Download Cardiac Responses during Stimulation of the Dorsal Motor Nucleus

606
Cardiac Responses during Stimulation of the
Dorsal Motor Nucleus and Nucleus
Ambiguus in the Cat
G. STEVEN GEIS AND ROBERT D. WURSTER
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
SUMMARY Studies were performed to determine the role of the dorsal motor nucleus (DMN) and
nucleus ambiguus (NA) in cardiac control in cats. Heart rate (HR), mean arterial blood pressure
(MABP), ventricular contractility, left ventricular end-diastolic pressure (LVEDP), and right ventricular end-diastolic pressure (RVEDP) were monitored in anesthetized, paralyzed and /J-blocked animals.
The rate of rise of the rising limb of the left ventricular pressure curve (dP/dt) and the output of a
strain gauge sutured to the right ventricle (SGF) served as indices of ventricular contractility. Pacing
electrodes were inserted into the ventricular myocardium and stimulating electrodes were stereotaxically placed in the DMN and NA. The nuclei were stimulated with and without cardiac pacing, before
and after ipsilateral vagotomy. DMN stimulation produced decreases in MABP, dP/dt, and SGF, no HR
change, and increases in LVEDP and RVEDP. HR and MABP decreased and dP/dt, SGF, LVEDP, and
RVEDP increased with NA stimulation. The responses to NA stimulation were abolished by ventricular
pacing. The responses to stimulating either nucleus were abolished by ipsilateral vagotomy. The
decreases in dP/dt and SGF with DMN activation were not secondary to preload decreases since
LVEDP and RVEDP increased during stimulation. However, since the dP/dt and SGF changes during
NA stimulation were abolished by cardiac pacing, the responses were secondary to bradycardia. The
data suggest cardiac vagal preganglionic somata are organized according to physiological function.
Cell bodies of the DMN control ventricular contractility whereas NA somata are involved in HR control.
Circ Res 46: 606-611, 1980
DIFFERENTIAL cardiac control refers to the anatomical organization of neural structures for controlling specific cardiac functions. Central and peripheral sympathetic and peripheral parasympathetic structures demonstrate this phenomenon.
Activation of the hypothalamus (Peiss, 1962),
vasomotor center (Chai and Wang, 1962), stellate
ganglion, or ventral roots (Randall et al., 1957;
Randall and Rohse, 1956) on the right side produces
increases in heart rate, whereas stimulation of corresponding left structures has minor chronotropic
effects. Regional cardiac inotropic responses result
from specific cardiac nerve stimulation (Randall
and Armour, 1977). Right vagal activation produces
negative chronotropic responses while left vagal
stimulation affects AV nodal conduction (Cohn and
Lewis, 1913; Hamlin and Smith, 1968). Resting
heart rate decreases after a lesion is made in the
right descending pressor pathway but is not affected
by cutting the left pathway (Wurster, 1977).
Cardiac vagal preganglionic somata may be organized for differential cardiac control. The cell
bodies are located in three distinct medullary regions: the dorsal motor nucleus of the vagus
From the Department of Physiology, Loyola University of Chicago,
Stritch School of Medicine, Maywood, Illinois.
Supported by National Institutes of Health Grant HL08682.
Address for reprints: Robert D. Wurster, Ph.D., Department of Physiology, Loyola University of Chicago, Stritch School of Medicine, 2160
South First Avenue, Maywood, Illinois 60153.
Received May 17, 1979; accepted for publication January 15, 1980.
(DMN), the nucleus ambiguus (NA), and an intermediate zone (IZ) between the DMN and NA (Geis
and Wurster, 1978). Certain morphological characteristics of the three cell body populations differ.
Malone (1913) suggested that morphological variations of neurons reflect differences in neuronal function.
The present investigation was designed to determine the functional significance of the location of
cell bodies in the DMN and NA. The nuclei were
stimulated electrically while cardiac parameters
were monitored. The IZ was excluded from the
study due to the paucity and scattered distribution
of cell bodies in this region (Geis and Wurster,
1978).
