J Appl Physiol
91: 137–144, 2001.
Effects of postural changes and vestibular lesions on
diaphragm and rectus abdominis activity in awake cats
L. A. COTTER,1 H. E. ARENDT,1 J. G. JASKO,1 C. SPRANDO,1 S. P. CASS,2 AND B. J. YATES1
Department of Otolaryngology, University of Pittsburgh School of Medicine,
Pittsburgh, Pennsylvania 15213; and 2Department of Otolaryngology,
University of Colorado Health Sciences Center, Denver, Colorado 80262
1
Received 19 December 2000; accepted in final form 13 February 2001
the resting length of
respiratory muscles, requiring alterations in the activity of these muscles if ventilation is to be unaffected.
For example, it is well established that nose-up tilt of
quadrupeds or standing in humans from a supine position can produce diaphragm shortening (11, 14, 16,
18, 25). Compensation for the effects of gravity on
diaphragm length during supine to head-up body tilts
includes both an increase in diaphragm activity and a
cocontraction of the abdominal muscles (5, 6, 8, 10, 13,
18, 25). Experiments in anesthetized dogs have suggested that vagal afferents play an important role in
eliciting changes in respiratory muscle activity during
postural alterations (7, 10). However, recent studies in
decerebrate, unanesthetized animals showed that the
vestibular system also contributes to altering respiratory muscle activity during movement and changes in
posture (22, 23, 27, 29). Furthermore, anatomic studies
have demonstrated that many bulbospinal neurons in
the medial medullary reticular formation provide inputs to both phrenic and rectus abdominis motoneurons (2); because this region of the reticular formation
receives substantial vestibular and other movementrelated inputs (19, 20, 26), it seems likely that reticulospinal neurons could adjust the activity of both diaphragm and abdominal motoneurons during postural
alterations.
The present study had several objectives. One goal
was to compare changes in diaphragm and abdominal
muscle activity during whole body tilts in awake cats,
to reassess the relative activation of these muscles
during movement. Unlike previous studies in anesthetized dogs (8, 10, 18, 25), body tilts were performed in
prone animals, because postural alterations from the
supine position (which were examined in the prior
studies) are infrequent in quadrupeds. Abdominal
muscle recordings were made from rectus abdominis,
because this is the only expiratory muscle thus far
demonstrated to be coactivated with the diaphragm by
the medial medullary reticular formation (1, 2). Although previous studies have indicated that rectus
abdominis displays less expiratory-related activity
than deeper abdominal muscles such as transversus
abdominis (12), rectus abdominis is well suited to tonically restrain the abdominal contents during postural
changes that allow gravity to displace the viscera (9).
In addition, rectus abdominis has been shown to be
activated during expiratory loading in cats and plays a
significant role in increasing abdominal cavity pressure during some behaviors such as coughing (3). A
second goal was to determine whether tonic firing of
rectus abdominis and the diaphragm or alterations in
the activity of these muscles during postural changes is
influenced by the vestibular system. For this purpose,
recordings were made from the muscles before and
after removal of vestibular inputs by means of a com-
Address for reprint requests and other correspondence: B. Yates,
Dept. of Otolaryngology, Univ. of Pittsburgh, Eye and Ear Institute,
Rm. 106, 203 Lothrop St., Pittsburgh, PA 15213 (E-mail:
[email protected]).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
respiration; abdominal muscle; plasticity
CHANGES IN POSTURE CAN AFFECT
http://www.jap.org
8750-7587/01 $5.00 Copyright © 2001 the American Physiological Society
137
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Cotter, L. A., H. E. Arendt, J. G. Jasko, C. Sprando,
S. P. Cass, and B. J. Yates. Effects of postural changes and
vestibular lesions on diaphragm and rectus abdominis activity in awake cats. J Appl Physiol 91: 137–144, 2001.—
Changes in posture can affect the resting length of the
diaphragm, requiring alterations in the activity of both the
abdominal muscles and the diaphragm to maintain stable
ventilation. To determine the role of the vestibular system in
regulating respiratory muscle discharges during postural
changes, spontaneous diaphragm and rectus abdominis activity and modulation of the firing of these muscles during
nose-up and ear-down tilt were compared before and after
removal of labyrinthine inputs in awake cats. In vestibularintact animals, nose-up and ear-down tilts from the prone
position altered rectus abdominis firing, whereas the effects
of body rotation on diaphragm activity were not statistically
significant. After peripheral vestibular lesions, spontaneous
diaphragm and rectus abdominis discharges increased significantly (by ⬃170%), and augmentation of rectus abdominis
activity during nose-up body rotation was diminished. However, spontaneous muscle activity and responses to tilt began
to recover after a few days after the lesions, presumably
because of plasticity in the central vestibular system. These
data suggest that the vestibular system provides tonic inhibitory influences on rectus abdominis and the diaphragm and
in addition contributes to eliciting increases in abdominal
muscle activity during some changes in body orientation.
