JOURNAL
OF
Vol. 231, No. 5, November
AMERICAN
PHYSIOLOGY
1976.
Printed
in U.S.A.
Basis for synchronization
phrenic nerve discharges
of sympathetic
SUSAN M. BARMAN
AND GERARD
L. GEBBER
Department
of Pharmacology, Michigan State University,
and
East Lansing, Michigan
48824
1601
Downloaded from http://ajplegacy.physiology.org/ by 10.220.33.3 on April 3, 2017
Gootman (7) also reported an instance in which this
pattern of temporal relations was reversed. Preiss et al.
(18) reported that the pattern of respiratory modulation
of the spontaneous discharges of single-preganglionic
sympathetic neurons usually was phase locked rather
than phase spanning. Unitary discharge most often was
augmented during inspiration and reduced during expiration, although three units also were found that fired
primarily during expiration. Koizumi et al. (15) also
described the pattern of respiratory modulation of SND
as phase locked rather than phase spanning.
Variations in the pattern of temporal relations between sympathetic and phrenic nerve discharges make
it difficult to accept the notion that “respiratory” periodicity is extrinsically
imposed on central sympathetic
networks by any one particular component of the respiratory oscillator. The present report entertained the
alternative possibility that the slow rhythms within
sympathetic and phrenic nerve discharges were generated by independent oscillators which normally are entrained to each other. Consideration of this hypothesis
slow sympathetic
oscillator; respiratory
oscillator; phase relawas warranted in view of certain experimental results
tions
reported, although not necessarily stressed, by others.
First, Figure 11 of Cohen and Gootman’s (7) paper is
particularly intriguing. As shown by computer summaTHE NATURALLY
OCCURRING
DISCHARGES
of pre- and tion, hypocapnia eliminated the component of SND time
postganglionic sympathetic nerve bundles exhibit a locked to the cycle of phrenic nerve activity. Nevertheless, oscillographic traces of SND during hypocapnia
slow rhythmic component with a period of the respiratory cycle (1, 2, 7, 12, 15, 17, 19). In addition to the showed slow oscillations that appeared similar in form
sympathoinhibitory
effects associated with activation of to those which were locked in a 1:l relation to the
phrenic nerve discharge cycle in the normocapnic state.
vagal lung inflation afferents (2, 8, 17), it is generally
agreed that some form of direct coupling between the Thus, a reduction in arterial Pco2 appeared to unlock
brainstem respiratory oscillator and the central sympa- the phase relations between sympathetic and phrenic
nerve discharge rather than to eliminate the slow
thetic networks is responsible for the slow sympathetic
rhythm (7, 12, 15, 18). However, the nature of the cen- rhythm within SND. Second, Koepchen and Thurau
(14) observed that blood pressure and respiratory
tral interaction remains in question. The present invesrhythms were not always synchronized. Oscillations of
tigation dealt exclusively with this problem.
Contradictory reports exist concerning the pattern of blood pressure in the dog most often occurred at the
same frequency as the respiration, but sometimes octemporal relations between sympathetic and phrenic
nerve discharges in vagotomized cats. Cohen and Goot- curred at half or twice the respiratory rate. The results
man (7) and Gootman and Cohen (12) described the presented in the current study support the view that the
temporal relations between computer-summed splanch- slow rhythms within sympathetic and phrenic nerve
nit sympathetic and phrenic nerve discharges as phase discharges arise from independent oscillators.
spanning. Sympathetic nervous discharge (SND) usu- METHODS
ally increased during late expiration and early inspiration, became maximal in midinspiration, and then deTwenty-eight cats weighing between 2.0 and 3.5 kg
clined to a minimum in early expiration. Cohen and were anesthetized by the intraperitoneal injection of a
BARMAN, SUSAN ha., AND GERARD L. GEBBER. Basis for
synchronization
of sympathetic and phrenic nerve discharges.