Methods
Twenty cats (2.3-4.0 kg) were p^eanesthetized
with chloroform followed by general anesthesia
with a-chloralose (40-45 mg/kg, iv). Femoral arterial and venous catheters were inserted. A tracheotomy was performed and the aortic depressor and
carotid sinus nerves were sectioned bilaterally to
denervate the baroreceptors. Each cat was then
secured in a Horsley-Clarke stereotaxic device, paralyzed with decamethonium bromide (Cio) (0.03
mg/kg, iv), and artificially ventilated. /^-Blockade '
was induced with propranolol (0.1 mg/kg, iv). An
occipital craniotomy was performed. Blood pressure
and heart rate were monitored with a Statham
P23Db pressure transducer and a cardiotachome-
RESPONSES TO STIMULATING THE DMN AND NA/Geis and Wurster
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
ter, respectively. End-expiratory %CO2 was monitored and maintained at 4.0-4.5% (Beckman LB1).
Rectal temperature was maintained at 37.0 ± 0.2°C
by a heating pad.
The right second through fifth ribs were then
removed. The pericardium was incised and stainless
steel pacing electrodes were inserted into the right
ventricular myocardium. Stimuli for pacing (4.0 V,
1.0 msec) were delivered from a stimulus isolation
unit (Grass model SI 4678) connected to a stimulator (Grass model S48). Pacing rates were adjusted
to the spontaneous heart rate demonstrated after
^-blockade.
Strain gauge output and dP/dt were used as
indices of ventricular contractility. Catheters were
inserted into the left and right ventricular chambers
by cardiac puncture. Ventricular pressures were
monitored by P23Db pressure transducers. The
right intraventricular pressure was recorded by
means of an oscillograph (Grass model 7) while the
left intraventricular pressure was amplified by a DC
carrier amplifier (Honeywell model 130-2C) and
simultaneously displayed on an oscilloscope (Tektronics model 565) and the oscillograph. We measured dP/dt as the rate of rise of the rising limb of
the left intraventricular pressure curve. The ventricular system connected to the oscilloscope had a
natural frequency of 100 Hz and a damping factor
of 0.4. Oscillograph preamplifier gains were adjusted
for accurate determination of end-diastolic pressures.
A Walton-Brodie strain gauge arch was sutured
to the right ventricle. Strain gauge output was
displayed on the oscillograph. Outputs were calibrated in grams. The values were not interpreted
as absolute measures of cardiac force. Strain gauge
output will be referred to as strain gauge force
(SGF) in the remaining discussion.
After surgical instrumentation, the left dorsal
motor nucleus (DMN) and nucleus ambiguus (NA)
were stimulated in 10 cats and the right nuclei were
activated in another 10 animals with bipolar electrodes (David Kopf, SNE-100; 100 /mi, exposed tip
length; 100 /mi, electrode tip diameter). The electrode tip was stereotaxically (Snider and Niemer,
1961) inserted into each nucleus at three different
medullary planes including the obex level, 1.5 mm
rostral to the obex and 1.5 mm caudal to the obex.
In 10 cats, sites 0.5 mm medial and lateral to the
DMN and NA also were stimulated in each of the
three medullary planes. A constant current (Grass
model 1A), isolated (Grass model SIU 5) stimulus
(Grass S44) of 20 seconds duration (0.1-0.15 mA,
1.0 msec, 50 Hz) was delivered at each site. Each
site was randomly stimulated three times with cardiac pacing and three times without cardiac pacing.
The ipsilateral vagus then was sectioned and each
site was stimulated again three times with and
without cardiac pacing.
Changes in afterload can produce secondary,
non-neurally mediated alterations in heart rate and
607
contractility (Falsetti et al., 1971; Ross and Braunwald, 1964). Therefore, the changes in cardiac function during brainstem stimulations may be passive
responses to neuraUy induced blood pressure
changes. To exclude this possibility, bilateral vagotomies were performed in 10 cats and the responses to injections of phenylephrine (30 jug/kg,
iv) and histamine (2.5 /xg/kg, iv) were recorded.