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VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
Table 1. Period of data recording and total number of experimental trials for each animal
Prevestibular Lesions
Animal No.
1
2
3
4
5
6
7
Postvestibular Lesions
Muscles Recorded
Recording period,
days
Total no. of tilts
performed
Recording period,
days
Total no. of tilts
performed
Diaphragm ⫹ RA
Diaphragm ⫹ RA
Diaphragm ⫹ RA
Diaphragm ⫹ RA
Diaphragm ⫹ RA
Diaphragm Only
RA only
79
41
109
106
146
106
79
1,038
1,134
998
703
798
424
549
22
40
34
33
30
20
25
401
707
632
417
363
355
302
RA, rectus abdominis.
METHODS
All of the procedures used in this study conformed to the
American Physiological Society’s Guiding Principles in the
Care and Use of Animals and were approved by the University of Pittsburgh’s Institutional Animal Care and Use Committee.
Overview of data collection procedures. Data were collected
from seven female adult cats that had been spayed before the
onset of data collection. The general procedures for producing
body tilts were similar to those in a previous study that
considered the effects of vestibular lesions on orthostatic
tolerance in awake cats (15). Animals were trained to remain
sedentary in the prone position on a tilt table during nose-up
or ear-down whole body rotations of 20, 40, or 60° amplitude.
A restraint bag with attached Velcro straps was placed
around the animal’s body; the Velcro straps were secured to
the sides of the tilt table to prevent the animal’s position from
shifting during testing. The animal’s head was immobilized
by inserting a screw into a bolt mounted on the skull. Activity
of rectus abdominis and the costal diaphragm was typically
recorded using pairs of Teflon-insulated stainless steel wire
Fig. 1. Example of respiratory muscle
activity recorded during whole body
tilt, illustrating the method used to
quantify data in this study. Trace A
shows rectus abdominis activity, trace
B shows diaphragm activity, and trace
C is a recording of table position. In
this example, the animal was tilted
from the prone position to 60° nose up.
Average respiratory muscle activity
was determined for the period in which
the animal was tilted maximally as
well as an equivalent time interval immediately before each tilt.
(Cooner Wire, Chatsworth, CA) stripped of insulation for ⬃5
mm and sutured to the muscle epimysium together with an
insulating patch of Silastic sheeting. In one animal, however,
wire pairs with uninsulated tips of ⬃1 mm length were
inserted directly into the muscles and secured using sutures.
The insulated portions of the wires were led subcutaneously
and soldered to a connector mounted on the animal’s head.
Data were collected during recording sessions with a duration of ⬃30 min; one to three recording sessions were conducted per day. During each recording session, only one
direction of tilt was performed (either nose up or left or right
ear down), although table rotations of 20, 40, and 60° amplitude were randomly disbursed so that animals could not
“predict” the amplitude of tilt at the onset of each rotation.
Tilts persisted for 40–60 s and were separated by at least 1
min. Only data recorded during trials in which animals were
observed to remain sedentary were analyzed. The tilt table
was rotated manually and was secured in the tilted position
using a spring device that permitted movement to one of
three predetermined amplitudes. Rotations from the Earthhorizontal to the nose-up or ear-down position were performed rapidly, at a velocity of ⬃60°/s at all three amplitudes.
