Sleep Medicine
Institute, Sheba Medical Centre (affiliated to
Sackler School of Medicine, Tel Aviv University)
and Department of Internal Medicine E, Asaf
Harofeh Medical Centre,
Israel
Case Report : Yawning is a
complex event that depends largely on the autoi
nomic nervous system. Microneurographic
techniques were used to study the mechanism
involved in yawning. A series of spontaneous
yawns displayed by a healthy 39-year-old male
offered us the opportunity to study the muscle
sympathetic nerve activity (MSNA) during this
phenomenon. It was found that 2 s of yawning
inhibited the MSNA recorded at the right
peroneal nerve in the lateral knee area, while 3
s of slow expiration succeeding a yawn provoked
an MSNA discharge. Blood pressure decreased with
each slow expiration by 5-6 mmHg, and increased
again with the renewed MSNA discharge. We
conclude that yawning is associated with a
sympathetic suppression that favours a
parasympathetic dominance, as indicated by the
MSNA and the decrease in blood pressure. The
slow expiration following a yawn is associated
with a sympathetic activation marked by an MSNA
discharge and an increase in blood pressure.
Introduction : Yawning involves a
spontaneous and involuntary wide opening of the
mouth and a widening of the jaw, together with a
long, deep inhalation through the mouth and nose
followed by a slow expiration associated with a
feeling of comfort.
The complex neuronal reflex system of yawning
appears te, be located in a reticular brainstem
system closely related through the
diencephalo-hypothalamic network with large
associative cortical areas. In animals it
subserves behaviour related to stressful
situations, and in humans behaviour related to
fatigue and boredom, suggesting an arousal
defence reflex. It is well known that lung
inflation can inhibit sympathetic outflow to
limb vessels, se, that most of the sympathetic
outflow to skeletal muscles takes place at the
end of expiration or early during inspiration,
but is inhibited by the peak of inspiration.
In this article we offer a new insight into
the mechanism of yawning, which as fat as we
know has not previously been studied by the
microneurographic technique. During a
microneurographic examination of the sympathetic
nervous system, the appearance of spontaneous
repeated yawning in a healthy control subject
has made it possible to demonstrate the
involvement of the autonomic nervous system in
yawning.
Subject and methods : The subject was
a healthy 39-year-old male volunteer who
displayed "repetitive yawning". A tungsten
microelectrode with a lip diameter of 2 µm
and a resistance of 1-10 meg was inserted,
without sedation, into the right peroneal nerve
in the lateral knee area of the subject as he
lay supine. The sympathetic axon fascicles were
detected by delicate manipulation based on
acoustic and visual techniques. The sympathetic
output, filtered by a DAM50 differential
amplifier (World Precision Instruments,
Saratoga, FL, USA), gain 60 dB, passed through a
Neurogram amplifier/integrator and noise
rejector (Nagoya University, Japan). The
resulting sympathetic signal, together with the
blood pressure (BP) and pulse rate (recorded
through a Finapres Ohmeda 2300, BOC Heaith Care,
Louisville, CO, USA), were displayed on a Nihon
Kohden thermal array recorder (Tokyo,Japan).
Results : A microneurographic
recording of the volunteer is presented. Muscle
sympathetic nerve activity (MSNA), BP and pulse
rate were recorded and evaluated during a series
of 33 spontaneous yawns lasting 5-7 s each,
uttered by the subject as he lay supine. Two
seconds of yawning were enough to suppress MSNA,
while expiration provoked an MSNA discharge.
With each yawn and MSNA suppression, the
systolic and diastolic BP decreased, after a
delay of 5 s. By increasing the MSNA, each
expiration increased the BP, after a shorter
delay of only 3 s. The mean decrease in the
systolic and diastolic BP was 5-8 mmHg. Figure 1
shows MSNA, BP and pulse behaviour during
regular breathing, VàIsa1va~s manoeuvre,
forced breathing and repeated yawning. The heart
beat was not significantly affected by the
variations in MSNA or BP, but a tendency to
bradycardia during yawning was observed. Yawning
provoked changes similar to those of forced
breathing, while normal breathing and Valsalva~s
manoeuvre did not.
