, 1970). On the other hand, in a previous paper (Ebara et al., 1990) it was reported that cardiac rhythm usually originated from the caudal region and sometimes from other portions of the heart, or occasionally from a middle part of the heart toward anterior and posterior end. The reversal of the beating direction has been noted in a number of insects at all stages of development (McCann, 1970). The present paper will propose some further interpretations of the propagation mechanism in the insect heart. MATERIAL
Initiating site of heart rhythm
AND METHODS
An adult armed wrestler beetle, Allomyrina dichotomus L., was used as the material. The isolated heart with a part of associated exoskeleton was usually set in a small elastic chamber in a solution composed df NaCl 160.7 rnG, KC1 2.7 mM. CaCl, 2.8 mM. NaHCO, 0.02%. For intracellular recoiding, a gliss pipette microelectrode filled with 3M KC1 and of lo-20 MR electrical resistance was employed. For extracellular recording, the usual method for recording action potential in the present paper involved using a small glass pipette, the tip of which was 50 _ 110 pm in diameter with a connected injection syringe as a suction electrode. The input signal was amplified and displayed on a sheet of recording paper with an electronic instrument (medicalcorder, PMP-3004 type, Nihon Kohden Kogyo Co.). Observation and experimentation was carried out at room temperatures (20.2-3 I PC). ‘Hamura High School, Hamura, Nishitama, Tokyo, 190-l 1. Vnstitute of Biological Sciences, University of Tsukuba, Tsukuba, 305.
As reported in the previous paper (Ebara et al., 1990), spontaneous activity is recognized even in a heart fragment which is larger than about 1.5 mm in length. The heart may indicate a diffuse nature of pacemaker, and a caudal fragment of the heart is apt to show the fastest rhythm but a fast rhythm may occur in an anterior fragment. These observations may indicate that differences in the rate of heartbeats is conceivable among individual specimens and certainly among portions of the heart. In an isolated heart, the propagation direction is not always forward, but sometimes backward. The transfer of pacemaker site is often observed in an isolated whole heart or in a heart fragment. This suggests that the pacemaker may be located in various parts of the heart. The heart appears to play an important role in simply moving the body fluid toward the peripheral regions of the body, regardless of the orientation of the bloodstream. The action potential recorded extra- and intracellularly always showed slow diastolic depolarization, suggesting spontaneous activity within the myocardium itself (Fig. 1). The results obtained from extracellular recording of an intact heart (Fig. 2) also indicated slow diastolic depolarization. The action potential recorded from the heart hardly shows a plateau potential in general, like that obtained from the nodal tissue of vertebrate heart (Hoffman and Cranefield, 1960).
601
602
hINOBLI
Eem
et al.
I 10
Fig. 1. Transmembrane
see
see
action potentials obtained simultaneously from two muscle cells in an isolated heart.
Velocity of impulse propagation
The heart of the beetle is a long slender tube similar in shape to those of other insects. The velocity of impulse propagation can be accurately measured using the difference in time between two peaks of action potential recorded simultaneously at two sites of the heart (Fig. 3) and by the distance between these two sites, because propagation occurs almost linearly straight along the length of the heart. The conduction pathways between the two sites, however, cannot be identified. Propagation velocity varied widely with hearts and individuals, for instance, the mean value of 845 velocities obtained from a single specimen is 85.3 cm/set and the data are ranged from 5.2 cm to 2100 m/set. These observations were obtained at a temperature of 26.5”C. The results are indicated in Fig. 4 with open circles. Reversal of propagation direction was also frequently observed. Velocities of the two beating directions were not always equal. For example, the following results were obtained from a single heart at a temperature of 20.5”C (Table 1). Impulse propagation direction