Am. J. Physiol. 231(5): 1601-1607.
1976. -The basis for the
relationship
between the discharges in the external carotid
postganglionic
sympathetic
and phrenic nerves was studied in
anesthetized
cats that were vagotomized,
paralyzed, and artificially ventilated.
It is generally
assumed that the slow
rhythmic component of sympathetic
nerve discharge (with the
period of the cycle of phrenic nerve activity) is extrinsically
imposed on central sympathetic
networks by elements of the
brainstem respiratory
oscillator. However, a number of observations made in the present study contradict this view. First,
changes in respiratory
rate were accompanied
by dramatic
shifts in the phase relations between sympathetic
and phrenic
nerve discharge. Second, slow oscillations
of sympathetic
and
phrenic nerve discharge were not always locked in a 1:l relation. Third, the slow sympathetic
rhythm persisted when respiratory
rhythmicity
disappeared
during
hyperventilation.
These results suggest that the slow periodic components
of
sympathetic
and phrenic nerve activity are generated by independent oscillators that normally are entrained to each other.
1602
S. M.
200
r
AND
G.
L. GEBBER
Brainstem
stimuZation.
The ventral aspect of the pons
was exposed after removal of portions of the occipital
and basisphenoid
bones.. The dura mater was opened
without
damage to the vertebral
and basilar arteries.
Pulses from a Grass S8 stimulator
were applied to selected sites in the pons through bipolar concentric stainless steel electrodes
(David Kopf Instruments,
model
SNE-100). The stimulating
electrodes were positioned
using the ventral median fissure and ventral surface of
the brainstem as landmarks
for lateral and dorsoventral
orientation.
The A-P level was set stereotaxically.
Statistical
analysis.
Statistical
analysis
was performed with the Student t test for unpaired data. Values
are expressed as means t standard error.
RESULTS
Phase relations
between sympathetic
and phrenic
nerve discharges.
Figure 1 illustrates
the “respiratory”
periodicity
in the spontaneous
discharges
of the external carotid postganglionic
sympathetic
nerve of the vagotomized cat. As described in earlier reports from this
laboratory
(9, 10, 20), sympathetic
nervous discharge
usually was synchronized
into bursts that were locked
in a 1:l relation to the cardiac cycle. The cardiac-related
bursts of SND occurred almost exclusively
during the
inspiratory
phase of the central respiratory
cycle (monitored by RC-integrated
phrenic nerve activity)
in the
example shown in Fig. 1.
Computer summation
was employed to analyze quantitatively
the temporal relations
between sympathetic
and phrenic nerve discharges.
As illustrated
in Fig. 2,
three distinct patterns were observed. The relationship
between sympathetic
and phrenic nerve discharges was
expiratory-inspiratory
(EI) in six cats (Fig. 2, A). The
SND began to increase from a minimum in early expiration and reached a maximum during inspiration.
The EI
pattern was the one most commonly observed by Cohen
and Gootman (7) and Gootman and Cohen (12). Eight
cats exhibited an inspiratory
(I) phase-relation
pattern
(Fig. 2, B). The SND began to increase at the start of
inspiration,
became maximal
near peak inspiration,
and then decayed in time with phrenic nerve discharge.
The I pattern most closely resembled that reported by
Koizumi et al. (15) and Preiss et al. (18). Finally,
an
Downloaded from http://ajplegacy.physiology.org/ by 10.220.33.3 on April 3, 2017
mixture of sodium diallylbarbiturate
(60 mg/kg), urethan (240 mg/kg), and monoethylurea
(240 mg/kg). Rectal temperature
usually
was maintained
between
36
.’
and 37°C with a heat lamp. Blood pressure was monitored from the lumbar aorta (via a femoral catheter) and
displayed on a Grass polygraph.
The cervical vagus
nerves were cut bilaterally
in all experiments
to eliminate sympathetic
and respiratory
reflexes associated
with lung inflation.
