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Simultaneous electrocardiograms and myograms of the isolated atrium ventricle and conus of the embryonic chick heart.

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Simultaneous Electrocardiograms and Myograms of
the Isolated Atrium, Ventricle and Conus of the
Embryonic Chick Heart'
GEORGE H. PAFF AND ROBERT J. BOUCEK
Departments of Anatomy and Medicine, University of Miami School
of Medicine, Coral Gables, Florida
Recently Paff, Boucek and Murphy ('59)
demonstrated a technique for recording the
mechanical behavior of the early embryonic chick heart. Stimulated by the work
of Wertheim-Salomonson, '13; Robb, '29;
Lagan and Sampson, '32; Bogue, '33;
Eyster, Krasno and Hettwer, '37; Hoff,
Kramer, Dubois and Patten, '37; and Lazzarini and Bellville, '56, whose cumulative
effort firmly established the fact that the
adult type of electrocardiogram can be recorded in the embryonic chick heart before
the third day of development, Boucek,
Murphy and Paff ('59) developed a method
for synchronizing the electrocardiogram
with the myogram. The present work is
an application of this expanded technique
to the study of isolated chambers of the
72 hour embryonic chick heart. It is presented for three reasons: lst, nowhere in
the literature can one find simultaneous recordings of myograms and electrocardiograms of the isolated atrium, ventricle and
conus; 2nd, regarding the electrical activity, the records permit a dissection of the
electrocardiogram to demonstrate characteristics of the three areas of the heart
previously not seen; and 3rd, a comparison
can be made between the electrical and
mechanical properties of the chambers of
the intact heart with those of the separated chambers.
TECHNIQUE
A 72 hour embryonic chick heart is isolated by transecting the conus and the
great veins where they enter the sinus
venosus. The heart is then planted in a
drop of brittle blood plasma (old rooster)
to which a trace of embryonic extract has
been added. After clotting occurs it is
transected cleanly at the atrioventricular
and ventriculoconal junctions. Each of the
three chambers, i.e., atrium, ventricle and
conus are then spatially separated.
Platinum electrodes are placed in position preparatory to recording the ECG and
myogram simultaneously. With the aid of
a microscope the exploring electrode is
placed on the atrium (ventricle or conus)
while the indifferent electrode is placed
in the medium in which the heart is beating (figs. 1, 2). This represents the essential circuit for the electrocardiogram. Action currents pass to an amplifier which
permits a gain of 400: 1 and thence to a
direct writing Sanborn recorder.
The exploring electrode (fig. 2 ) serves
a dual purpose. Not only is it essential to
recording the ECG, it is also one arm of a
lever whose fulcrum is centered in a piece
of plastic which insulates i t from the opposite arm of the lever. The latter passes
between two condensing plates and, with
each beat of the heart, it oscillates between
the plates. It is part of the apparatus for
recording the myogram (Boucek et al. ,'59).
All records were taken at a temperature of
approximately 30°C.
0 8 SERVATIONS
For reference purposes a typical electrocardiogram of an isolated 72 hour embryonic chick heart has been included (fig. 3 ) .
To obtain this record the exploring electrode was placed near the greater curvature of the ventricle (see insert). Note the
three major deflections, i.e., the P wave,
RS complex and T wave.
Z-SLnior Investigator, Howard Hughes Medical Institute.
73
74
GEORGE H. PAFF AND ROBERT J. BOUCEK
Fig. 1 Seventy-two hour heart showing chambers separated after transection. The numbers 4 to 9 indicate where the exploring electrode was placed to obtain the correspondingly
numbered records shown in plate 1, figures 4 to 9. The black circle represents the indifferent
electrode.
Figures 4, 5 and 6 are simultaneous recordings of the electrical and mechanical
activity in the atrium, ventricle and conus
respectively of a heart which was transected at the atrioventricular and ventriculoconal junctions. Figures 7, 8 and 9 are
similar recordings for a second heart. The
positions of the exploring and indifferent
electrodes used to obtain each of the 6 recordings is indicated by corresponding
numbers in figure 1 (e.g., to obtain the
record shown in figure 4 the position of
the exploring electrode is indicated by the
black “4” on the isolated atrium).