As to the direction of impulse propagation, only two antagonistic directions are supposable and adoptable. Because propagation in the slender tubular heart shows a seemingly limited direction, further experiments may profit from study of propagation precisely in comparison with another heart such as the chambered heart of a vertebrate with three dimensions of propagation (Armour and Randall, 1970; Bonke, 1973). Under a serious condition of the heart or in a weakened animal, the impulse within the middle portion of the heart sometimes disappeared. This indicates that propagation was blocked at this part probably due to the ceasing of spontaneous activity. The heartbeat frequency obtained from each fragment of the heart shows a rate gradient along the length of the heart which may be applicable to that of the intact heart. The impulse does not always
\I
1
50mV
generate from the caudal region; in some individuals and in some cases the impulse originates from the anterior region and propagates towards the posterior. The flow of body fluid, is reversed in the latter case, but circulatory problems are unlikely to be brought about given the open vascular system that is common in insects. Impulse propagation and heartbeat rate
The propagation speed varied, as mentioned above. The wide distribution of values may be derived from an alignment coordination of spontaneous discharges corresponding to the phase-response curve (Ebara et al., 1990). One set of results is shown with closed circles in Fig. 4. Each numbered beat was obtained from succeeding action potentials at a temperature of 26.5”C. Figure 4 shows that it is conceivable that propagation velocity does not always correspond to heartbeat rate, nor does change in velocity always correspond to propagation direction. Considerable changes in velocity seem to be linked to the fundamental properties of propagation in the beetle heart. In the present experimental specimen, the forward heartbeat had a mean rate of 135.4 beats per minute and a mean propagation velocity of 155.1 cm/set (N = 77), whereas the backward heartbeat had a mean heartbeat rate of 155.4 beats per minute and a mean velocity of 40.9 cm/set (N = 7). During reverse propagation, velocity is often lower than that of forward propagation. DISCUSSION
Because of both the presence of spontaneity in every fragment of the heart and the presence of the cardiac action potential which always involves slow diastolic depolarization, the muscle cells of the heart are considered to possess a more or less automatic property in themselves. If two impulses develop almost simultaneously from two different sites of the heart, the velocity of the propagation between the two sites seemingly becomes extremely high, often,
2mV
Fig. 2. Action potentials recorded extracellularly from an intact heart with a suction electrode
603
Propagation of impulse in beetle heart
cl ul
0.5mV
2mv
1
set
Fig. 3. Two traces of action potentials recorded extracellularly and simultaneously from two sites of an isolated heart at a temperature of 26.5%. The distance between recorded sites was 5.1 mm. in fact, approximately infinite. It is conceivable that velocity is profoundly related to an alignment mechanism. The impulse generated from a faster pacemaker comes to precede the other, so that the impulse initiated from the true pacemaker propagates apparently to other portions which are so-called latent pacemakers. In the alignment coordination which is capable of modification of the intrinsic rhythm of the myocardia, muscle cells of the heart interact to shift their
inherent rhythms to speed up or slow down so as to establish some compromised frequency of rhythm. As a result, impulse propagation can be seen, and a delay in time between impulses generated spontaneously from two portions of the heart may determine the direction and the speed of propagation. In this case, the higher the rate of heartbeats the more the chance of a true pacemaker emerging. The impulse usually appears to propagate from the caudal to cephalic portion of the heart.
500
400 Velocity of Propagation (open circle) (cm/set) 300
Rate
of
Heartbeats (closed circle) (beats/min)
20
40 Number
of
60 the
Beat
Fig. 4. Velocity of propagation (open circle) and rate of heartbeats (closed circle) measured simultaneously from two sites (distance: 10.6 mm) of an isolated heart during the process of alignment coordination at a temperature of 26.5%. Abscissa shows number of the action potential. The reversed heartbeat is indicated with an asterisk in the figure.