Respiratory muscle responses to tilt were recorded in animals with eighth cranial nerves intact over a period of
41–146 days (Table 1). Average activity of the diaphragm
and rectus abdominis was determined for the period during
which the animal was tilted maximally and compared with
activity averaged over an equivalent time period immediately before the tilt, as indicated in Fig. 1. Subsequently,
vestibular inputs were removed bilaterally, and respiratory
muscle activity before and during tilts was measured in the
same manner as before the lesion. The postlesion recordings
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bined bilateral labyrinthectomy and transection of the
eighth cranial nerves. However, rapid plastic changes
occur in the central vestibular system after removal of
labyrinthine inputs (21, 24, 28), in part because the
vestibular nuclei receive substantial nonlabyrinthine
inputs signaling body position in space (28). Thus effects of vestibular lesions on respiratory muscle activity were monitored for ⬃1 mo to determine whether
long-term compensation for deficits in respiratory regulation produced by the lesions would occur.
VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
during the postsurgical period, an intravenous injection port
remained in place for 2 days after surgery, and 50 ml of 5%
dextrose solution were administered intravenously each day.
In addition, feeding was done by hand until the animal’s
spontaneous consumption of food and water returned to prelesion levels, which required 3–5 days.
Data recording procedures. During recording sessions, a
cable was attached to the head-mounted connector to allow
EMG signals to be fed to an alternating-current amplifier
(model 1700, A-M Systems, Carlsberg, WA); activity was
amplified by a factor of 104, filtered with a band pass of
10–10,000 Hz, and full-wave rectified with a time constant of
1 ms. Subsequently, signals were recorded digitally using a
1401-plus data collection system (Cambridge Electronic Design, Cambridge, UK) interfaced with a Macintosh G3 computer (sampling rate of 1,000 Hz). A potentiometer mounted
on the tilt table provided a recording of table position; the
voltage from this potentiometer was digitized and sampled at
100 Hz. The Spike-2 software package (Cambridge Electronic
Design) was used for data analysis.
Average EMG activity was determined for the time period
an animal was tilted from the prone position as well as over
an equivalent time period immediately preceding each tilt
(see Fig. 1). To determine whether baseline respiratory muscle firing was altered by removal of vestibular inputs in a
particular animal, levels of pretilt activity ascertained for
pre- and postlesion trials were averaged and compared statistically as described in Statistical analysis of data. To pool
results from all animals, an average was made of the mean
percent change in respiratory muscle activity produced by
eighth cranial nerve transection in each animal. Because
percent changes in activity were considered in this analysis,
differences between animals in baselines and noise levels of
EMG recordings were accounted for.
Verification of recording electrode locations and vestibular
lesions. At the conclusion of data recording, animals were
anesthetized with an intraperitoneal injection of pentobarbital sodium (40 mg/kg) and perfused transcardially with phosphate-buffered saline followed by the paraformaldehydelysine-sodium metaperiodate fixative developed by McLean
and Nakane (17). The diaphragm was then removed so that
the placement of EMG recording electrodes could be determined. Rectus abdominis was also inspected to confirm electrode placement. In three animals, the head was removed
and decalcified using a solution of EDTA and hydrochloric
acid. The temporal bone on each side was subsequently
removed, embedded in 12% celloidin, cut in the coronal plane
(30-␮m thickness), and stained using hemotoxilyn. The temporal bone sections were then inspected histologically to
determine the extent of damage to the eighth cranial nerves
and vestibular labyrinth. In all cases, it was obvious that
peripheral vestibular inputs were eliminated on both sides.
Statistical analysis of data. Statistical analyses of data
were performed with the use of the Prism 3 software package
(GraphPad Software, San Diego, CA) running on a Macintosh
G4 computer. A nonparametric repeated-measures ANOVA
procedure (Friedman test) in combination with a post hoc
test (Dunn’s multiple-comparison test) was used to compare
respiratory activity measured before the peripheral vestibular lesion, in the first week after the lesion, and at subsequent times. This procedure was also used to compare
changes in respiratory muscle activity elicited by different
rotation amplitudes and directions. A Mann-Whitney test
was used to compare changes in diaphragm and rectus abdominis activity during specific postural alterations. Statistical significance was set at P ⬍ 0.05. Pooled data are presented as means ⫾ SE.
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began the day after the surgery and continued for 20–34 days
(see Table 1). Data recording was performed daily for the first
week after the lesions and subsequently at least every 3 days.