Each cat was immobilized
vvith gallamine triethiodide (4 mg/kg, iv) and artificially
ventiiated. Additional
doses of gallamine (2 mg/kg) were administered
as required to maintain paralysis.
Pneumothoracotomy
was
performed
to minimize
the blood pressure
variations
that, normally accompany changes in intrathoracic
pressure. The respirator
pump was adjusteid so that the rate
and amplitude of phrenic nerve discharge were comparable. to that observed in the’ spontaneously
breathing
and vagotomized
preparation
Arterial
Pco2 levels
ranged from 33-43 mmHg (Instr,umentation
Laboratory
pH/gas analyzer, model 113) under these conditions.
Nerve recording
and data analysis.
The procedures
used to record the discharges
of the external
carotid
postganglionic
sympathetic
branch of the superior cervical ganglion and of the phrenic nerve have been described in earlier reports from this laboratory
(11, 21).
The cat was placed in a David Kopf Instruments
stereotaxic apparatus.
The right external carotid and phrenic
nerves were exposed via a ventral approach in the neck
after reflection
of the trachea and esophagus.
Nerve
potentials were recorded monophasically
under oil with
bipolar
platinum
electrodes
after
capacity-coupled
preamplification.
The preamplifier
band pass for the
postganglionic
nerve was l-1,000 Hz, and that for the
phrenic nerve was 104,000 Hz. Nerve potentials were
displayed simultaneously
on a Grass polygraph
and a
dual-beam oscilloscope. The temporal relations between
sympathetic
and phrenic nerve discharges
were analyzed by computer
summation.
After RC integration
(time constant,
0.05 s), nerve potentials
were fed to a
Nicolet 1070 computer. The sweep of the computer was
triggered by a timing pulse derived near the start of
inspiration
(RC-integrated
phrenic nerve discharge).
The memory content of the computer was displayed on a
second oscilloscope and photographed
on 35mm film.
BARMAN
SLOW
SYMPATHETIC
1603
OSCILLATOR
.
;;2
FIG. 2. Patterns
of phase relations
between
spontaneously
occurring phrenic
and sympathetic
nerve
discharges
3 vagotomized
cats. Each panel shows computer-summed
records
sweeps) of RCintegrated
phrenic
(top traces)
and sympathetic
(bottom
traces)
nerve activity.
Address
bin was 4 ms. Increased
nerve discharge
is
shown as an upward
deflection.
Sweep of computer
was triggered
by
a timing
pulse
derived
near beginning
of inspiratory
phase of
phrenic
nerve
discharge
cycle. A: EI pattern.
B: I pattern.
C: IE
pattern.
Horizontal
calibration
is 1 s.
inspiratory-expiratory
(IE) pattern was observed in five
cats (Fig. 2, C). The SND began to increase after the
start of inspiration and reached a maximum in early
expiration. The central respiratory rate (30.9 5 3.2 cycles/min) in vagotomized cats exhibiting the IE pattern
was higher than in those animals in which the phaserelation pattern was EI (22.2 it 2.6 cycles/min) or I (23.4
t 2.3 cycles/min). These values, however, were not
significantly different on a group basis (P < 0.05).
The phase relations between the discharges of the
external
carotid sympathetic
and phrenic nerves
changed spontaneously during the course of five experiments. One such instance is illustrated in Fig. 3. Respi-
FIG. 3. Shift in phase relations
between
phrenic
and sympathetic
nerve discharge
accompanying
change in respiratory
rate in vagotomized cat. Sequence
of computer-summed
traces (32 sweeps) in each
panel is as described
in Fig. 2. Address
bin was 4 ms. Respiratory
rate was 31 cycles/min
in A and 24 cycles/min
in B. Horizontal
calibration
is 1 s.