604
ANNOBUEBARA et al. Table 1. Ranges of velocity variation in a single heart
Direction of propagation
Range of velocity
cm/set (mean)
Forward Backward
12.1-7880 14.3-47.8
(926.4) (23.9)
Electrical coupling is rarely found among muscle cells of the beetle heart, in contrast to other hearts such as those of rabbit and rat (Pollack and Huntsman, 1973). Accordingly, it cannot be suggested that electrical communication relates to the propagation of impulse as in the molluscan heart (Ebara, 1964, 1967, 1969; Irisawa et al., 1969). The reversal of heartbeat was first observed in insects by Marcello Malpighi in 1660 (Mislin, 1969). The reversal is explained as a basic problem of myogenic automatism (Richter, 1973). Anomalous spread of excitation was sometimes observed and the direction of conduction is flexible in the heart of the chick embryo (Sakai et al., 1983). In the bundle of His in mammalian heart (dog, calf and goat), a difference found between orthodromic and antidromic velocities is conceivably not significant (Alanis et al., 1959). The pacemaker site can change frequently in insect and molluscan hearts (Irisawa, 1978). The periodic reversal of heartbeat in Salpa (Ebara, 1954) and in ascidians (Ebara, 1961, 1971) occurs without any confusion. It was rarely observed that impulse propagation was completely abolished at a middle portion of the heart, unless the specimen became markedly weakened, or that two impulses initiating almost simultaneously from two sites of the heart conflicted with each other at a middle part. These findings suggest that the rhythm of the preceding pacemaker modified by the activity of the latent (following) pacemaker can accompany the rhythm of the following latent pacemaker altered by the activity of the preceding true pacemaker in consequence of the property represented by the phase-response curve reported in the previous paper (Ebara ef al., 1990). Even in cases in which the propagated impulse disappeared in a middle portion of the heart, a renewed impulse with a different cardiac rhythm generated from adjacent portion and spread in the same direction toward the end of the heart. Summation of short delays existing among myocardia of the beetle is considered to extend the length in time which the propagation is seen. Consequently, the velocity must vary extensively because of a wide range of distribution in length of the delay. Conduction velocities measured from adult and fetal mammalian myocardial tissues have ranged well below 1 m/set (Weidmann, 1970) with the exceptions of the Purkinje fiber (Cranefield and Hoffman, 1958). His bundle (Alanis et al., 1959) and false tendon (Cranefield, 1987) of some mammals which often show more than 1 m/set; in the chick embryo heart, 0.4-0.5 m/set and in cultured heart preparation, l-30 cm/set (DeHaan and Fozzard, 1975). In sheep ventricle the transverse conduction velocity was three times lower than the longitudinal conduction velocity (Weidmann, 1982). It can be concluded that propagation in the beetle heart is derived from simultaneous and coordinated
production of spontaneous impulses generated separately from two adjacent fibers, between which there is present little or no electrical coupling. In insect hearts there is no conductive tissue and no separated area for rhythm initiation (S-R6zsa and V-Sziike, 1972). In the larval heart of a moth, the conduction is performed forward at the speed of l-2 cm per second (McCann, 1963). In the beetle heart, adjacent fibers may be influenced by active fibers by electrical deflection produced through local circuit (Lehmkuhl and Sperelakis, 1965), even if a low resistance pathway does not assist in forming a small potential on the adjacent fiber (Ebara, 1969), or even if adjacent fiber may be affected by mechanical contraction exerted by active fibers (Uesaka et al., 1987). REFERENCES Alanis J., Lopez E. and Pulido J. (1959) The potential and the conduction velocity of the bundle of His. J. Physiol. 147, 315-324.
Armour J. A. and Randall W. C. (1970) Structural basis for cardiac function. Am J. Physiol. 218, 1517-1523. Bonke F. I. M. (1973) Electrotonic spread in the sinoatrial node of the rabbit heart. Pfliigers Arch. 339, 17-23. Cranefield P. F. and Hoffman B. F. (1958) Electrophysiology of single cardiac cells. Physiol. Rev. 38,41-76. Cranefield P. F. (1987) The conduction of the cardiac impulse 1951-1986. Experientia 43, 1040-1044. DeHaan R. L. and Fozzard H. A. (1975) Membrane response to current pulses in spheroidal aggregates of embryonic heart ce& J. gen. Physiol. 65, 20%222. Ebara A. (19541 The oeriodic reversal of the heart-beat in Salpa f&for&is. 199-217.
Sii. Rep. Tokyo Kyoiku Daigaku, B 7,
Ebara A. (1961) Circulation of the blood in the compound ascidian, Perophora orientalis .&rnbLck. Sci. Rep. Tokyo Kyoiku Daigaku, B 10, 53-60.
Ebara A. (1964) Effect of restricted conduction pathway on the transmembrane potential of oyster myocardium, Crassostrea gigas. Sci. Rep. Tokyo Kyoiku Daigaku, B 12, 1-8.
Ebara A. (1967) Coordination of activities between myocardia in oyster. Sci. Rep. Tokyo Kyoiku Daigaku, B 13, 129-137.
Ebara A. (1969) The role of small potentials in the regulation of rhythm in an oyster heart. Experientia, suppl. 15, 244-249.
Ebara A. (1971) Physiological relation of the dorsal ganglion to the heart of a compound ascidian, Perophora orientalis. Comp. Biochem. Physiol. 39A, 795-805.
