Download Electrical Activity During the PR Interval

Electrical Activity During the P-R Interval
By
BRIAN F . HOFFMAN, M.D., PAUL P . CRANEFIELD, P H . D . ,
JACKSON H. STUCKEY, M.D.,
AND ALBIN A. BAGDONAS, M.D.
With the assistance of Juan Piera, M.D.
and left ventricles.0"11 This method, which
permits exact localization of the recording
electrodes without apparent injury to the tissues under investigation, has been used to
record from the His bundle, the bundle
branches and the false tendons of the canine
heart. The electrical activity of the specialized conducting system has been correlated
with the standard electrocardiogram both in
the open-chest preparation and in the intact
animal after completion of the surgical repair.
R
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ECENT studies of the electrical activity
of single cardiac fibers suggest that
most, if not all, disturbances of rhythm have
their origin in specialized cardiac tissues
rather than in the muscle fibers of the atria
or ventricles.1'2 Similarly, many disorders of
conduction result from disordered function of
these same structures.2 Unfortunately, the
leads employed in clinical electrocardiography
fail to show any direct indication of electrical
activity of nodal tissue or of the specialized
conducting system. Even if electrocardiograms
are recorded directly from the epicardial surface of the heart, no obvious deflections occur
during P-R interval which are attributable to
activity in the atrioventricular node, the His
bundle, bundle branches and the Purkinje
fibers. In attempting to detect activity in
these tissues, only a few records have been
obtained from the sinoatrial3 and atrioventricular nodes3'4 and Purkinje system5"7 of
closed heai'ts by means of needle electrodes
inserted through the epicardium and into
these structures. However, this method has
the disadvantage that extract localization of
the electrodes is difficult and that injury to
tissue surrounding the electrode tip is inevitable. Bipolar needle electrodes also have been
used to record from the His bundle of isolated
perfused dog hearts.s
It is possible to record the electrical activity
of the specialized ventricular conducting S3'stem during total cardiopulmonary bypass
through small electrodes attached to the endocardial surfaces of the right atrium and right
Methods
Surgical Technics
Healthy mongrel dogs weighing 18 to 23 Kg.
were anesthetized by intravenous injection of 2.5
per cent thiopental sodium and placed on controlled respiration. The chest was opened transsternally at the level of the fifth interspace and
tapes were placed around the superior and the
inferior venae cavae. The pericardium was opened
widely and the dog was given an intravenous
injection of heparin, 2.5 mg./Kg. body weight.
One venous drainage catheter of the bypass circuit
was introduced into the superior vena eava through
the azygos vein and a second was introduced
directly into the inferior vena cava. The arterial
cannula was placed in the femoral artery. Venous
blood flowed by gravity from the superior and
inferior venae cavae to the oxygenator where it
was oxygenated in an atmosphere of 97 per cent
oxygen and 3 per cent carbon dioxide in a rotating
disk oxygenator and then returned to the animal
by occlusive roller pump through the femoral
artery. Cardiopulmonary bypass was achieved by
tightening the slings around the catheters in the
superior and inferior venae cavae.
With the dog on cardiopulmonary bypass, the
right atrium and one or both ventricles were
opened. In making the right ventriculotomy incision care was taken not to injure the freerunning Purkinje fibers which extend from the
base of the anterior papillary muscle to the wall
of the right ventricle.
Blood was titrated against protamine at 30
minute intervals and a heparin level of SO to 90
gamma per ml. was maintained throughout perfusion. The rectal temperature was maintained
From the Departments of Physiology and Surgery,
State University of New York Downstate Medical
Center, Brooklyn, N. T.
Supported in part by grants from the American
Heart Association and the TJ. S. Public Health Service (H-3916; H-4801; H-1101).
Beceived for publication June 3, 1960.
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Circulation Research, Volume VIII. November 1960
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at 37 to 38 C. by incorporating a heat exchanger
in the perfusion circuit. The mean blood pressure was kept above 100 mm. Hg during the
perfusion by flow rates of 80 to 90 ml. of blood
per Kg. of body weight.