Training procedures. A training period of ⬃2–3 mo was
required for animals to learn to remain sedentary during
experimental sessions. The training was performed in two
phases. As a first step, animals learned to tolerate body
restraint in a vinyl bag. The restraint period initially lasted
for only a few minutes, but it was gradually increased until
animals remained sedentary for at least 30 min. Food was
provided at the end of the testing period as a reward, and the
experimental session was terminated promptly if the animal
attempted to move from the restraint bag or showed any
signs of distress (e.g., vocalization). The second phase of
training involved teaching the animal to tolerate head fixation. Initially, the head was fixed for only a few minutes, but
this interval was increased over time until the animal remained relaxed throughout a head-fixation period of 30 min.
No data were collected until training was complete and the
animal could be restrained throughout the testing period
without vocalization or any indication of discomfort.
Surgical procedures. Two recovery surgeries were required
for each animal. Both surgeries were performed using sterile
procedures in a dedicated operating suite. The first surgical
procedure was performed to secure a bolt to the skull to
permit head fixation and to implant electromyogram (EMG)
recording electrodes. The second surgery to produce peripheral vestibular lesions was performed after initial data collection was complete.
For each surgery, animals were initially anesthetized using an intramuscular injection of ketamine (15 mg/kg) and
acepromazine (0.2 mg/kg). Subsequently, an endotracheal
tube and intravenous catheter were inserted. Anesthesia was
supplemented as necessary using 1–1.5% isoflurane vaporized in O2 to maintain areflexia and stable heart rate. Ringer
lactate solution was infused intravenously to replace fluid
loss during the surgery, and a heating pad was used to
maintain rectal temperature near 38°C.
To place EMG electrodes for recording diaphragm activity,
a small incision was made through linea alba, and the liver
and adjacent viscera were retracted to provide access to the
costal diaphragm on one side. After implantation of diaphragm electrodes, the abdominal musculature was closed
with the use of sutures, and EMG electrodes were attached to
a portion of rectus abdominis near the border with the external oblique. Subsequently, the animal’s head was secured in
a stereotaxic frame, and a head fixation bolt was mounted
with the use of procedures described in a previous publication (15). Wires from the EMG recording electrodes were
attached to a connector that was mounted on the skull behind
the fixation plate.
To eliminate vestibular inputs, the tympanic bulla on each
side was exposed using a ventrolateral approach and opened
to expose the cochlea. A drill was used to remove temporal
bone near the base of the cochlea, thereby producing a labyrinthectomy that rendered the vestibular apparatus dysfunctional. This procedure also provided access to the internal
auditory canal. The eighth cranial nerve was then transected
under microscopic observation within the internal auditory
canal. Thus two independent lesions affecting the vestibular
system were made on both sides to ensure that vestibular
inputs were removed. In no case did nystagmus or deviation
in eye position occur after the surgery, suggesting that the
peripheral lesions were complete bilaterally. Furthermore,
our laboratory has previously demonstrated that this procedure is effective in eliminating vestibular input (15). To
ensure that animals received proper hydration and nutrition
139
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VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
RESULTS
Fig. 2. Effects of nose-up and ear-down
tilts of different amplitudes on electromyogram activity recorded from rectus
abdominis and the diaphragm. Every
data point represents pooled responses
from 6 animals. Error bars indicate SE.
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Successful recordings of EMG activity were made
from both rectus abdominis and the diaphragm in five
of the seven animals; in one additional animal, only
rectus abdominis activity was reliably recorded
throughout the experiment, and, in another case, only
the diaphragm provided consistent data during the
entire recording period. Thus a sample of six animals
was used to determine the effects of tilt on either rectus
abdominis or diaphragm firing; the consequences of
bilateral removal of vestibular inputs on spontaneous
respiratory muscle activity and on tilt-elicited changes
in muscle discharges were examined in all of these
cases.