Each animal was perfused with 0.9% saline followed by 10% formalin fixative. The brainstem was
removed and stored overnight in a solution of 10%
formalin and sodium nitroferricyanide. Ten-micron
serial sections were cut and stained with cresyl
violet. The stimulation sites were identified by the
blue stain resulting from the reaction of iron deposits from the electrode tip with sodium nitroferricyanide.
Data were organized into groups corresponding
to the nucleus stimulated. Thus, NA and DMN
groups were formed. For each group, control parameters and the responses to stimulating the left and
right sides were compared by the unpaired £-test.
Analysis of variance was used to compare control
parameters and the responses to stimulating the
three medullary planes for each group. For each
group, comparisons were made between prevagotomy controls and responses, pre- and postvagotomy controls, pre- and postvagotomy responses,
and postvagotomy controls and responses by paired
*-test.
Parameters during pacing were compared with
corresponding parameters with and without pacing
using the paired t-test for each group. Pre- and
postvagotomy controls and pre- and postvagotomy
responses were compared in this manner. Control
and response parameters observed during pacing
were then compared by paired t-test. The test was
made between prevagotomy controls and responses
and postvagotomy controls and responses. Cardiovascular responses to each drug were compared
with controls by paired t-test. Variance (F) and
probability values less than 0.05 were considered
statistically significant (Gilbert, 1976).
Results
For each nucleus the data corresponding to the
two sides of the brain stem were pooled, since
control parameters and the responses to stimulating
the left and right sides were not significantly different (P > 0.05). Since analysis of variance indicated
no significant differences (F > 0.05) in control parameters and the responses to stimulating each
nucleus in the different medullary planes, the data
associated with the three planes were pooled.
DMN stimulation produced significant (P <
0.05) decreases in dP/dt, SGF, and mean arterial
blood pressure (MABP) (Figs. 1 and 2). The stimulus did not affect heart rate (HR) (P > 0.05) but
produced significant increases in left ventricular
end-diastolic pressure (LVEDP) and right ventricular end-diastolic pressure (RVEDP) (P < 0.05).
608
CIRCULATION RESEARCH
AA/^AAAAAAAAAAAAA
sO\AMMA/WlAMAM /vwvwwwwww
STIMULATION
W w
"
w ; w
VOL.
46, No. 5,
MAY
1980
™^^
VWIAAAAAMAAAAA
RECOVERY-CONTROL
Wffiflff
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
FIGURE 1 Responses of a single cat to DMN stimulation are shown before (A) and after (B) vagotomy. Tracings of each panel are from top to bottom: blood pressure
(BP), left ventricular pressure (LVP), right ventricular
pressure (RVP), and strain gauge force (SGF). The LVP
and R VP are amplified for observing end-diastolic pressures. The "stimulation" tracings shown are from the
last several seconds of the stimulus. Time marker indicates 1-second intervals. Prestimulation controls are
shown on the left and recovery controls on the right.
Arrows indicate end-diastolic pressures.
Ipsilateral vagotomy did not affect control parameters ( P > 0.05) but abolished the responses to
DMN stimulation (P > 0.05). Neither control parameters nor the responses to DMN stimulation
were affected by cardiac pacing (P > 0.05).
Intact cats demonstrated significant decreases
( P < 0.05) in MABP and HR but significant increases ( P < 0.05) in dP/dt, SGF, LVEDP, and
RVEDP during NA stimulation (Figs. 3 and 4).
Cardiac pacing did not affect control parameters
(P > 0.05) but abolished the responses to stimula-
G7/W
i
RVP
mmHg
FIGURE 3 Responses of a single cat to NA stimulation
are shown with (A) and without (B) cardiac pacing.
Tracings ofeachpanel are from top to bottom: BP, LVP,
RVP, and SGF. Time marker indicates 1-second intervals. Downward deflection of the marker indicates stimulus duration. The stimulation tracings shown are from
the last several seconds of the stimulus. Arrows indicate
end-diastolic pressures.
tion (P > 0.05). Ipsilateral vagotomy had no effect
on control parameters ( P > 0.05). NA stimulation
produced no significant changes (P > 0.05) in parameters after vagotomy. Stimulation of sites 1.0
mm medial and lateral to the DMN or NA had no
affect on cardiac function.