Recording Technics
The recording electrodes employed in these experiments consisted of fine silver wires embedded
in plastic plaques.* The diameter of the wire
varied from 0.036 to 0.12 mm. depending on the
number of contacts and the use of the electrode.
Each plaque contained from 3 to 16 contacts
separated by distances of 0.3 to 1.0 mm. The
plaque containing the silver wires was attached
to the endocardium at the desired location by 5-0
silk sutures which were located 1.5 to 3.0 mm.
from the actual recording site. Similar electrodes
usually were attached to the epicardium of the
right atrium and right or left ventricle to record
from these chambers and to apply driving and
testing stimuli. A plastic probe containing 2 or
4 contacts at the tip was employed as an exploring
electrode to locate the optimum site for recording
the electrical activity of the bundle of His and
the right and left bundle branches. Records from
the free-running Purkin je fibers in the false tendons were obtained through electrodes embedded
in a small groove in a similar plastic probe; this
probe was positioned manually so that the electrodes made only light contact with the false
tendons.
Bipolar leads were employed for most tracings
of the electrical activity of the specialized conducting system; unipolar tracings using the left
leg for the indifferent electrode were recorded
in some instances. For most records from the
specialized conducting system the low frequency
components of the electrogram were filtered to
increase baseline stability and to facilitate identification of the electrical activity of the specialized
fibers. The characteristics of the filters employed
are shown in figure 1; filter settings, where pertinent, are specified for each illustration. Records
were displayed on an 8-trace switched beam oscilloscope (Electronics for Medicine) and photographed
on 7-inch paper moving at a speed of 200 mm./sec.
Driving and testing stimuli were provided by
American Electronics stimulators and stimulus
isolation units. Electrocardiograms were recorded
through needle electrodes by means of a standard
ECG preamplifier. The temperature of the endoeardial surface of the heart was recorded by means
of a miniature thermister which was placed on the
*The authors would like to acknowledge the kindness of Professor T>. Durrer of Amsterdam who
supplied 2 excellent 10-contact electrodes of extremely
small size.
Circulation Research, Volume VIII, November 1960
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Figure 1
Characteristics of loio-pass and high-pass filters
of preamplifiers. (A) Low-pass filter set at 0.1
c.p.s.; high-pass filter settings at 2,000 c.p.s.
(o—o), 500 c.p.s. (•—•) and 100 c.p.s. (x—a;).
(B) Response plotted as per cent of maximum
amplitude with low-pass filter at 0.1 c.p.s. when
low- and high-pass filters were at the folloicing
settings: (•—•) 4,500; (o—o) 4^00; (x—x)
1.2,500; and (A.—A), 40,500.
endocardium next to the electrode sites after each
series of recordings.
Results
Electrical Activity of the Bundle of His
Identification of Records
Figure 2 shows records of the electrical
activity of the His bundle recorded from an
intact dog, after closure of the heart and
thoracotomy incision, through electrodes attached to atrial muscle overlying the common
bundle. Also shown are bipolar electrograms
recorded directly from the right atrium and
the right and left ventricles and a standard
lead II electrocardiogram. The bipolar electrogram recorded through the electrodes located over the common bundle shows 3
discrete complexes: The first set of the deflections (a) appears slightly after the earliest
recorded atrial activity and clearly results
from depolarization of atrial muscle; the final
HOFFMAN, CRANEFIELD, STUCKEY, BAGDONAS
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Figure 2
Bipolar electrograms recorded from a closed-chest
dog through implanted electrodes and a lead II
electrocardiogram. (A) Records obtained 2 hours
after surgical preparation. Top trace, electrogram
from right atrial appendage; second trace, electrograin from bundle of His; third and fourth traces,
electrograms from the right and left ventricles;
bottom trace, lead II. In the His electrogram, (a)
indicates local atrial activity and (h) electrical activity in the common bundle. Low- and high-pass
filter settings for His electrogram at 40/1,000 and
for other electrograms at 4/200 (B) Lead II electrocardiogram recorded immediately prior to surgery; compare with similar records in (A) and
(C). (C) Records obtained from the same animal
one day after surgical preparation shoiving the
same sequence of leads as in (A). Polarity of His
electrogram reversed. Note general similarity of
His electrogram and constancy of P-R interval of
electrocardiogram. Filter settings at 40/2,000 for
His bundle and 4/500 for other electrograms. In
this and all subsequent records, time lines indicate
intervals of 40 msec.
