Ventilation, arterial pressure, and cardiac
frequency increase immediately with the onset of
exercise. The exact mechanisms controlling these
responses are still debated despite over a
century of investigation (Volkman, 1841).
Central command and feedback from contracting
muscles have both been proposed as providing the
neural drive to, the respiratory and
cardiovascular systems during exercise
(Mitchell, 1985; Dejours, 1964).
Several investigators have provided
experimental evidence that a reflex originating
from mechanical or metabolic stimulation of
receptors within contracting skeletal muscles is
responsible for the autonomic responses to
exercise. This possible mechanism has been
studied in anesthetized animals by stimulating
motor nerves to induce muscular contraction.
This experimental maneuver elicits increases in
ventilation, cardiac frequency and arterial
pressure. McCloskey and Mitchell (1972) have
shown that group III and group IV afferent
fibers form the sensory pathway for this
reflex.
Central command originating in the
suprapontine brain provides drive to the
locomotor, respiratory, and cardiovascular
systems during exercise. This mechanism has been
studied by chemical and electrical stimulation
of the subthalamic locomotor region (SUR) in the
hypothalamus. Activation of neurons in this site
causes locomotion, increases respiration,
arterial pressure and cardiac frequency, and
produces an alteration of organ blood flows
similar to that measured during voluntary
exercise. These responses were shown not to be
dependent upon feedback from peripheral
receptors.
Ibe interaction between feedback mechanisms
and central command has not been investigated.
Each of these control mechanisms has been
studied separately. However, Yamamoto (1977) has
pointed out that for the control of exercise
hyperpnea you may have sufficient mechanisms;
each of which in a given, isolated circumstance
explains the whole phenomenon. When they act
simultaneously, they mask each other. Thus, he
suggested that neural occlusion is occurring
with the mechanisms controlling breathing during
exercise.
The purpose of this study was to investigate
possible interactions between central command
activated by STLR stimulation and the feedback
reflexes elicited by induced muscular
contractions. Our results suggest that the
central command mechanism predominates over the
feedback reflexes activated by hindlimb muscular
contraction in controlling breathing.
Discussion
Two different mechanisms thought to be
involved in controlling the cardiovascular and
respiratory systems during exercise were
examined in this study. Feedback from
contracting muscles was induced by stimulating
spinal ventral roots to cause static contraction
of hindlimb muscles. In agreement with other
studies, we observed significant increases in
respiration, arterial pressure and cardiac
frequency in response to this type of
contraction. The second mechanism investigated
was central command which was activated by
stimulation of the subthalamic locomotor region.
Eldridge et al (1981, 1985) have proposed
recently that neural output from this
hypothalamic site controls the locomotor,
respiratory and cardiovascular systems during
exercise.
Stimulation of the subthalamic locomotor
region in the decorticate cat, in very fightly
anesthetized cats or in cats anesthetized with
Althesin' elicits locomotor movements. However,
this locomotor activity is depressed by
anesthesia reported that stimulation of this
area with 50-300 µA does not evoke
locomotor activity in cats anesthetized with
chloralose and urethane. The same stimulation
parameters were utilized in the prescrit study
in which no locomotor movements were produced by
STLR stimulation. However, the cardiorespiratory
responses are elicited by this intensity of
stimulation in anesthetized cats. Thus, the
autonomic responses to stimulation of the
subthalamic locomotor region in this study were
not accompanied by complicating feedback from
contracting locomotor muscles.
In our study, induced muscular contraction
and STLR stimulation, when performed
individually, evoked similar increases in mean
arterial pressure (27.7 and 31.4 mm Hg,
respectively). However, SUR stimulation produced
significantly larger cardiac frequency and
respiratory responses than did muscular
contraction. Cardiac frequency and minute
phrenic activity rose 8% and 60%, respectively,
during muscular contraction as compared to a 13
% increase in cardiac frequency and a 142 %
increase in minute phrenic activity during STLR
stimulation. Ibese responses to STLR stimulation
are similar to those reported previously from
this laboratory (Waldrop et al., 1986).