Ebara A., Uesaka H. and Yamagishi H. (1990) Pacemaker activity in the heart of a beetle, Allomyrina dichotomus. Camp. Biochem. Physiol. 97A, 223-228.
Hoffman B. F. and Cranefield P. F. (1960) The sinoatrial node. The atrioventricular node. In Elecrrophysiology qf the Heart, pp. 104-174, McGraw-Hill, New York. Irisawa H.. Irisawa A. and Shiaeto N. (1969) Effect of Na+ and Ca2+ on the spontaneous excitation’of the bivalve heart muscle. Experientia, suppl. 15, 176-191. Irisawa H. (1978) Comparative physiology of the cardiac pacemake; medhanism. Physioi. kev. 58, 461-498. Lehmkuhl D. and Soerelakis N. (1965) Electronic soread of current in cultured chick heart dells. J. Cell: Camp. Physiol. 66, 119-133. McCann F. V. (1963) Electrophysiology of an insect heart. J. gen. Physiol. 46, 803-821.
McCann F. V. and Sanger J. W. (1969) Ultrastructure and function in an insect heart. Experienfia, suppl. 15, 29-46.
Propagation of impulse in beetle heart McCann F. V. (1970) Physiology of insect hearts. Ann. Reo. Enromol. 15, 173-200. Mislin H. (1969) Patterns of reversal in the heart of Ciona intestinalis L. Experientia, suppl. 15, 192-199. Pollack G. H. and Huntsman L. L. (1973) Intercellular pathways in the heart: Direct evidence for low resistance channels. Experienfia 29, 1501-l 502. Richter K. (1973) Struktur und Funktion der Herzen wirbelloser Tiere. 2001. Jahrb. Physiol. 71, 477-668. Sakai T., Hirota A., Fujii S. and Kamino K. (1983) Flexibility of regional pacemaking priority in early embryonic heart monitored by simultaneous optical recording of action potentials from multiple sites. Jap. J. Physiol. 33, 337-350.
605
S-Rozsa K. and V-Sziike I. (1972) Ion mechanism of the resting and action potentials in the heart of some insect species. Comp. Biochem. Physiol. 41A, 495-506. Uesaka H., Yamagishi H. and Ebara A. (1987) Stretchmediated interaction between the auricle and ventricle in an oyster Crassostrea gigus. Comp. Biochem. Physiol. 88A, 221-227. Weidmann S. (1970) Electrical constants of trabecular muscle from mammalian heart. J. Physiol. 210, 104-1054.
Weidmann S. (1982) Low resistance constants and the propagation of the cardiac action potential. In Normal and Abnormal Conduction in the Heart, pp. 43-52, Futura, New York.
Camp. Biochem. Physiol. Vol. 97A, No. 4, pp. 60-605, 1990 Printed in Great Britain
PROPAGATION OF IMPULSE IN THE HEART BEETLE ALLOMYRINA DICHOTOMUS ARINOBU
EBARA, HATSUMI
Institute of Physics,
AKIYAMA,*
HIROSHI YAMAGlsHIt
and
OF THE
HISASHI OHSHIMA
Science University of Tokyo, Kagurazaka, Shinjuku, Tokyo 162, Japan (Receiued 19 April 1990)
Abstract-l. Propagation of impulse is studied electrophysiologically in the heart of an adult armed wrestler beetle. 2. The velocity of propagation shows extensive range of values, for example, from 5.2 cm to 2100 m/set in a specimen at a temperature of 26.5% 3. The propagation is considered to be the result of the alignment behavior of pacemakers as represented
by a phase-response curve. 4. The propagation may be derived from sequence of impulses generated spontaneously and successively from one pacemaker to an adjacent one with a short delay, the length of which may vary widely.
INTRODUCTION
RESULTS No nervous element at all could be found in the action potential of the heart muscle from extracellular recording, even in the intracellular results. When a suction electrode was impaled through the body cavity avoiding the heart, rapid spike potentials were often observed sporadically and intermittently, clearly varying from the electrocardiogram in their time course. These rapid deflections might be nerve action potentials.