set of deflections occurs during and after the
S wave of the electrocardiogram and presumably results from depolarization of the base
of the interventricular septum and the crista
supraventrieularis.12 The second set of deflections (h), identified as resulting from electrical activity in the bundle of His, appears
midway in the P-R interval of lead I I ; it thus
follows the end of atrial activity and precedes the earliest depolarization of ventricular
muscle. A similar deflection has been recorded
from the His bundle by Alanis.8
Several criteria can be employed in support
of the identification of this complex with the
electrical activity of the bundle of His. A
complex similar to that indicated by h in figure 2 could be recorded only from a sharply
circumscribed area which agreed in extent
with the anatomic location of the common
bundle. The possibility that the h complex
resulted from electrical activity in the atrioventricular node was made unlikely by results
obtained during stimulation of the cut peripheral end of either vagus nerve. As shown in
figure 3, when the atrium was driven electrically at a constant rate, vagal stimulation
caused a progressive increase in the separation between the atrial (a) and His bundle
(h) complexes (fig. 3B) indicating that the
activity identified as depolarization of the His
bundle originated distal to the site of increased A-V delay and thus distal to the atrioventricular node.13'14 Also, during the period
of complete A-V dissociation caused by vagal
activity (fig. 3B) the atrial component of the
electrocardiogram (a) recorded from the vicinity of the common bundle can be identified
with ease. In many experiments, identification
of the His electrogram was facilitated by
studying records obtained during spontaneous
or induced ventricular extrasystoles or after
"vagal escape." Results varied depending on
the site of origin of the extrasystole and the
rapidity with which activity entered the specialized conducting system ; in some instances,
the His electrogram was buried in the complex resulting from ventricular depolarization, but often a clearly identifiable electrogram recorded from the bundle of His preCirculation Research, Volume Vlll, November 1960
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ceded the local ventricular electrogram while
the component due to atrial depolarization
followed ventricular activity after an appropriate V-A (vcntriculo-atrial) delay (see figs.
4 and 6).
The records shown in figure 4 are of interest, not only with respect to the question of
identification of the electrogram recorded
from the bundle of His, but also in relation
to the site of the ventricular pacemaker during the A-V dissociation caused by vagal
activity. In this experiment, records were obtained during cardiopulmonary bypass. Electrodes were attached to the right atrial appendage, over the common bundle, over the
anterior portion of the left bundle branch at
its site of emergence from the left septal surface, and at a point close to the junction of the
anterior false tendon with the anterior papillary muscle of the left ventricle. The sequence
of discrete electrograms recorded from the
bundle of His (h)and from the 2 ends of the
false tendon is the same before (A) and during (B) vagal stimulation. However, the shift
in the atrial electrogram indicates that during
vagal activity the pacemaker site shifted to
some location in the His bundle. The absence
of an appreciable change in the time interval
between activity in the His bundle and other
sites in the specialized conducting system,
taken in conjunction with the long delay between the His complex and the atrial electrogram, strongly supports the conclusion that
the pacemaker site is distal to the atrioventricular node. This observation is in agreement with results obtained from records of
the transmembrane potentials of single fibers
in the His bundle and atrioventricular node
of isolated preparations of rabbit and dog
hearts.14 These records, in conjunction with
those in figure 3, also show that vagal activity
sufficient to cause complete atrioventricular
dissociation has no measurable effect on conduction velocity in the bundle of His, the
bundle branches or the Purkinje fibers of the
ventricular conducting system. This result
would be expected from the results of studies
of transmembrane potentials of isolated
preparations.2-15
Circulation Research, Volume VIII, November I960
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Figure 3
Electrocardiogram and electrogranns recorded from
the same animal as for figure 2, showing the effects
of stimulation of the vagus nerve. (A) Control
conditions; electrograms from above down show
activity of right atrial appendage, bundle of His
(filter settings 40/1,000), bundle of Sis (filter
settings 4/200), and left ventricle. Bottom trace
is a> lead II electrocardiogram. Note effect of amplifier frequency response on relative amplitude of
His bundle electrogram. (B) Vagal stimulation.