The records for the chambers of the
first heart (figs. 4, 5 and 6 ) reveal in the
atrium the positive-negative deflection of
the P wave (depolarization) followed by
the negative T wave (repolarization). The
time which elapses between the beginning
of the P wave and the onset of atrial systole,
hereafter referred to as the electro-mechanical delay (EM), is 0.038 sec. The duration of the atrial contraction is relatively
short and the extent of systolic excursion
as indicated by the height of the myogram
is relatively small. The rate of the isolated
atrium was 100 per min. Previous to tran-
75
ACTIVITY O F EMBRYONIC HEARTS
z
indiffered
t's
decfrode
on ventricle; i n d i f f e r e n f
electrode i s ;n plasm0
.
Fig. 2 Schematic diagrams showing the essential features of the apparatus for recording ECG's
and myograms. Please see text for explanation.
section the rate of the entire heart was 96
beats per min.
The electrical activity of the ventricle
(fig. 5) is represented by an RS complex
(depolarization) which precedes the peaked
repolarization wave T. The delay between
the onset of the RS complex and the beginning of ventricular systole i.e., the electromechanical delay (EM) is 0.038 sec. As
for the ventricular myogram, its overall
appearance is one of power. From experience we know that this is expressed primarily by the height of the rapid initial
thrust seen in the first part of the systolic
rise from the baseline and the total height
of the curve. The ventricle was beating 42
times per min.
Finally in figure 6 is shown a record of
the electrical and mechanical activity of
the conus. The positive peaked depolorization wave, R, followed by the negative repolarization T wave. The EM is 0.04 sec.
and the height of the conal myogram is
intermediate between those for the atrium
and ventricle. The rate of beat of the isolated conus was 3 per min.
The electrical and mechanical activity
for the isolated atrium, ventricle and conus
of a second heart is shown in figures 7, 8
and 9. Considering electrical activity first,
it is apparent that while a depolarization
wave followed by a repolarization wave is
present in the record for each chamber,
the deflection from the baseline in each
case is practically opposite in direction to
that seen in the isolated chambers of the
previous heart (compare figs. 4 and 7, 5
and 8, 6 and 9). The position of the exploring electrode was different for each
corresponding pair of records (see figs. 1,4
and 7, 5 and 8, 6 and 9). In these experiments the EM was 0.037 sec. for atrium;
0.02 sec. for the ventricle; and 0.03 sec.
for the conus. The height of the myogram
was least for the atrium, greatest for the
ventricle and intermediate for the conus.
The rate of beat was 96,40, and 6 per min.
respectively for the atrium, ventricle and
conus. Before sectioning the heart rate
was 96 per min.
76
GEORGE H. PAFF AND ROBERT J. BOUCEK
DISCUSSION
In presenting the technique, a point was
made of the fact that the isolated hearts
were placed in brittle blood plasma before
they were sectioned. In preliminary experiments the hearts were transected in a
fluid medium with discouraging results
i.e., the electrocardiograms and myograms
showed evidence of extensive damage. A
soft plasma clot from a young rooster was
an improvement but the brittle plasma
from an old rooster was found to be best.
Under these conditions when a sharp knife
was passed cleanly through the embedded
hearts at the atrioventricular and ventriculoconal junctions, the chambers retained
their shapes, damage was reduced to a
minimum, and the electrodes could be positioned with ease.
An electrocardiogram consists of a series
of deflections from a base or isoelectric
line. Each of these deflections is referable to depolarization or repolarization of
the surface membranes in a certain part
of the heart. By sectioning the isolated
heart between the atrium and ventricle
and between the ventricle and conus each
chamber can be made to exhibit its own
electrical and mechanical activites. A depolarization and repolarization wave for
each of these chambers is then observed.
'This isolated activity is usually not observed in the electrocardiograms of the
intact heart because the repolarization phenomenon of the atrium occurs simultaneously with depolarization of the ventricle.
[n human electrocardiography, the repolarization wave of the atrium can be seen
only when a dissociation of the atrium
and the ventricle occurs as the result of
some diseased state.
The electrocardiograms from the three
isolated areas differ in the duration of repolarization. Electrical systole, i.e., the
time between the R- and the T-wave is
shortest in the atrium and longest in the
conus. The R-S portion consumes little
time, the greater proportion of electrical
systole consisting of the S-T interval plus
the T-wave. This latter portion of the
electrocardiogram is considered to be rerelated to the metabolic processes of recovery and repolarization.
In the three fragments of the embryonic
heart the electro-mechanical delay was
practically similar, 0.034 sec. average.
These fragments possess an inherent and
similar property of response to electrical
stimulation. This is quite different from
values obtained in the intact embryonic
heart (Boucek et al., '59) in which the
electro-mechanical delay of the atrium was
shorter than the ventricle and the conus
was approximately three times as long as
the other two areas. The reason for the
difference between the intact and the fragmented heart in the electro-mechanical delay is not apparent.