Other studies have also reported large
pressor responses with only small changes in
breathing and cardiac frequency during static
muscular contraction induced by ventral root
stimulation in cats. For instance, Rodgers
(1968), Coote etal. (1971) and McCloskey and
Mitchell (1972) reported that muscular
contraction elicited a 50% or less increase in
ventilation. In the latter two studies, static
contraction of hindlimb muscles caused a 20-55
rnm Hg increase in arterial pressure with less
than 5 % increase in cardiac frequency. Thus,
reflexes activated by contracting muscles alone
do not evoke large increases in ventilation and
cardiac frequency. However, activation of
central command, ie., STLR stimulation, evokes
large increases in respiration, arterial
pressure and cardiac frequency.
Stimulation of the subthalamic locomotor
region combined with muscular contraction
yielded smaller increases in respiration,
arterial pressure and cardiac frequency than
would be predicted from summing the individual
responses alone. These results support
Yamamoto's (1977) hypothesis that occlusion of
the neural drives controlling the respiratory
and cardiovascular systems occurs during
exercise. Thus, the influence of central command
and reflexes eficited by muscular contraction,
when presented alone, probably differs from the
effect of each when activated simultaneously as
occurs during voluntary exercise.
As discussed above, the responses to
combined STLR stimulation and muscular
contraction were less than what would be
predicted from a simple addition of the
individual responses. "Mis occurred regardless
of the sequence in which the stimulations were
performed. However, the stimulation sequence
made a considerable difference in the magnitude
of the responses that occurred when the second
stimulus was applied. Ventral root stimulation
given during SUR conditioning stimulation had
only a negligible effect on respiration and
caused only small increases in cardiac frequency
and arterial pressure. In contrast, stimulation
of the subthalamic locomotor region during
muscular contraction elicited large increases in
all the recorded respiratory and cardiovascuIar
parameters. Thus, these results suggest that
STLR stimulation predominates over the reflex
activity occurring as a result of muscular
contraction.
Even though STLR stimulation evoked large
increases in phrenic nerve activity, arterial
pressure and cardiac frequency during muscular
contraction, these responses were smaller than
when the STLR was stimulated by itself. However,
the reduction in response for this sequence of
stimulation was much less than that observed
with ventral root stimulation during STLR
stimulation. When the subthalamic locomotor
region was stimulated during muscular
contraction, minute phrenic activity, arterial
pressure and cardiac frequency were 69, 49, and
70%, respectively of those changes seen with
stimulation of the STLR by itself. Thus, at
least for minute phrenic activity and cardiac
frequency, depressive effects of ventral root
stimulation upon central command were
minor.
Our results do not allow a determination of
the actual neurophysiological mechanism
responsible for the effects of SUR stimulation
upon the reflexes evoked by muscular
contraction. Presynaptic or postsynaptic
inhibition could have occurred at any of the
synapses between the primary afferent input to
and the motor outflow from. the spinal cord.
Since the respiratory frequency response to
muscular contraction was depressed during STLR
stimulation, at least part of the depressive
action must have taken place at the level of the
respiratory rhythm generator in the
brainstem.
An alternative explanation for the depressed
responses to muscular contraction during SUR
stimulation is that saturation occurred in the
involved neuronal circuitry. Thus input from the
subthalamic locomotor region and feedback from
the periphery would saturate neuronal elements
common to both. This possibility does not seem
likely for two reasons. First, SUR stimulation
and muscular contraction when performed alone
caused the same increase in respiratory output
in one cat in the present study. However, the
respiratory response to muscular contraction
during STLR stimulation was trivial compared to
the increase in minute phrenic activity which
occurred when the subthalamic locomotor region
was stimulated during muscular contraction.
Obviously, this reduced response to muscular
contraction during STLR stimulation cannot be
attributed to saturation of neuronal circuits in
this cat. In addition, Eldridge et aL (1982)
have shown that stimulation of hindlimb muscles
during either hypercapnia or carotid sinus nerve
stimulation produces the same increase in
phrenic nerve activity and arterial pressure as
that caused by hindlimb muscle stimulation by
itself during normocapnia. Thus, it appears more
likely that the subthalamic locomotor region
asserts a depressive effect on the reflex
activity elicited by muscular contraction.