Note prolongation of delay betiveen atrial (a) and
His bundle (h) activity and unchanged interval
between activity in His bundle and ventricle. The
appearance of complete failure of A-V nodal transmission of the second atrial impulse clearly identifies
the atrial component of the His bundle electrogram.
Form of the His Bundle Electrogram
We have made no systematic attempt to
study the confirmation of the electrogram recorded from the bundle of His at different
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HOFFMAN, CRANEFIELD, STUCKEY, BAGDONAS
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Figure 4
Biopolar electrograms recorded from 4 different
sites during total cardiopulmonary bypass. Heart
temperature 37.5 G. Top trace, right atrial appendage; second trace, bundle of His; third trace,
septal end of anterior false tendon of left ventricle; bottom trace, peripheral end of same false
tendon. (A) Control records: (a), atrial electrogram complex; (h), His bundle electrogram; (s),
electrogram from septal end of false tendon; and
(p), electrogram from peripheral Purkinje fibers.
Filter settings of 12/500 employed for bundle of
His and 4/200 for all other traces. (B) Effect of
vagal stimulation. Note that earliest recorded
electrical activity is the electrogram complex of
the His bundle, that conduction time from His to
2)eripheral Purkinje fiber is unchanged and that
the conduction time from the bundle of His to the
atrium is approximately twice the normal atriumHin interval. The absence of change in the polarity
of the biphasic His deflection suggests that the
pacemaker site is between the recording electrode
and the atrioventricular node.
locations; indeed, in most experiments, filters
were employed to emphasize this complex in
the electrogram and to diminish in amplitude
any activity of atrium or ventricle which
might distort or mask the activity recorded
from the specialized tissue. For the same
reason, most records were obtained with contiguous bipolar electrodes. The effect of the
filters on the bipolar electrogram can be seen
in figure 3. In this tracing, the records on
the second and third lines were obtained
through the same set of close bipolar leads
using a different filter setting for each channel. It is clear from a comparison of the
relative amplitudes of His bundle and ventricular electrograms that a poor highfrequency response seriously limits ability to
obtain good records from the His bundle.
Similarly, if the low-frequency components
of the ventricular electrogram are present,
the relative amplitude of the h complex is
less and its identification is made more difficult. Unipolar electrograms were recorded
only infrequently from the His bundle. The
third trace of figure 5 shows one such set
of records obtained from a closed-chest dog
through an electrode containing 5 contacts
and located over the common bundle. Also
shown in the figure are bipolar electrograms
recorded from the right atrium, the bundle
of His, the left ventricle and a standard lead
II electrocardiogram. The unipolar His bundle
electrogram obviously varies in shape depending on the location of the electrode employed;
the record obtained through a contact nearer
the atrioventricular node (fig. 5A) shows
only a small, largely monophasic His deflection arising from the latter part of a large,
slow positive wave; somewhat farther from
the atrioventricular node the His deflection
arises slightly later and shows a more prominent initial positivity (fig. 5B) and at the
recording site nearest the septal end of the
common bundle of the slow wave has changed
in amplitude and configuration and the His
bundle electrogram is clearly diphasic (fig.
5C). The possible significance of the slow
waves preceding the His bundle electrogram
are discussed in a subsequent section.
Circulation Research, Volume Vlll, November I960
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Perhaps the most significant observation
made on the general appearance of the electrogram deflection recorded from the bundle of
His is that, during normal atrioventricular
transmission, this component of the electrogram always was of short duration (10 msec,
or less) and relatively simple in contour. Although polyphasic deflections and notches
were frequently recorded from other parts
of the heart, unipolar and bipolar records
from the bundle of His were of a configuration compatible with almost simultaneous excitation of parallel fibers conducting at more
or less uniform velocity. During retrograde
excitation, however, the electrogram recorded
from the His bundle at times revealed a
greater degree of asynchrony than was present during normal activation (fig. 6). This
record, obtained through electrodes implanted
in a dog with a closed chest, shows several
beats originating from some focus distal to
the common bundle followed by several driven
beats caused by stimuli applied to the right
atrium. The polyphasic complex recorded
during retrograde activity contracts sharply
with.that observed after resumption of normal
A-V transmission.