The electrode tracts in each of the three medullary planes penetrated are illustrated in Figure 5 for
• N=10
N = 2O
•
11 • L
i
I
•
Control I
Stimulation
1
I
H
N = 20
Control I
N = 10
Stimulation^!
I
X
JL
I
INTACT
VAGOTOMY
Inl
INTACT
VAGOTOMY
2 Average cardiovascular responses to DMN
stimulation without cardiac pacing before and after
vagotomy. Filled circles indicate significant difference
from control. Brackets indicate SE.
FIGURE
INTACT
INTACT
PACED
VAGOTOMY
INTACT
INTACT
PACED
VAGOTOMY
4 Average cardiovascular responses to NA
stimulation are shown for intact cats without cardiac
pacing, intact cats with pacing, and after vagotomy
without pacing. Filled circle indicates significant difference from control. Brackets indicate SE.
FIGURE
RESPONSES TO STIMULATING THE DMN AND NA/Geis and Wurster
609
Discussion
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
FIGURE 5 The three planes of electrode penetration
from a representative experiment (bottom = 1.5 mm
caudal to obex, middle = obex level, top = 1.5 mm rostral
to obex). Filled circles indicate sites of the electrode tip
at which changes in cardiac function were produced.
Unfilled circles indicate sites of the electrode tip at
which no changes in cardiac function were elicited. NA
= nucleus ambiguus, LRN = lateral reticular nucleus,
ION = inferior olivary nucleus, N XII = hypoglossal
nucleus, DMN = dorsal motor nucleus, NS' = nucleus
solitarius.
a representative experiment. Since cresyl violet
stains cell bodies, various nuclei were apparent.
Electrode tips were located in the DMN or NA
when changes in cardiac function were elicited.
In bilaterally vagotomized cats, phenylephrine
and histamine produced significant increases (P <
0.05) and decreases (P < 0.05) in MABP, respectively. The other cardiovascular parameters did not
change significantly (P > 0.05) after administration
of either drug.
Cardiac vagal preganglionic somata in the DMN
are capable of controlling ventricular contractility
while NA somata can affect heart rate. Stimulation
of the DMN produced decreases in the indices of
ventricular contractility (dP/dt and SGF) but no
HR changes (Figs. 1 and 2). NA stimulation resulted
in HR decreases (Figs. 3 and 4). The responses to
stimulating either nucleus were abolished by ipsilateral vagotomy.
Hamlin and Smith (1968) and Cohn and Lewis
(1913) reported that right vagal stimulation inhibits
the SA node while left vagal stimulation affects AV
nodal conduction. In the present study the cardiac
responses to stimulating corresponding brainstem
sites on the left and right sides were not significantly
different. The differences between our results and
the reports by Hamlin and Smith and by Cohn and
Lewis are not necessarily contradictory. Cardiac
responses to vagal stimulation depend on the level
at which the nerve is activated. Randall and Armour (1977) reported that the branches to the SA
node on the right vagus diverge from the main
trunk at sites more caudal than corresponding
branches of the left vagus. Thus, stimulating the
right vagus may affect SA nodal firing while activating the left vagus at a corresponding level may
affect AV nodal conduction, since the major
branches to the SA node are not within the main
trunk at that level. The sites of our stimulations
may have been at a level where the composition of
somata with axons traveling to the SA node were
similar on the left and right sides. Furthermore,
Hamlin and Cohn and Lewis used dogs for their
studies, whereas cats were studied in the present
investigation. Thus, species variations may be responsible for the different results.
Contractility is an intrinsic myocardial property
(Falsetti et al., 1971; Ross and Braunwald, 1964).