Downloaded from http://ajplegacy.physiology.org/ by 10.220.33.3 on April 3, 2017
ratory rate decreased from 31 to 24 cycleslmin as rectal
temperature fell from 38 to 35OC.The change in respiratory rate was accompanied by a dramatic shift in the
phase relations between sympathetic and phrenic nerve
discharges. The pattern changed from I (Fig. 3, A) to EI
(Fig. 3, B). The shift in phase relations was further
characterized by an increase in the duration of expiration and prolongation of the excitatory phase of the cycle
of SND. A similar shift from an I to-an EI pattern was
observed in two additional experiments. In two other
cats, respiratory rate increased from 18 to 25 cycles/min
and from 12 to 27 cycles/min when rectal temperature
was raised 2- *3”Cwith a heat lamp. These changes were
accompanied by a shift in th .e phase relations between
sympathetic and phrenic nerve discharges from EI to I.
Dissociation of slow rhythmic components of sympathetic and phrenic nerve discharges. The observation
that changes in respiratory rate were accompanied by
dramatic shifts in the phase relations between external
carotid sympathetic and phrenic nerve discharges
raised the possibility that the slow rhythms in thesenerves were generated by independent oscillators. This
hypothesis is supported by the observation that slow
oscillations of sympathetic and phrenic nerve discharges could be dissociated.
SPONTANEOUS
DISSOCIATION.
Figure 4 illustrates two
of three instances in which the slow rhythmic compo-
1604
S. M.
B
200
loo
L”~~ALJJJJ.JkL~ww
J-iuuAl~LW~L~L~
rhythmic
compoin 2 vagotomized
is as described
in
is 1 s/division.
nen ts of sy,mpathetic and ph.renic nerve discharge were
not locked in a 1:l relation. Panel A shows recordings
from a vagotomized cat in which the respiratory rate
was 13 cycles/min. Each burst of phrenic nerve activity
was accompanied by ti period of enhanced SND. However, an additional period of augmented SND occurred
during the expiratory phase of every second respiratory
cycle. That is, the slow rhythmic components of sympathetic and phrenic nerve discharges were locked in a 39
relation. PaneZ B contains recordings from one of two
cats in which periods of enhanced SND occurred with a
frequency half that of the respiratory rate (33 cycles/
min). Note also that the phase relations between the
slow oscillation of SND and the cycle of phrenic nerve
activity were not tightly locked. An I pattern is evident
for the first two sympathetic oscillations, whereas the
pattern was distinctly EI for the last slow cycle of SND.
HYPERVENTILATION.
Hyperventilation
to the point of
phrenic nerve quiescence was accomplished by increasing the respirator pump rate. Contrary to the results
reported by others (15, 18), the slow sympathetic
rhythm was maintained in 11 of 18 experiments when
the rhythmic discharge of the phrenic nerve ceased. The
mean rate of slow sympathetic oscillations in these experiments was 25 t 3 before and 26 2 1 cycles/min
during hyperventilation.
A typical experiment is shown
in Fig. 5, A. Note that the form and frequency of occurrence of the slow sympathetic oscillations were not
markedly changed during hyperventilation
in this cat.
AND
G.
L. GEBBER
Hyperventilation
to the point of phrenic nerve quiescence was associated with disappearance
of the slow
rhythmic
component of SND in the remaining
seven
experiments
(Fig. 5, B). The amplitude of SND during
hyperventilation
in these cats was comparable to that
observed during the peak of the excitatory
phase of the
slow sympathetic
oscillation in the normocapnic
state.
Persistence
of the slow periodic component of SND
during hyperventilation
would be a strong argument in
favor of the existence of an independent
sympathetic
oscillator, providing that phrenic nerve quiescence was
due to a change in the functional state of the brainstem
respiratory
oscillator.