Effects of body tilt on rectus abdominis and diaphragm activity before vestibular lesions. An example
of diaphragm and rectus abdominis EMG activity recorded before and during a 60° nose-up tilt in one
animal is shown in Fig. 1. The effects of 20, 40, and 60°
nose-up and ear-down tilt on rectus abdominis and
diaphragm firing are shown in Fig. 2; the data points in
this figure represent pooled responses from six animals. Nose-up tilt produced an increase in rectus abdominis activity whose magnitude was dependent on
the amplitude of the rotation; the relationship between
tilt amplitude and the increase in muscle activity was
shown to be statistically significant using a nonparametric repeated-measures ANOVA procedure (Friedman test, P ⫽ 0.002). Similarly, ipsilateral ear-down
tilt (toward the muscle that was recorded from) produced a statistically significant (P ⫽ 0.001) amplitudedependent increase in rectus abdominis activity. During contralateral ear-down tilt, the increase in rectus
abdominis activity with respect to rotation amplitude
approached statistical significance (P ⫽ 0.052). In contrast, no significant relationship between tilt amplitude and changes in diaphragm activity could be ascertained (P ⬎ 0.05) for any direction of rotation.
Although the increase in rectus abdominis activity
(23%) during 60° nose-up tilt appeared larger than
that during either 60° ipsilateral (13%) or contralateral (15%) ear-down tilt, these differences did not
reach statistical significance (P ⬎ 0.05, Friedman
test). Nonetheless, the increase in rectus abdominis
activity elicited by 60° nose-up pitch was significantly (P ⫽ 0.02, 2-tailed Mann-Whitney test) larger
than the increase in diaphragm activity (4%) elicited
by the same rotation. However, the changes in rectus
abdominis and diaphragm activity produced by 60°
ipsilateral and contralateral ear-down roll were not
statistically distinguishable (P ⬎ 0.05, 2-tailed
Mann-Whitney test).
Effects of bilateral eighth cranial nerve transection
on spontaneous rectus abdominis and diaphragm
activity. After bilateral removal of vestibular inputs,
background activities of rectus abdominis and the
diaphragm recorded when animals were in the
prone, untilted position were compared with firing
measured before the lesions. Figure 3 compares average EMG activity before and after the vestibular
neurectomy in each animal. Removal of vestibular
inputs produced a highly statistically significant
(P ⬍ 0.0001, Friedman test) increase in rectus abdominis and diaphragm activity in every animal. Respiratory muscle activity typically diminished after
the first 3 days after removal of vestibular inputs,
but it was still significantly higher than before the
lesions in the majority of animals (see Fig. 3). In four
cases for both rectus abdominis and diaphragm recordings, spontaneous activity did not recover to
prelesion levels even after more than a week.
To further consider the effects of eighth cranial nerve
transection on baseline respiratory muscle activity, the
percent changes in spontaneous EMG activity from
prelesion values determined for all animals were
pooled. The results of this analysis are shown in Figure
4. Because spontaneous rectus abdominis and diaphragm activity typically remained elevated for at
least a week after peripheral vestibular lesions (see
Fig. 3), all data collected in the first week after the
removal of vestibular inputs were combined to form a
single group. When all animals were considered together, it was determined that the postlesion increase
in both rectus abdominis and diaphragm activity was
statistically significant (P ⫽ 0.006 for rectus abdominis
and P ⫽ 0.03 for the diaphragm, Friedman test). However, a post hoc test (Dunn’s multiple-comparison test)
indicated that this significant increase in muscle activity could only be demonstrated for the first week after
removal of vestibular inputs. Rectus abdominis and
diaphragm EMG activity recorded subsequently was
not statistically different (P ⬎ 0.05) from prelesion
VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
141
Fig. 3. Effects of removal of vestibular inputs on baseline rectus abdominis (A) and
diaphragm (B) activity in each animal. Electromyogram activity was recorded when animals were in the prone position, both before
and after peripheral vestibular lesions. The
postlesion data were separated into 3 groups
for this analysis: those recorded in the first 3
days after the lesion (D1–3), those recorded
in the following 3 days (D4–6), and those
recorded subsequently (Subs). Error bars indicate SE. *Postlesion average significantly
different from that before removal of vestibular inputs, P ⬍ 0.05.
this decrease in the muscle’s response to tilt was only
significant during the first week after the lesion. However, removal of vestibular inputs resulted in no reduction in the percent increase in rectus abdominis activity during either ipsilateral or contralateral ear-down
tilt or in the modest increases in diaphragm activity
during any direction of tilt.
Because spontaneous respiratory muscle activity
was elevated after the removal of vestibular inputs,
one possibility is that a “ceiling effect” prevented further increases in firing levels during body tilts. However, in all animals, transient increases in muscle
activity that were much higher than the mean baseline
level were noted after the lesions, particularly during
voluntary movements at the end of recording sessions.