SGF and dP/dt are measures of contractile force
which depend on preload, afterload, and contractility. The changes in dP/dt and SGF with DMN
stimulation were not secondary responses to
changes in preload and afterload. LVEDP and
RVEDP increased during stimulation (Figs. 1 and
2). Decreases in contractile force cannot result from
preload increases unless the heart functions on the
descending limb of the Frank-Starling curve (Ross
and Braunwald, 1964; Sarnoff and Mitchell, 1962).
Aortic pressure changes with DMN stimulation did
not produce the changes in dP/dt and SGF. Bilaterally vagotomized cats demonstrated no changes
(P > 0.05) in the indices of ventricular contractility
with drug-induced blood pressure alterations.
Contractile force changes produced by NA stimulation were secondary to HR decreases. Bradycardia increases diastolic filling time, end-diastolic
pressure and, ultimately, contractile force (Hamlin,
1977). LVEDP and RVEDP increased during NA
stimulation (Figs. 3 and 4). Cardiac pacing abolished all responses to NA stimulation. Therefore,
610
CIRCULATION RESEARCH
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
the changes in dP/dt, SGF, LVEDP, and RVEDP
were mechanical alterations produced by bradycardia.
Anatomical studies suggest parasympathetic preganglionic somata develop a viscerotopic organization. Vagal branches to different viscera were sectioned (Mitchell and Warwick, 1955) and the locations of the resulting chromatolytic neurons were
compared. Cell bodies innervating a given organ
were arranged in relatively distinct groups. The
studies are limited since the entire brain stems were
not thoroughly examined. However, the possibility
of viscerotopic organization may be significant to
the present study.
Somata of the DMN and NA may demonstrate
cardiotopic organization. DMN cell bodies at the
obex level may control ventricular contractility
while more rostral somata may affect HR. NA
somata at the obex may regulate HR while somata
of the rostral NA may affect ventricular contractility. The responses to stimulating each nucleus at
the obex level, 1.5 mm rostral to the obex and 1.5
mm caudal to the obex were not significantly different (F > 0.05). Histological evidence indicated
that cardiac vagal preganglionic somata are located
in these medullary planes (Geis and Wurster, 1978).
Thus, the data suggest the responses illustrated in
Figures 2 and 4 characterize myocardial control by
all somata of the DMN and NA, respectively.
However, the stimulating electrodes may have
been activating axons or interneurons of a cardiac
vagal reflex. This is possibile for four reasons. First,
histological data indicate the electrode tips were
located in the DMN or NA (Fig. 5). Second, the
stimulus currents were within the accepted limits
for activating central neural structures with minimal current spread (Wilkus and Peiss, 1963). Third,
stimulating 0.5 mm medial and lateral to the DMN
and NA had no effect on cardiac parameters.
Fourth, all responses were abolished by vagotomy
ipsilateral to the stimulating electrode.
Medullary reflex pathways affecting the cardiac
vagus are bilateral. The bradycardia in response to
unilateral carotid sinus nerve stimulation is diminished by unilateral vagotomy and completely abolished by bilateral vagotomy (Quest and Gebber,
1972). Carotid sinus chemoreceptor pathways project bilaterally as do aortic baroreceptor and aortic
chemoreceptor pathways (Kunze, 1972). The nucleus tractus solitarius lies immediately dorsolateral
to the DMN and contains the second-order neurons
of the baroreceptor and chemoreceptor reflexes
(Code et al., 1936; Cottle, 1964). Calaresu and
Pearce (1965) produced bradycardia by unilateral
electrical stimulation of the nucleus tractus solitarius. The responses were abolished only after bilateral vagotomy. Thus, if the stimuli in the present
study were activating known afferent autonomic
pathways, the responses would be abolished only
after bilateral vagotomy. However, ipsilateral vagotomy abolished the responses to DMN and NA
VOL.
46, No. 5, MAY 1980
stimulation in our studies. Therefore, electrical currents were activating vagal preganglionic neurons
and not afferent component of cardiac vagal reflexes.
The extent of vagal innervation of the ventricles
is controversial. Anatomical data suggest minimal
or no innervation by parasympathetic preganglionic
axons (Cullis and Tribe, 1913; Nonidez, 1939). However, physiological studies have supported parasympathetic ventricular innervation. DeGeest et al.