That such was the case is indirectly suggested by the results of experiments
in which
the phrenic nerve responses elicited by single shocks (10
V; 0.5 ms) applied to inspiratory-facilitatory
sites located in the dorsolateral
pontine reticular
formation
(P3, L3.5, H-3 to H-6) were compared in the normocapnic and hyperventilated
states. One of the two experiments performed is illustrated
in Fig. 6. As previously
reported by Cohen (5), single-shock
stimulation
of the
dorsolateral
rostra1 pons during
inspiration
elicited
short latency (3.3 ms) phrenic nerve responses (Fig. 6,
Al). The phrenic nerve discharge elicited during early
expiration
(Fig. 6, A2) was somewhat smaller in amplitude and had a longer onset latency (5.6 ms). Significantly, the phrenic nerve response evoked by pontine
stimulation
during hyperventilation
(Fig. 6, B3) was
only slightly smaller than the discharge elicited previously during expiration in the normocapnic state. These
observations indicate that phrenic nerve quiescence
during hyperventilation
could not be attributed to inexcitability of descending inspiratory pathways or spinal
inspiratory motoneurons. Rather, these resu.lts indirectly support the experim ents of Cohen ( 3) wh ich demonstrated that hypocapnia i.n the cat led to disappearante of the rhythmic components of the discharges of
brainstem respiratory neurons.
DISCUSSION
The slow rhythm in SND of vagotomized cats is generally assumed to be extrinsically imposed upon central
sympathetic networks by phase-spanning and/or phaselocked elements of the brainstem respiratory oscillator
(7, 12, 15, 18). However, a number of observations made
in the present study contradict this view. Rather, they
support the hypothesis that the slow periodic components of sympathetic and phrenic nerve activity are
generated by independent oscillators that are normally
but not always entrained to each other.
First, it was observed that changes in respiratory rate
were accompanied by dramatic shifts in the phase relations between the discharges of the phrenic and external
carotid sympathetic nerves. The pattern of temporal
relations was shifted from I to EI when respiratory rate
slowed and from EI to I when the respiratory rate was
increased. These results make it difficult to accept the
notion that respiratory periodicity is extrinsically imposed on central sympathetic networks by any one partitular component of the respiratory oscillator. If such
were th .e case, then the phase relations between sympa-
Downloaded from http://ajplegacy.physiology.org/ by 10.220.33.3 on April 3, 2017
FIG. 4. Dissociation
of 1:l relation
between
slow
nents of sympathetic
and phrenic
nerve discharges
cats (A and B). Sequence
of traces in each panel
Fig. 1. Vertical
calibrations
are 40 pV. Time base
BARMAN
1605
on slow rhythmic
components
of
discharges
in 2 vagotomized
cats (A
and B).
Vertical
Sequence
calibrations
:I\ 3
d ;-
thetic and phrenic nerve discharges
should have been
independent
of the respiratory
rate.
Second, the slow oscillations
of sympathetic
and
phrenic nerve activity were not always locked in a 1:l
relation.
As was shown in Fig. 4, the slow rhythmic
component of SND could occur at a frequency less than
or greater than the respiratory
rate. Thus, dissociation
of the slow rhythms
exhibited
in sympathetic
and
phrenic nerve discharges was possible.
of traces in each panel is as described
are 40 pV. Time base is 1 s/division.
J
in Fig.
1.
FIG. 6. Effect of hyperventilation
on
phrenic
nerve response
evoked
by single-shock
stimulation
(10 V, 0.5 ms) of
an inspiratory
facilitatory
site in dorsolateral
pontine
reticular
formation.
Top traces show phrenic
neurogram
before (A) and during
(B) hyperventilation. Bottom
traces (records
13) are
computer-summed
phrenic
nerve
responses (32 sweeps) evoked
by pontine
stimulation.
Address
bin was 0.2 ms.
Record
1: phrenic
response
elicited
by
shock applied
during
inspiration.
Record 2: response
evoked
by shock applied during
early
expiration.
Record
3: response
evoked
by shock applied
once every
4 s after disappearance
of
spontaneously
occurring
phrenic
nerve
activity
during
hyperventilation.