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Possible Effects of Injury
Whenever electrodes are applied directly
to the heart, there probably is some local
injury and, as a result, some distortion of
the records of electrical activity obtained
through such electrodes. Since the bundle of
His is located beneath a superficial layer of
atrial myocardium, it was thought that attachment of the electrode to endocardium over
the His bundle would not injure that structure. The records shown in figure 2C support
this impression. These tracings were obtained
through the same electrode employed for figure 2A, 20 hours after electrode implantation
and 18 hours after closure of the chest. It is
clear that there has been no measurable change
in either the interval between atrial depolarization and the h complex or between the h
complex and depolarization of the ventricular
myocardium. The configuration of the electrogram recorded from atrial muscle is changed
in figure 2C because driving stimuli were apCirculation Research, Volume VIII, November 1960
Figure 5
'Records of activity in the bimclle of His recorded
from a closed-chest dog through unipolar and
biopolar leads. (A) From above downward, the
records shoiv biopolar electrograins from the right
atrium, the bundle of His, a unipolar electrogram
from the bundle of His, a bipolar electrogram from
the left ventricle and lead II. The filter setting for
the bipolar His electrogram was 40/1,000 and
for the unipolar electrogram 0.1/500. (B) and (C)
The second, third and fourth traces a>re shown.
The unipolar recording site is moved progressively
farther from the atrioventricular node in (B) and
(C). Note the change in configuration of the slow
deflection proceeding the His electrogram. See
text for discussion.
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HOFFMAN, CRANBFIBLD, STUCKBY, BAGDONAS
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Figure 6
Records obtained through implanted electrodes 24 hours after surgical preparation. Top
trace, right wtrial appendage; second and third traces, bipolar electrograms recorded from
the bundle of Sis; fourth trace, bipolar electrogram from the epicardial surface of the
left ventricle; bottom trace, lead II. In the His electrogram, (a) represents atrial and,
(h) His btmdle activity. In all traces except the fourth, the artifact of the driving stimulus is apparent. Filter settings for the upper and lower His electrograms are 40/1,000
and 4/200, respectively. Arrow indicates the instant at which normal A-V transmission
through the His bundle is initiated; note the fusion beat in lead II. Note the change in
configuration and synchrony of activity in the bundle of His on resumption of normal
A-V transmission.
plied to the right atrium; the complex recorded from the His bundle, however, is
similar in configuration to that shown in A.
Electrical Activity of the Bundle Branches and
Peripheral Purkinje Fibers
Electrograms were recorded from the right
and left bundle branches at the point of their
appearance on the right and left septal surfaces. On the left side, the emergence of the
left branch was visualized with ease. On the
right side, the bundle branch was located with
an exploring electrode in an area posterior
to the superior papillary muscle and beneath
the septal cusp of the tricuspid valve. Electrograms were recorded both through the
exploring electrode, which was placed lightly
on the septal surface, and through multipolar electrodes sutured to the septal endocardium. Comparison of the records obtained
by both means suggested that the method
employed to attach the electrode to the endocardium did not injure the fibers of the
bundle branch under study. Records were
obtained from the free-running false tendons
through bipolar electrodes located in a groove
in curved probe. The probe was positioned
by hand so that the false tendon lay lightly
in this groove. The electrical activity of
Purkinje fibers at the junction of the false
tendons with the papillary muscles was recorded either through the exploring electrode
or through multipolar electrodes sutured to
the base of the papillary muscle. Up to
the present time records from the bundle
branches, false tendons and peripheral Purkinje fibers have been obtained only through
ventriculotomy incisions during cardiopulmonary bypass.