It is important, however, that such a
controlling mechanism exists in the tubular embryonic heart. The conus must remain inactive during the major portion of
veiitricular contraction if a patent outflow
tract during the period of ventricular systole is to be maintained. The mechanism
of the protracted EM delay in the conus
of the intact heart may be related to the
slow recovery process of this portion of the
heart. This would explain the long R-T
interval of the isolated conus. Perhaps
when the conus is driven at a higher rate
by the atrium, the slow recovery of the
conus delays the mechanical response to
the electrical impulse.
Contraction and relaxation times of the
fragments do not differ from those of the
intact heart. The longer contraction and
relaxation times of the conus, a slow sinusoidal type of activity, are similar to the
ventricular myograms of the embryonic
heart at 30 and 32 hours of development.
The similarity extends to the slow intrinsic
rate and to the long electro-mechanical
activation time of the earlier embryonic
heart. This suggests that the conus remains the least differentiated portion of
the tubular heart at the 72 hour period.
In these records of the electrocardiograms of the separate chambers it is noted
that the depolarization wave of a given
chamber might vary, depending upon the
position of the exploring electrode. Variations in the direction of the wave are related to the position of the electrode in
reference to the predominant electrical
vectorial forces. As was observed earlier,
electrocardiographic evidence of a preferential pathway of activation of the impulse
exists in these early stages of the heart.
ACTIVITY O F EMBRYONIC HEARTS
antedating any morphologically recognizable conduction system.
SU IMMARY
1. Simultaneous recordings of electro-
cardiograms and myograms of the isolated
atrium, ventricle and conus of 72 hours
embryonic chick hearts planted in blood
plasma have been presented.
2. The electrocardiograms show in each
case both a depolarization and a repolarization wave.
3. The time between the beginning of
the electrical effect and mechanical response is practically similar in the three
chambers i.e., 0.034 sec. as an average.
The probable significance of this is discussed.
4. The height of the myogram is least
for the atrium, greatest for the ventricle
and intermediate for the conus.
LITERATURE CITED
Bogue, Y. J 1932 The heart rate of the developing chick. J. Exp. Biol., 9: 351-358.
77
Boucek, R. J., W. P. Murphy, Jr. and G. H. Paff
1959 Electrical and mechanical properties of
chick embryo heart chambers. Circulation Res.,
7: 787-793.
Eyster, J. A. E., M. R. Krasno and J. P. Hettwer
1937 Electrical potentials of the heart of the
chick embryo. Amer. J. Physiol., 120: 173.
Hoff, E. C., T. C. G a m e r , D. DuBois and B. M.
Patten 1937 The development of the electrocardiogram of the embryonic heart. Amer.
Heart J., 17: 4, 470-488.
Lagan, J. B., and J. J. Sampson 1932 Influence
of digitalis on the electrocardiogram of the
chick embryo. Proc. SOC. Exper. Biol. Med.,
29: 735.
Lazzarini, A. A., Jr., and J. W. Bellville 1956
Method for study of E. K. G. of early chick
embryo within the shell. Proc. SOC. Exp. Biol.,
93(1): 27-30.
Paff, G. H., R. J. Boucek and W. P. Murphy, Jr.
1959 Atrial, ventricular and conal myograms
of the embryonic chick heart. Anat. Rec., 133:
47-55.
Robb, J. S. 1929 The elemental character of
embryonic electrocardiograms. Amer. J. Physiol., 90: 496.
Wertheim-Salomonson, J. K. A. 1913 Das elektrokardiogramm von Hunerembryonen. Pflug.
Arch. j.d. ges. Physiol., 153: 533.
PLATE 1
EXPLANATION OF FIGURES
3
Electrocardiogram of isolated 72 hour embryonic heart showing typical
P, RS and T waves.
4
ECG and myogram of isolated atrium showing P and T waves.
5
ECG and myogram of isolated ventricle showing RS and T waves.
Same heart as in figure 4.
6
ECG and myogram of isolated conus showing R and T waves. Same
heart as in figures 4 and 5 .
7 ECG and myogram of isolated atrium of a second heart showing P
and T waves.
8
ECG and myogram of isolated ventricle showing R and T waves.
Same heart as in figure 7.
9 ECG and myogram of isolated conus showing S and T waves. Same
heart as in figures 7 and 8.
78
ACTIVITY OF EMBRYONIC HEARTS
George H. Paff and Robert J. Boucek
PLATE 1
79
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