Figure 6 illustrates an example of a transient burst of
Fig. 4. Percent increase in baseline respiratory muscle activity after removal of vestibular inputs for all animals pooled. To perform
this analysis, prelesion rectus abdominis and
diaphragm activity in each animal was standardized at 100%, and the percent change in
muscle activity after the lesion was determined for each animal. Subsequently, the values from each animal were averaged. W 1, first
week; Subs, subsequent to first week. Error
bars indicate SE. *Postlesion average significantly different from that before removal of
vestibular inputs, P ⬍ 0.05.
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values, despite the fact that in many animals the
baseline level of firing remained significantly elevated
(see Fig. 3).
Effects of bilateral eighth cranial nerve transection
on changes in rectus abdominis and diaphragm activity
during whole body tilts. The effects of removal of vestibular inputs on changes in rectus abdominis and
diaphragm activity during 60° nose-up and ear-down
tilt were also examined and are shown in Fig. 5. Figure
6 provides examples of rectus abdominis responses to
60° nose-up tilt before and 1 day after vestibular lesions in one animal (animal 5). Eighth cranial nerve
transection resulted in a significant (P ⫽ 0.006, Friedman test) decrement in the percent increase in rectus
abdominis activity during 60° nose-up pitch. A post hoc
test (Dunn’s multiple-comparison test) indicated that
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VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
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Fig. 5. Effects of removal of vestibular inputs on
increases in rectus abdominis and diaphragm
activity during 60° nose-up and ear-down tilt.
Bars represent pooled data from 6 animals. Error bars indicate SE. *Postlesion average significantly different from that before removal of vestibular inputs, P ⬍ 0.05.
muscle activity that occurred during nose-up tilt after
eighth cranial nerve transection. These observations
indicate that a ceiling effect did not result in the
postlesion decrement of rectus abdominis responses to
60° nose-up tilt.
DISCUSSION
Nose-up or ear-down tilt from the prone position in
awake cats resulted in an amplitude-dependent in-
crease in rectus abdominis activity, presumably to restrain the abdominal viscera during these movements.
Although prior studies that considered the effects of
postural changes on abdominal muscle activity (e.g.,
Refs. 8, 10) largely ignored rectus abdominis, mainly
because this muscle is typically silent (12), the present
data show that rectus abdominis exhibits posturally
related discharges in awake cats. Furthermore,
changes in rectus abdominis activity during 60°
VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
143
Fig. 6. Example of effects of removal of vestibular inputs on spontaneous activity of rectus abdominis and on
increases in muscle activity during 60° nose-up tilt from the prone position. The postlesion activity was recorded
1 day after bilateral transection of the eighth cranial nerves. An arrow denotes a brief burst of activity during the
postlesion recording. The occurrence of this burst of muscle firing indicates that activity was not maximal and that
the lack of a response to nose-up tilt after the removal of vestibular inputs was not due to a “ceiling effect.”
jections from the medial medullary reticular formation, because neurons in this region have been
demonstrated to make synaptic connections with diaphragm and abdominal motoneurons (1, 2, 30) and to
receive vestibular inputs (4, 20). However, further experiments will be required to establish whether either
the tonic inhibition or the posturally related excitation
of respiratory motoneurons provided by the vestibular
system is mediated by medial medullary reticulospinal
neurons.
After a few days after bilateral eighth cranial nerve
transection, tonic activity of both the diaphragm and
rectus abdominis and modulation of rectus abdominis
activity during nose-up tilts tended to return to prelesion values, although in many animals complete recovery was not observed. Such compensation is not unexpected, however, because after removal of labyrinthine
inputs vestibular nucleus neurons quickly regain spontaneous activity and even modulation of their firing
during whole body rotations (21, 24, 28). This adaptive
plasticity is undoubtedly related to the presence of
substantial nonlabyrinthine inputs reflecting body position in space to the vestibular nuclei (28). Thus, even
after elimination of inputs from the inner ear, the
central vestibular system could potentially influence
the regulation of respiratory muscle activity. It is
therefore likely that bilateral vestibular nucleus lesions would have larger effects on tonic respiratory
muscle activity and alterations in this activity during
changes in posture than would bilateral eighth cranial
nerve transection. This prospect remains to be explored experimentally.