Figure 4 shows bipolar electrograms recorded in one experiment from the His bundle
Circulation Research, Volume V1H, November 1960
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and the proximal (septal) and distal ends
of the anterior false tendon of the left ventricle. Figure 7A, obtained in another experiment, shows records from the His bundle,
the upper part of the right bundle branch
and the papillary-Purkinje junction on the
anterior papillary muscle of the right ventricle. Electrograms from the left bundle
branch recorded during normal A-V transmission are shown in figure 7B. In each of
these tracings, the electrical activity of the
specialized conducting system is identified
with ease. In every instance, the record from
either the right or left bundle branch clearly
precedes the earliest ventricular activity;
records from the papillary-Purkinje junction,
however, at times merge with the deflections
resulting from depolarization of adjacent ventricular muscle. In all experiments, the eonfiguration of electrograms from the right
bundle branch indicated synchronous activity
of the underlying fibers of the specialized
conducting system. This was true regardless
of the exact location of the electrodes with
respect to the bundle branch. On the left
side of the heart, in contrast, if the recording electrodes were located high on the septum
the electrogram recorded from the left bundle
branch was of short duration and similar in
configuration to that shown in figure 7B. If
the recording electrodes were located somewhat lower on the septum and thus made
contact with more than one subdivision of
the left bundle, the shape of the electrogram
indicated some slight degree of asynchronj'
of depolarization in the underlying specialized
fibers. Records from the free-running false
tendons were biphasic or triphasic; close to
the junction of the Purkinje fibers with the
papillary muscles the records from the specialized tissues frequently were polyphasic.
In all instances, however, electrograms recorded from various parts of the specialized
conducting system gave no indication of any
important degree of asynchrony in the activation of the various fibers in any one bundle.
From records similar to those shown in
figures 4, 6 and 7, it is possible to determine
the speed of conduction in each part of the
Circulation Research, Volume VIII, November 1960
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Figure 7
(A) Bipolar electrograms recorded from the right
atrial appendage (a, bottom trace), the bundle of
His (h), the right bundle branch (s) and the
junction of the Purkinje fibers loith the anterior
papillary muscle (p, top trace) during cardiopidmonary bypass. (B) Bipolar electrograms recorded during cavdiopulmonary bypass from
another dog. Top trace, His bundle (h); middle
trace, left bundle branch (s); and bottom trace,
peripheral~Pur~kinje-papillaryjunction (p). See
text for discussion.
specialized ventricular conducting system and
it has been found that velocity is considerably
higher in the false tendons than in the bundle
of His.10 Also, it is possible to compare the
speed of conduction during normal and retrograde transmission. If A'entricular activity
originates late enough during diastole, it has
been found that conduction velocit}' is the
same in both directions in the His bundle and
the ventricular Purkinje system.10 The propagation of early ventricular extrasystoles is
reported elsewhere.10
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HOFFMAN, CRANBFIELD, STUCKEY, BAGDONAS
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Figure 8
Superimposed
tracings of bipolar electrograms
recorded in one animal from A, right atrial appendage; H, bundle of His; LBB, left bundle
branch; RFT, right ventricular false tendon;
LAFT, anterior false tendon of left ventricle. Also
sho%vn is the simultaneous lead II electrocardiogram. See discussion.
Transmission Through the Atrioventricular Node
Electrograms recorded from the region of
the His bundle through close bipolar leads
give a clear indication of the time of local
excitation of atrial muscle and also of the
time at which propagated activity passes
through the His bundle. Because of the great
difference in velocity of propagation in the
atrioventricular node and bundle of His,13
it is reasonable to assume that a major part
of the delay between the atrial and His bundle
components of the local electrogram results
from delay in the spread of excitation through
the atrioventricular node. If the timing of
the h complex is related to the standard lead
II electrocardiogram, it is clear that activity
in the His bundle is initiated about midway
in the P-R interval; also, if the local atrial
deflection is compared to the P wave in the
limb leads, it is apparent that the termination
of the P wave is an inappropriate reference
point for timing the beginning of A-V nodal
delay. In most experiments, atrial activity
recorded through electrodes located over the
His bundle appears rather early in the P
wave, as would be expected from the results
of earlier studies.17 This timing sequence is
the same whether atrial activity originates
from the normal sinus area (fig. 2A) or from
driving electrodes located on the right atrial
appendage (fig. 2C). Finally, it is apparent
that the extent to which the V-A delay exceeds the A-V delay is extremely variable.