The contractile wave in the heart of an adult moth Hyalophora is peristaltic in nature and usually proceeds from the caudal toward the cephalic region at low velocity (about 25 mm/set) (McCann and Sanger, 1969). It appears that conduction velocity increases with heart rate in insects (McCann, 1970). On the other hand, in a previous paper (Ebara et al., 1990) it was reported that cardiac rhythm usually originated from the caudal region and sometimes from other portions of the heart, or occasionally from a middle part of the heart toward anterior and posterior end. The reversal of the beating direction has been noted in a number of insects at all stages of development (McCann, 1970). The present paper will propose some further interpretations of the propagation mechanism in the insect heart. MATERIAL
Initiating site of heart rhythm
AND METHODS
An adult armed wrestler beetle, Allomyrina dichotomus L., was used as the material. The isolated heart with a part of associated exoskeleton was usually set in a small elastic chamber in a solution composed df NaCl 160.7 rnG, KC1 2.7 mM. CaCl, 2.8 mM. NaHCO, 0.02%. For intracellular recoiding, a gliss pipette microelectrode filled with 3M KC1 and of lo-20 MR electrical resistance was employed. For extracellular recording, the usual method for recording action potential in the present paper involved using a small glass pipette, the tip of which was 50 _ 110 pm in diameter with a connected injection syringe as a suction electrode. The input signal was amplified and displayed on a sheet of recording paper with an electronic instrument (medicalcorder, PMP-3004 type, Nihon Kohden Kogyo Co.). Observation and experimentation was carried out at room temperatures (20.2-3 I PC). ‘Hamura High School, Hamura, Nishitama, Tokyo, 190-l 1. Vnstitute of Biological Sciences, University of Tsukuba, Tsukuba, 305.
As reported in the previous paper (Ebara et al., 1990), spontaneous activity is recognized even in a heart fragment which is larger than about 1.5 mm in length. The heart may indicate a diffuse nature of pacemaker, and a caudal fragment of the heart is apt to show the fastest rhythm but a fast rhythm may occur in an anterior fragment. These observations may indicate that differences in the rate of heartbeats is conceivable among individual specimens and certainly among portions of the heart. In an isolated heart, the propagation direction is not always forward, but sometimes backward. The transfer of pacemaker site is often observed in an isolated whole heart or in a heart fragment. This suggests that the pacemaker may be located in various parts of the heart. The heart appears to play an important role in simply moving the body fluid toward the peripheral regions of the body, regardless of the orientation of the bloodstream. The action potential recorded extra- and intracellularly always showed slow diastolic depolarization, suggesting spontaneous activity within the myocardium itself (Fig. 1). The results obtained from extracellular recording of an intact heart (Fig. 2) also indicated slow diastolic depolarization. The action potential recorded from the heart hardly shows a plateau potential in general, like that obtained from the nodal tissue of vertebrate heart (Hoffman and Cranefield, 1960).
601
602
hINOBLI
Eem
et al.
I 10
Fig. 1. Transmembrane
see
see
action potentials obtained simultaneously from two muscle cells in an isolated heart.
Velocity of impulse propagation
The heart of the beetle is a long slender tube similar in shape to those of other insects. The velocity of impulse propagation can be accurately measured using the difference in time between two peaks of action potential recorded simultaneously at two sites of the heart (Fig. 3) and by the distance between these two sites, because propagation occurs almost linearly straight along the length of the heart. The conduction pathways between the two sites, however, cannot be identified. Propagation velocity varied widely with hearts and individuals, for instance, the mean value of 845 velocities obtained from a single specimen is 85.3 cm/set and the data are ranged from 5.2 cm to 2100 m/set. These observations were obtained at a temperature of 26.5”C. The results are indicated in Fig. 4 with open circles. Reversal of propagation direction was also frequently observed. Velocities of the two beating directions were not always equal. For example, the following results were obtained from a single heart at a temperature of 20.5”C (Table 1). Impulse propagation direction