Vertical calibrations
are 20 PV for phrenic
neurogram
and 66 PV for computersummed
evoked
potentials.
Horizontal
calibrations
are 200 ms for phrenic
neurogram
and 10 ms for evoked
responses.
Third, and perhaps most definitive, slow sympathetic
oscillations that were locked in a 1:l relation to the
phrenic nerve discharge cycle in the normocapnic state
often persisted when respiratory rhythmicity
disappeared during hyperventilation.
This observation is pertinent when viewed in the light of experiments performed by Cohen (3). He reported that hypocapnia in
the cat led to disappearance of the rhythmic components
of the discharges of brainstem respiratory neurons. As a
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FIG. 5. Effect of hyperventilation
sympathetic
and phrenic
nerve
1606
BARMAN
AND
G. L. GEBBER
tions. First, the two independent
oscillators
might, in
some way, directly interact with each other. Elements
of the respiratory
oscillator might entrain the slow sympathetic oscillator to the cycle of phrenic nerve activity.
Alternatively,
the respiratory
and slow sympathetic
oscillators might be reciprocally
connected. Second, it is
conceivable that both oscillators
receive common inputs
from a distinct brainstem
synchronizing
mechanism. In
this case, the respiratory
and slow sympathetic
oscillators would not be directly connected.
The slow sympathetic
rhythm
is mani fested by the
waxing
and waning
of the amplitude
of more rapid
periodic components within the SND. This ‘was clearly
evident in experiments
in which the SND took the form
of bursts locked in a 1:l relation to the cardiac cycle. The
“cardiac”
periodicity
(3-5 Hz) has been previously
shown to be representative
of a sympathetic
rhythm of
brainstem
origin that normally is entrained to the cardisc cycle by the baroreceptor
refle xes (9, 10, 20). Thus,
the brainstem
network responsible for generation of the
3-5 Hz periodicity
apparently
receives inputs from the
slow sympathetic
oscillator.
Gootman and Cohen (12)
reported that the predominant
periodicity
in the SND
sometimes was changed from 3 to 10 Hz during inspiration in vagotomized cats. Evidence for such a change is
shown in Fig. 5, B of the present study. Consequently,
the slow sympathetic
oscillator apparently
also serves
as a modulator of transmission
in spinal networks
that
have been shown by McCall and Gebber (16) to be
responsible
for the lo-Hz periodic component
of the
SND.
In summary,
the present study has extended our
knowledge
of the hierarchical
nature of the organization
of central sympathetic
networks.
Brainstem
and spinal
networks
are inherently
capable of synchronizing
the
discharge of populations
of sympathetic
neurons into 3to ~-HZ and lo-Hz periodically
occurring
wave forms.
These networks
appear to be subordinate
to a slow
sympathetic
oscillator presumably
located in the brainstem. This oscillator
functions
as an amplitude
and
sometimes as a freq uency modulator with regard to the
mass discharges
of peripheral
sympathetic
nerve b undles. The slow sympathetic
oscillator is linked to at least
one other brainstem system, i.e., the respiratory
oscillator.
This
investigation
was supported
by Public
Health
Service
Grant
HL-13187*
Received
for publication
25 March
1976.
REFERENCES
1. ADRIAN,
E. D., D. W. BRONK, AND G. PHILLIPS.
Discharges
in
mammalian
sympathetic
nerves.
J. PhysioZ.,
London
74: 115133, 1932.
2. BRONK, D. W., L. K. FERGU~ON,
R. MARGARIA,
AND D. Y. SoLANDT. The activity
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centers.
Am. J.
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117: 237-249,
1936,
3. COHEN, M. I. Discharge
patterns
of brain-stem
respiratory
neurons in relation
to carbon
dioxide
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31:
142-165,
1968.
4. COHEN, M. I. How respiratory
rhythm
originates:
Evidence
from
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patterns
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In: Ciba
Found.