This question is considered in detail elsewhere ;10 however, records of retrograde transmission obtained from hearts with essentially
normal specialized conducting systems suggest
that conduction time in the retrograde direction is not necessarily much greater than in
a normal direction. If, on the other hand,
there is some disturbance of normal A-V nodal
transmission or if retrograde transmission
reaches the node before complete recovery of
its excitability, the usual prolongation of V-A
conduction time is observed.
Electrograms recorded through unipolar
leads on the upper end of the bundle of His
occasionally show a slow wave somewhat similar to that obtained from the atrioventricular
node by Scher.4 This wave is seen only in
records obtained with a long time-constant on
the preamplifiers, and thus has been eliminated from most tracings shown in this
paper. To what extent this deflection represents nodal depolarization and to what extent it results from repolarization of atrial
muscle is difficult to decide. Additional studies
in progress are designed to record more successfully from the atrioventricular node itself.
Electrical Activity During the P-R Interval
We have not yet obtained records through
chronically implanted electrodes from numerous sites in the specialized ventricular conducting system. For this reason, it is perhaps
premature to assign any specific timing to
the depolarization of various parts of this
system. On the other hand, simultaneous
Circulation Research, Volume VIII, November 1960
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electrograms from the His bundle, the bundle
branches and the peripheral Purkinje fibers
recorded during total cardiopulmonary bypass
probably do give a reasonable indication of
the sequence of electrical activity in the specialized conducting system in relation to the
standard electrocardiogram recorded under
the same conditions. One such set of records
is reproduced in figure 8 and emphasizes
several points. First, as mentioned before,
the bundle of His is activated early in the
P-R interval. Since conduction through the
atrioventricular node is known to be slow13
the conduction time between atrial muscle
near the sinoatrial node and the atrioventricular node nmst be quite short. Second,
although the distance from the His bundle
to the emergence of the bundle branches on
the interventricular septum is short in comparison to the distance from the bundle
branches to the periphery, a major part of
the delay between activity in the His bundle
and depolarization of ventricular muscle is
due to conduction in the His bundle and
bundle branches. This finding would be expected from the observation that conduction
velocity in the free-running Purkinje fibers
is considerably higher than in the bundle of
His. 8 ' 10 Finally, it is apparent that, there
is electrical activity somewhere in the conducting system during the entire P-R interval
even though that activity is not detected in
the electrocardiogram.
Discussion
The electrical activity of the specialized
conducting system was first recorded from
excised, perfused dog hearts in 1930 by
Maeno.18 Subsequently Burchell et al.,5 Scher7
and others recorded from either the bundle
branches or subendocardial Purkinje fiber
network through needle electrodes plunged
into the myocardium. More recently a number of investigators have employed needle
electrodes inserted into various parts of the
heart to record from the atrioventricular
node,4 the bundle of His 8 ' 19 and the specialized ventricular conducting system. As a
result of these and other studies attempts
have been made to characterize the electroCirculation Research, Volume VIII, November I960
1209
gram deflections typical of electrical activity
in each part of the specialized conducting system and to determine the electrophysiologic
properties of the specialized tissues. Also, it
has been possible to indicate the sequence of
activation of the specialized conducting system with respect to the standard electrocardiogram.
The results reported in this paper have
been obtained by a teehnic somewhat different
from that employed by others. It is thought
that this teehnic offers several advantages. In
the first place, by use of total cardiopulmonary bypass, direct observation, and an exploring electrode it is possible to locate any
part of the specialized conducting system with
certainty. Also, comparison of records obtained through the exploring electrode and
through the electrodes attached to the endocardium permits evaluation of local injury
resulting from the method of attachment.