As to the direction of impulse propagation, only two antagonistic directions are supposable and adoptable. Because propagation in the slender tubular heart shows a seemingly limited direction, further experiments may profit from study of propagation precisely in comparison with another heart such as the chambered heart of a vertebrate with three dimensions of propagation (Armour and Randall, 1970; Bonke, 1973). Under a serious condition of the heart or in a weakened animal, the impulse within the middle portion of the heart sometimes disappeared. This indicates that propagation was blocked at this part probably due to the ceasing of spontaneous activity. The heartbeat frequency obtained from each fragment of the heart shows a rate gradient along the length of the heart which may be applicable to that of the intact heart. The impulse does not always
\I
1
50mV
generate from the caudal region; in some individuals and in some cases the impulse originates from the anterior region and propagates towards the posterior. The flow of body fluid, is reversed in the latter case, but circulatory problems are unlikely to be brought about given the open vascular system that is common in insects. Impulse propagation and heartbeat rate
The propagation speed varied, as mentioned above. The wide distribution of values may be derived from an alignment coordination of spontaneous discharges corresponding to the phase-response curve (Ebara et al., 1990). One set of results is shown with closed circles in Fig. 4. Each numbered beat was obtained from succeeding action potentials at a temperature of 26.5”C. Figure 4 shows that it is conceivable that propagation velocity does not always correspond to heartbeat rate, nor does change in velocity always correspond to propagation direction. Considerable changes in velocity seem to be linked to the fundamental properties of propagation in the beetle heart. In the present experimental specimen, the forward heartbeat had a mean rate of 135.4 beats per minute and a mean propagation velocity of 155.1 cm/set (N = 77), whereas the backward heartbeat had a mean heartbeat rate of 155.4 beats per minute and a mean velocity of 40.9 cm/set (N = 7). During reverse propagation, velocity is often lower than that of forward propagation. DISCUSSION
Because of both the presence of spontaneity in every fragment of the heart and the presence of the cardiac action potential which always involves slow diastolic depolarization, the muscle cells of the heart are considered to possess a more or less automatic property in themselves. If two impulses develop almost simultaneously from two different sites of the heart, the velocity of the propagation between the two sites seemingly becomes extremely high, often,
2mV
Fig. 2. Action potentials recorded extracellularly from an intact heart with a suction electrode
603
Propagation of impulse in beetle heart
cl ul
0.5mV
2mv
1
set
Fig. 3. Two traces of action potentials recorded extracellularly and simultaneously from two sites of an isolated heart at a temperature of 26.5%. The distance between recorded sites was 5.1 mm. in fact, approximately infinite. It is conceivable that velocity is profoundly related to an alignment mechanism. The impulse generated from a faster pacemaker comes to precede the other, so that the impulse initiated from the true pacemaker propagates apparently to other portions which are so-called latent pacemakers. In the alignment coordination which is capable of modification of the intrinsic rhythm of the myocardia, muscle cells of the heart interact to shift their
inherent rhythms to speed up or slow down so as to establish some compromised frequency of rhythm. As a result, impulse propagation can be seen, and a delay in time between impulses generated spontaneously from two portions of the heart may determine the direction and the speed of propagation. In this case, the higher the rate of heartbeats the more the chance of a true pacemaker emerging. The impulse usually appears to propagate from the caudal to cephalic portion of the heart.
500
400 Velocity of Propagation (open circle) (cm/set) 300
Rate
of
Heartbeats (closed circle) (beats/min)
20
40 Number
of
60 the
Beat
Fig. 4. Velocity of propagation (open circle) and rate of heartbeats (closed circle) measured simultaneously from two sites (distance: 10.6 mm) of an isolated heart during the process of alignment coordination at a temperature of 26.5%. Abscissa shows number of the action potential. The reversed heartbeat is indicated with an asterisk in the figure.