Three caveats must be considered when interpreting
the results of this study. First, the peripheral lesions
used to remove vestibular inputs undoubtedly also
diminished auditory signals to the central nervous
system. Thus the possibility exists that the effects of
eighth cranial nerve transections on respiratory muscle activity were related more to the peripheral auditory lesion than to removal of vestibular inputs. However, this prospect seems remote, because auditory
stimulation has not been demonstrated to affect respiration. Second, the only abdominal muscle that was
studied was rectus abdominis, and it is possible that
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nose-up tilts were significantly larger than alterations
in diaphragm activity during these rotations. It was
previously observed in anesthetized dogs that prevention of diaphragm shortening during nose-up tilts from
a supine position was more related to increases in
abdominal muscle activity than diaphragm activity
(13). The present data show that similar relative increases in diaphragm and rectus abdominis activity
occur during nose-up rotations from a prone position in
awake cats.
The present study also demonstrated that the vestibular system tonically influences respiratory muscle
activity in awake animals, because removal of vestibular inputs produced a significant increase in spontaneous firing of both rectus abdominis and the diaphragm. The simplest explanation for this observation
is that the vestibular system provides tonic drive to
spinally projecting neurons that inhibit phrenic and
abdominal motoneurons. In addition, modulation of
rectus abdominis activity during 60° nose-up tilts from
a prone position was significantly reduced after removal of vestibular inputs, indicating that the vestibular system provides phasic, posturally related influences on activity of this abdominal muscle in addition
to the tonic influences described above. It seems likely
that posturally related increases in abdominal muscle
activity that are elicited by vestibular inputs are produced through descending excitatory pathways. Thus
two bulbospinal projections may relay vestibular signals to rectus abdominis and perhaps other abdominal
motoneurons: an inhibitory pathway that receives
tonic vestibular drive that is unrelated to body position
in space and an excitatory pathway that is only activated when the animal assumes particular postures.
At present, the descending pathways that relay vestibular signals to respiratory motoneurons are largely
unknown. In decerebrate animals, large brain stem
lesions that either destroyed the dorsal and ventral
respiratory groups or removed the projections of respiratory group neurons to spinal motoneurons did not
abolish vestibular influences on diaphragm or abdominal muscle activity (22, 23, 29). Thus other pathways
must be largely responsible for mediating vestibulorespiratory responses. One possibility is bulbospinal pro-
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VESTIBULORESPIRATORY INFLUENCES IN AWAKE ANIMALS
We thank Drs. Robert Schor and Joseph Furman for comments on
a previous version of this manuscript. We are also grateful to Brian
Jian, Michael Holmes, Andrew Etzel, David Eisenberg, Sarah Graff,
and Aaron Bergsman for assistance with the completion of these
experiments.
This study was supported by National Institute on Deafness and
Other Communication Disorders Grants R01 DC-00693, R01 DC03732, and P01 DC-03417. Electronics support was provided through
National Eye Institute Core Grant EY-08098.
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activity of other abdominal muscles would not have
been altered by removal of peripheral vestibular inputs. Nevertheless, the present findings indicate that
the vestibular system tonically influences intra-abdominal pressure through effects on at least one abdominal muscle and in addition contributes to producing necessary alterations in intra-abdominal pressure
during some postural changes. Third, our diaphragm
recordings were limited to the costal portions of this
muscle, although previous studies have shown that
larger increases in activity occur in the crural than in
the costal diaphragm during nose-up tilts from a supine position (25). Thus more pronounced effects of tilt
on diaphragm firing might have been observed in the
present experiments if the crural region were studied.
Perspectives. The present data show that the vestibular system provides tonic inhibitory influences on the
activity of rectus abdominis and the diaphragm and in
addition contributes to eliciting increases in the activity of rectus abdominis during nose-up rotations from
the prone position. These observations demonstrate
that control of respiratory muscle activity in awake
animals is complex, in that sensory inputs in addition
to those traditionally considered to influence breathing
(such as those from chemoreceptors and pulmonary
receptors) participate in the regulatory process. Further studies will be required to elucidate how these
multiple sensory inputs interact in the adjustment of
respiratory muscle contractions.