(1965) stimulated the vagi while monitoring ventricular contractility. Stimulation of either vagus
produced decreased left ventricular systolic pressure when HR, coronary perfusion pressure, and
end-diastolic volume were kept constant. The reduction ranged from 7 to 34%, depending on the
stimulation frequency, and the responses were abolished by atropine. Daggett et al. (1967) also demonstrated a negative inotropic effect on the left
ventricle by vagal stimulation in a right heart bypass preparation in which aortic pressure, cardiac
output, and heart rate were held constant. Negative
inotropic effects of vagal stimulation on ventricular
myocardium in the dog have been confirmed by
several groups (Harmon and Reeves, 1968; Levy et
al., 1966). The results of the present investigation
confirm the capacity of the cardiac vagus to regulate
ventricular contractility.
The data also provide physiological evidence confirming the anatomical location of cardiac vagal
preganglionic somata in the DMN and NA in the
cat (Geis and Wurster, 1978). However, the results
conflict with reports by Calaresu and Pearce (1965)
and Gunn et al. (1968). Cardiac responses to stimulation of a variety of brain stem sites were monitored. Short latency bradycardia was produced by
NA activation. The authors concluded that cardiac
vagal preganglionic somata are located in the NA.
However, changes in HR alone do not necessarily
reflect cardiac innervation. Parasympathetic nerve
fibers also control cardiac inotropic and dromotropic activity (Randall and Armour, 1977). As
shown by the present study, cardiac vagal preganglionic somata are organized according to physiological function. Since Calaresu and Pearce and
Gunn et al. recorded only HR, the effects of DMN
stimulation were not apparent.
Randall and Armour (1977) suggested that the
nervous system may have the capacity to differentially regulate cardiac function. Stimulation of specific peripheral nerves produced specific cardiac
responses. These data suggested that under one set
of circumstances the nervous system may regulate
cardiac output by HR control whereas under another set of circumstances the nervous system
might regulate cardiac output by means of ventricular contractility. The anatomic substrate for differential cardiac control at the central level has
been described (Geis and Wurster, 1978). The present study provides physiological evidence in confirmation of the anatomical report.
RESPONSES TO STIMULATING THE DMN AND NA/Geis and Wurster
Acknowledgments
We extend thanks to Mira Milosavljevic for preparing the
histology and to Vivian Rogala for typing the manuscript.
References
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
Calaresu FR, Pearce JW (1965) Effects on heart rate of electrical
stimulation of medullary vagal structures in the cat. J Physiol
(Lond) 176: 241-251
Chai CY, Wang SC (1962) Localization of central cardiovascular
control mechanisms in lower brain stem of the cat. Am J
Physiol 202: 25-30
Code CR, Dingle WT, Morrhouse VHK (1936) The cardiovascular carotid sinus reflex. Am J Physiol 115: 249-260
Cohn AE, Lewis T (1913) The predominant influence of the left
vagus upon conduction between the auricles and ventricles in
the dog. J Exp Med 18: 739-747
Cottle MK (1964) Degeneration studies of primary afferents in
IXth and Xth cranial nerves in the cat. J Comp Neurol 122:
329-346
Cullis W, Tribe EM (1913) Distribution of nerves in the heart.
J Physiol (Lond) 46: 141-150
Daggett WM, Nugent GC, Carr PW, Powers PC, Harada Y
(1967) Influence of vagal stimulation on ventricular contractility, O2 consumption and coronary flow. Am J Physiol 212:
8-18
DeGeest H, Levy MN, Zieske H, Lipman RI (1965) Depression
of ventricular contractility by stimulation of the vagus nerves.
Circ Res 17: 222-235
Falsetti HL, Mates RE, Greene DG, Bunnell IL (1971) Vm« as
an index of contractile state in man. Circulation 43: 467-479
Geis GS, Wurster RD (1978) Localization of cardiac vagal preganglionic soma (abstr). Neurosci Abstr4: 20
Gilbert N (1976) Statistics. Philadelphia, W. B. Saunders Company
Gunn CG, Sevelius MJ, Puigarri MJ, Myers FK (1968) Vagal
cardiomotor mechanisms in the hindbrain of the dog and cat.