604
ANNOBUEBARA et al. Table 1. Ranges of velocity variation in a single heart
Direction of propagation
Range of velocity
cm/set (mean)
Forward Backward
12.1-7880 14.3-47.8
(926.4) (23.9)
Electrical coupling is rarely found among muscle cells of the beetle heart, in contrast to other hearts such as those of rabbit and rat (Pollack and Huntsman, 1973). Accordingly, it cannot be suggested that electrical communication relates to the propagation of impulse as in the molluscan heart (Ebara, 1964, 1967, 1969; Irisawa et al., 1969). The reversal of heartbeat was first observed in insects by Marcello Malpighi in 1660 (Mislin, 1969). The reversal is explained as a basic problem of myogenic automatism (Richter, 1973). Anomalous spread of excitation was sometimes observed and the direction of conduction is flexible in the heart of the chick embryo (Sakai et al., 1983). In the bundle of His in mammalian heart (dog, calf and goat), a difference found between orthodromic and antidromic velocities is conceivably not significant (Alanis et al., 1959). The pacemaker site can change frequently in insect and molluscan hearts (Irisawa, 1978). The periodic reversal of heartbeat in Salpa (Ebara, 1954) and in ascidians (Ebara, 1961, 1971) occurs without any confusion. It was rarely observed that impulse propagation was completely abolished at a middle portion of the heart, unless the specimen became markedly weakened, or that two impulses initiating almost simultaneously from two sites of the heart conflicted with each other at a middle part. These findings suggest that the rhythm of the preceding pacemaker modified by the activity of the latent (following) pacemaker can accompany the rhythm of the following latent pacemaker altered by the activity of the preceding true pacemaker in consequence of the property represented by the phase-response curve reported in the previous paper (Ebara ef al., 1990). Even in cases in which the propagated impulse disappeared in a middle portion of the heart, a renewed impulse with a different cardiac rhythm generated from adjacent portion and spread in the same direction toward the end of the heart. Summation of short delays existing among myocardia of the beetle is considered to extend the length in time which the propagation is seen. Consequently, the velocity must vary extensively because of a wide range of distribution in length of the delay. Conduction velocities measured from adult and fetal mammalian myocardial tissues have ranged well below 1 m/set (Weidmann, 1970) with the exceptions of the Purkinje fiber (Cranefield and Hoffman, 1958). His bundle (Alanis et al., 1959) and false tendon (Cranefield, 1987) of some mammals which often show more than 1 m/set; in the chick embryo heart, 0.4-0.5 m/set and in cultured heart preparation, l-30 cm/set (DeHaan and Fozzard, 1975). In sheep ventricle the transverse conduction velocity was three times lower than the longitudinal conduction velocity (Weidmann, 1982). It can be concluded that propagation in the beetle heart is derived from simultaneous and coordinated
production of spontaneous impulses generated separately from two adjacent fibers, between which there is present little or no electrical coupling. In insect hearts there is no conductive tissue and no separated area for rhythm initiation (S-R6zsa and V-Sziike, 1972). In the larval heart of a moth, the conduction is performed forward at the speed of l-2 cm per second (McCann, 1963). In the beetle heart, adjacent fibers may be influenced by active fibers by electrical deflection produced through local circuit (Lehmkuhl and Sperelakis, 1965), even if a low resistance pathway does not assist in forming a small potential on the adjacent fiber (Ebara, 1969), or even if adjacent fiber may be affected by mechanical contraction exerted by active fibers (Uesaka et al., 1987). REFERENCES Alanis J., Lopez E. and Pulido J. (1959) The potential and the conduction velocity of the bundle of His. J. Physiol. 147, 315-324.
Armour J. A. and Randall W. C. (1970) Structural basis for cardiac function. Am J. Physiol. 218, 1517-1523. Bonke F. I. M. (1973) Electrotonic spread in the sinoatrial node of the rabbit heart. Pfliigers Arch. 339, 17-23. Cranefield P. F. and Hoffman B. F. (1958) Electrophysiology of single cardiac cells. Physiol. Rev. 38,41-76. Cranefield P. F. (1987) The conduction of the cardiac impulse 1951-1986. Experientia 43, 1040-1044. DeHaan R. L. and Fozzard H. A. (1975) Membrane response to current pulses in spheroidal aggregates of embryonic heart ce& J. gen. Physiol. 65, 20%222. Ebara A. (19541 The oeriodic reversal of the heart-beat in Salpa f&for&is. 199-217.
Sii. Rep. Tokyo Kyoiku Daigaku, B 7,
Ebara A. (1961) Circulation of the blood in the compound ascidian, Perophora orientalis .&rnbLck. Sci. Rep. Tokyo Kyoiku Daigaku, B 10, 53-60.
Ebara A. (1964) Effect of restricted conduction pathway on the transmembrane potential of oyster myocardium, Crassostrea gigas. Sci. Rep. Tokyo Kyoiku Daigaku, B 12, 1-8.
Ebara A. (1967) Coordination of activities between myocardia in oyster. Sci. Rep. Tokyo Kyoiku Daigaku, B 13, 129-137.
Ebara A. (1969) The role of small potentials in the regulation of rhythm in an oyster heart. Experientia, suppl. 15, 244-249.
Ebara A. (1971) Physiological relation of the dorsal ganglion to the heart of a compound ascidian, Perophora orientalis. Comp. Biochem. Physiol. 39A, 795-805.
Ebara A., Uesaka H. and Yamagishi H. (1990) Pacemaker activity in the heart of a beetle, Allomyrina dichotomus. Camp. Biochem. Physiol. 97A, 223-228.
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