Hering-Breuer
Centenary
Symp.;
Breathing.
London:
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1970, p. 125-150.
5. COHEN, M. I. Switching
of the respiratory
phases and evoked
phrenic responses
produced
by rostra1 pontine
electrical
stimulation. J. Physiol.,
London
217: 133-158,
1971.
6. COHEN, M. I. The genesis of respiratory
rhythmicity.
In: Central
Rhythmic
and Regulation.
Stuttgart:
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1974, p. 1535.
7. COHEN, M. I., AND P. M. G~~TMAN.
Periodicity
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nerve of the cat. Am. J. Physiol.
218: 10921101, 1970.
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general rule, the discharges
of expiratory
(E) and expiratory-inspiratory
neurons became continuous,
whereas
the discharges of inspiratory
and inspiratory-expiratory
neurons became sporadic and eventually
ceased as the
level of arterial Pcoz was lowered. Thus, phrenic nerve
quiescence produced by hyperventilation
in our experiments presumably
was associated with disappearance
of
the rhythmic
discharges
in those mutually
inhibitory
brainstem
neurons (I and E, IE and EI) that comprise
the central respiratory
oscillator (4, 6, 13). Under these
conditions, it would be impossible to attribute
the generation of the slow rhythm ic component of SND to a
direct connection
between
th .e brainstem
respiratory
oscillator
and the central
sympathetic
networks.
Rather, the possibility
must be considered that the slow
rhythmic
component of SND was generated by an independent sy pmpathetic oscillator. The neuronal types.that
constitute
the slow sympathetic
oscillator
apparently
are less apt to lose thei .r rhy thmi .c discharge pa ttern
duri ng hyperventila tion than are those neurons that
comprise the respiratory
oscillator.
Arguments
may be raised concerning whether each of
the observations
discussed above is sufficient to support
the conclusion
that the slow rhythmic
component
of
SND was generated by an oscillator independent of the
one responsible for respiratory
rhythmicity.
Preiss et al.
(18) have suggested that population recording does not
allow for precise hypotheses concerning the mechanism
of respiratory
periodicity,
since any particular
pattern
of phase relations
between
sympathetic
and phrenic
nerve activity
might arise from the superposition
of
more than one firing pattern of the contributing
units.
It could be argued that dissociation of the slow rhythmic
components
of sympathetic
and phrenic
nerve discharges as seen in Fig. 4 might have occurred at a locus
within sympathetic
or respiratory
networks
distal to the
point of direct connection
between
the two systems.
Finally, the question whether all brainstem
respiratory
neurons lost their rhythmic
discharge pattern at a time
when the phrenic nerve became quiescent cannot be
it is our opi nion that the presanswered. Nevertheless,
ently available evidence as a whole is m .ost consi .stent
with the independent oscillator hypothesis.
Synchronization
of the two independent
oscillators
undoubtedly
is important
in coordinating
sympathetic
and respiratory
responses to a variety of environmental
conditions. The mechanism responsible for synchronization of the respiratory
and slow sympathetic
oscillators,
however,
is not clear at the present time. At least two
possibilities
should be entertained
in future investiga-
S. M.
SLOW
SYMPATHETIC
OSCILLATOR
8: DALY, M. DEB., J. L. HAZZLEDINE,
AND A. UNGAR.
The reflex
effects of alterations
in lung volume
on systemic
vascular
resistante in the dog. J. PhysioZ.,
London
188: 331-351,
1967.
9. GEBBER, G. L. Basis for phase relations
between
baroreceptor
and sympathetic
nervous
discharge.
Am. J. Physiol.
230: 263270, 1976.
Organization
10. GEBBER, G. L., D. G. TAYLOR, AND R. B. MCCALL.
of central
vasomotor
system.
In: Symposium
on Mechanisms
of
Drug Action
on Central
Cardiovascular
Control.
Proc. Intern.
Congr.
Pharmacol.
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