Records obtained from more than 50 dogs
during the past 2 years suggest that surface
electrodes can be used for long periods of
time without producing appreciable injury
to the tissues under consideration. In contrast, studies of single cardiac fibers made
with intracelhilar mieroelectrodes have clearly
demonstrated that an electrode tip of as
little as 2 microns in diameter will cause an
important degree of injury to cardiac muscle.
Records similar to those shown in figure 2,
which demonstrate the constancy of the P-R
interval and timing of the His electrogram
after recovery from cardiopulmonary bypass,
support the belief that neither the surgical
procedure itself nor the presence of the electrode causes an appreciable distortion of the
normal sequence of activation.
Another advantage of the methods described is the possibility of obtaining simultaneous records from a number of different
parts of specialized conducting system. Even
when electrical activity is recorded simultaneously from the His bundle and a peripheral Purkinje fiber, estimates of conduction
velocity give a wide range of variation (2.6
to 4.4 M./sec.).11' This variation results from
local differences in conduction velocity in the
His bundle, bundle branches, free-running
HOFFMAN, CRANEFIELD, STUCKEY, BAGDONAS
1210
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Purkinje fibers and subendocardial Purkinje
network;10 measurements of conduction velocity require records of local activity at either
end of each part of the specialized conducting
system. Similarly, since it has beeu demonstrated that the transmembrane action potentials of the atrioventricular node, the His
bundle, the false tendons and the subendocardial Purkinje fibers differ with respect to
magnitude, voltage-time course and duration,
simultaneous records from several of these
tissues are essential in a stud}' of the electrophysiology of the intact specialized conducting system.
Identification of various unusual waveforms observed in records from parts of the
specialized conducting system is greatly facilitated if simultaneous electrograms indicate
the time of activation of other parts of the
His bundle or bundle branches. This is true
particularly in the ease of records from the
region of the atrioventricular node. The low
rate of depolarization of nodal fibers and the
extremely low conduction velocity in the atrial
end of the node13 strongly suggest that records of electrical activity made with surface
electrodes will fail to show rapid transients.
On the other hand, since activity in the bundle
of His is initiated early in the P-R interval
and often shortly after the end of the P wave,
it is unlikely that slow deflections which have
their origin late in the P-R interval and
which last well into the QRS complex are
indeed nodal potentials.19 In particular, if
records from the nodal region are obtained
through needle electrodes, local injury must
be considered as a possible cause of slowly
rising monophasic deflections of long duration. For positive identification of surface
records of nodal activity other criteria such
as the effects of rate or of vagal stimulation
are essential.
Summary
Electrical activity of the specialized conducting system (His bundle, bundle branches,
false tendons and peripheral Purkinje fibers)
of canine hearts has been recorded in situ
through electrodes attached to the endocardium during total cardiopulmonary bypass.
Simultaneous records from multiple sites have
been correlated with electrocardiograms to indicate the sequence of activation of the specialized conducting system during normal and
retrograde activation and during vagal stimulation. The results obtained indicate that
the method employed has several advantages
among which are an absence of injury at the
recording site and an applicability to chronic
studies.
Summario in Interlingua
Le activitate electric del specialisate systema de
conduction del corde canin—fasce de His, brancas,
tendines false, fibras peripheric de Purkinje—cssova
rogistrate in sito per electrodos attachate al endocardio durante circumconduction cardiopulmonar
total. Le registrationes in multiple sitos, obtenito
simultanccmente, esseva correlationate con le electrocardiogramma pro indicar le sequentia del activation
in le specialisate systema de conduction durante le
activation normal o retrograde e durante stimulation
vagal. Le resultatos obtenite indica quo le metliodo
empleate lia pluro avantages, incluse le facto que
nulle trauma, occurre al sito del registration e que
illo es applicable a studios chronic.
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Electrical Activity During the P-R Interval
BRIAN F. HOFFMAN, PAUL F. CRANEFIELD, JACKSON H. STUCKEY, ALBIN A.
BAGDONAS and Juan Piera
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Circ Res. 1960;8:1200-1211
doi: 10.1161/01.RES.8.6.1200
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