The cardiac frequency and arterial pressure
responses to muscular contraction were not as
depressed during STLR stimulation as was
respiratory output. This difference can probably
be explained by spinal circuitry which can
generate reflex increases in cardiovascular
function. Several investigators have reported
increases in arterial pressure and cardiac
frequency in response to afferent stimuli in
spinalized cats (Brooks, 1933;
Staszewska-Barczak and Dusting, 1977; Waldrop et
aL, 1984). Furthermore, it has recently been
shown that a pressor response to muscular
contraction persists after spinal (C- 1)
transection (Iwamoto et aL, 1985).
In summary, our results from anesthetized
cats demonstrate that central command and
reflexes evoked by ventral root induced muscular
contraction exert smaller respiratory and
cardiovascular effects when activated
simultaneously than when activated individually.
In addition, central command as activated by
stimulation of the subthalamic locomotor region
has a predominant effect over the responses
caused by muscular contraction.
Abercrombie
J, Gendrin A Des maladies de
l'encéphale et de la moelle
épinière Germer-Baillière
1835
Abercrombie
J Yawning and apoplexy Medical Times and
Gazette 1863;1:656-661
Bauer G. et al
Involuntary motor phenomena in the locked in
syndrome J Neurology 1980;223;:91-198
Bertolotti
M. Etude sur la pandiculation automatique
des hémiplégiques Rev Neurol
1905;2(19): 953-959
de
Buck Classification des mouvements anormaux
associés à
l'hémiplégie Rev Neurol
1899;6:361-365
Furtado D.
Provocation spinale d'un réflexe de
bâillement. Rev d'oto neuro
ophtalmologie.1951;23(1):
Ghika
J., Bogousslavsky J. Dissociated
preservation of automatic-voluntary jaw
movements in a patient with biopercular and
unilateral pontine infarcts Eur Neurol
2003;50:185-188
Heusner A P
Yawning and associated phenomena Physiological
Review 1946;25:156-168
Lanari A.,
Delbono O. The yawning and stretching sign
in hemiplegics Medicina (B Aires)
1983;43(3):355-35
Liecey Nouvelle
observation de bâillement convulsif
périodique Le Courrier Médical
1879;29;334-336
Liégey Deux
observations de bâillements intermittents
Gazette médicale de Strasbourg 1851;
p118-119
Louwerse E
Forced yawning as a pseudobulbar sign in
amyotrophic lateral sclerosis J Neuroscience
Research 1998, sup, 392
Mulley G.
Assoctiated reactions in the hemiplegic arm
Scand J Rehab Med 1982;14:117-120
Ogle
JW. Arm rising during yawning The Medical
Times and Gazette. 28 february 1863 p 213
Pierre
Marie La Pratique Neurologique
Hémiplégie, mouvements
associés Masson 1911, p477-480
Pierre
Marie et Léri A. Mouvements
involontaires dans les membres paralysés
1911 Nouveau Traité de médecine et
de thérapeutique Brouardel, Gilbert,
Thoinot JB Baillière Ed 1911
p283-291
Quoirin E.
Elévation involontaire du membre
supérieur chez
l'hémiplégique lors d'un
bâillement Thèse doctorat en
médecine Poitiers 2002
Thomson HC
Associated movements in hemiplegia : their
origin and physiological significance Brain
1903;26:515-523
Töpper
R, Mull M, Nacimento W Involuntary
stretching during yawning in patients with
pyramidal tract lesions: further evidence for
the existence of an independent emotional motor
system European J Neurology 2003;10:495-499
Trautmann R. Le
bâillement Thèse Bordeaux; 1901-02;
N° 40; 86 pages
Vulpian
A Leçons sur la physiologie
générale et comparée du
système nerveux faites au Museum
d'histoire naturelle. Rédigées par
E.Brémond. Paris, Baillière,
1866
Vulpian
A Maladies du système nerveux Paris,
Doin, 1879
Walshe FMR
On certain tonic or postural reflexes in
hemiplegia with special reference to the so
called "associated movements". Brain,
1923;46:1-37
Wimalaratna HS,
Capildeo R. Is yawning a brainstem
phenomenon ? a stroke patient who stretched his
hemiplegic arm during yawning Lancet
1988;1(8580):300 8580):300