Am J Physiol 214: 258-262
Hamlin RL (1977) Myocardial contractility. Adv Vet Sci Comp
Med 21: 19-38
Hamlin RL, Smith CR (1968) Effect of vagal stimulation of S-A
and A-V nodes. Am J Physiol 215: 560-568
Harmon MA, Reeves TJ (1968) Effect of efferent vagal stimu-
611
lation on atrial and ventricular function. Am J Physiol 215:
1210-1217
Kunze DL (1972) Reflex discharge patterns of cardiac vagal
efferent fibres. J Physiol (Lond) 222: 1-15
Levy MN, Ng M, Martin P, Zieske H (1966) Sympathetic and
parasympathetic interaction upon the left ventricle of the dog.
Circ Res 19: 5-10
Malone EF (1913) The nucleus cardiacus nervi vagi and the
three distinct types of nerve cells which innervate the three
different types of muscle. Am J Anat 15: 121-127
Mitchell GAG, Warwick R (1955) The dorsal vagal nucleus. Acta
Anat 25: 371-395
Nonidez JF (1939) Studies on the innervation of the heart. Am
J Anat 65: 361-413
Peiss CN (1962) Sympathetic control of the heart. (Central
nervous mechanisms). In Cardiovascular Functions, edited by
AA Luisada. New York, Mc-Graw Hill, pp 314-323
Quest JA, Gebber GL (1972) Modulation of baroreceptor reflexes
by somatic afferent nerve stimulation. Am J Physiol 222:
1251-1259
Randall WC, Armour JA (1977) Gross and microscopic anatomy
of the cardiac innervation. In Neural Regulation of the Heart,
edited by WC Randall. New York, Oxford University Press,
pp 13-41
Randall WC, Rohse WG (1956) The augmentor action of sympathetic cardiac nerves. Circ Res 4: 470-475
Randall WC, McNally H, Cowan J, Caliguiri L, Rohse WB (1957)
Functional analysis of cardioaugmentor and cardioaccelerator
pathways in the dog. Am J Physiol 19: 213-217
Ross J Jr, Braunwald E (1964) Studies on Starling's law of the
heart. IX. The effects of impeding venous return on performance of the normal and failing human left ventricle. Circulation
30: 719-727
Sarnoff SJ, Mitchell JH (1962) The control of the function of
the heart, section 2, Circulation, vol 1, edited by WF Hamilton,
P Dow. Washington, D.C., American Physiological Society, pp
489-532
Snider RS, Niemer WT (1961) A Stereotaxic Atlas of the Cat
Brain. Chicago, University of Chicago Press
Wilkus RJ, Peiss CN (1963) Stimulation parameters for cardiovascular responses from medulla and hypothalamus. Am J
Physiol 205: 601-605
Wurster RD (1977) Spinal sympathetic control of the heart. In
Neural Regulation of the Heart, edited by WC Randall. New
York, Oxford University Press, pp 211-246
Cardiac responses during stimulation of the dorsal motor nucleus and nucleus ambiguus in
the cat.
G S Geis and R D Wurster
Downloaded from http://circres.ahajournals.org/ by guest on April 28, 2017
Circ Res. 1980;46:606-611
doi: 10.1161/01.RES.46.5.606
Circulation Research is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1980 American Heart Association, Inc. All rights reserved.
Print ISSN: 0009-7330. Online ISSN: 1524-4571
The online version of this article, along with updated information and services, is located on the
World Wide Web at:
http://circres.ahajournals.org/content/46/5/606.citation
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in
Circulation Research can be obtained via RightsLink, a service of the Copyright Clearance Center, not the
Editorial Office. Once the online version of the published article for which permission is being requested is
located, click Request Permissions in the middle column of the Web page under Services. Further information
about this process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Circulation Research is online at:
http://circres.ahajournals.org//subscriptions/