Discussion : The similarities between
forced breathing and yawning in this case study
offer a possible explanation for the fact that 2
s of yawning inhibit MSNA, while 3 s of slow
expiration provoke an MSNA discharge. During the
deep inhalation associated with yawning, the
efferent sympathetic nerve traffic is blocked
and the autonomic nervous system moves to
parasympathetic activity, which is
simultaneously stimulated by the pulmonary vagal
afférents. The associated changes in BE
which are synchronized with each yawn and
consist of a reduction of 5-6 mmHg of the
systolic and diastolic arterial pressure, seem
to be the direct consequence of the sympathetic
outflow suppression. It may be suggested that
the decreased BP excites baroreceptors,
principally those of the carotid sinus
afférents (through the glossopharingeus)
and of the aortic arch (through the vagus). Once
the stimuli have reached the tractus nucleus
solitaris, the sympathetic ganglions enter a
state of excitation which is expressed by MSNA
discharges appearing 3 s after yawn cessation.
Such a mechanism would explain why the BP rises
by 5-6 mmHg until the next yawn or forced
inspiration starts. The variation in heart rate
observed during yawning and forced breathing was
not significant, but as a consequence of the
vagal effect of yawning there is a tendency for
the heart beat to decrease. These variations are
not synchronized with the BP. The MSNA
discharges blocked by yawning may explain the
association with the peripheral vasodilatation,
pende erection and increased peristalsis that
have been described in animals and humans as the
result of a cholinergic dominance. This case
study offers an explanation for the mechanism by
which vaso-vagal syncope appears in the wake of
repeated or prolonged yawning.
Conclusion : Yawning is a complex
event that involves an extensive network of
neurons and interneurons and a large number of
neurotransmitters. Although our study deals with
only one subject, the findings were so regular
and consistent throughout a long series of yawns
that we believe them to demonstrate the
involvement of the autonomic nervous system in
the yawning process: a parasympathetic response
to yawning itself, and a sympathetic reaction to
the slow expiration that succeeds it.
Askenasy
JJM. Is yawning an arousal defense reflex? J
Psychol 1989; 321: 609-621.
Ferrari
F, Pelloni F, Giuliani D. Behavioural evidence
that different neurochernical mechanisms underly
stretching, yawning and penil erection induced
in male rats by SND 919, a new selective D2
dopamine receptor agonist. Psychopharmacol
(Bertin) 1993, 311: 172-176.
Aloe F. Yawning. Arq
Neuropsiquiatr 1994; 52: 273.
Shepherd JT. The lungs as receptor sites for
cardiovascular regulation. Circulation 1981; 63:
1-10.
Eckberg DL, Nerhed C, Wallin BG. Respiratory
modulation of muscle sympathetic and vagal
cardiac outflow in man. J Physiol (Lond) 1985;
365: 181-196.
Melis
MR, Mauri A, Argiolas A. Apomorphine- and
oxytocin induced penile erection and yawning in
intact and castrated male rats: effect of sexual
steroids. Neuroendocrinol 1994; 59:
349-354.
Urba-Holmgren
R, Santos A, Holmgren B, Eguibar JR. Two
inbred rat sublines that differ in spontaneous
yawning behavior also differ in their responses
to cholinergic and dopaminergic drugs. Behav
Brain Res 1993; 56: 155-159.
Melis
MR, Stancampiano R, Argiolas A. Hippocampal
oxytocin mediates apornorphine-induced penile
erection and yawning. Pharmacol Biochem Behav
1992; 42: 61-66.
Cronin TG
Yawning : en early manifestation of vasovagal
reflex AJR, 150, January, p209, 1988
Figure 1. Muscle sympathetic nerve activity
(MSNA), blood pressure (BP) and pulse during (A)
regular breathing, (B) VaIsalva's manoeuvre, (C)
forced breathing and (D) repeated yawning. In
normal breathing, random MSNA activity is
associated with a relatively stabilized BP and
heart beat. In Valsalva's manoeuvre, the sudden
drop in BP is associated with a sustained MSNA
activity. During yawning and in forced
breathing, there is a rhythmic inhibition of
MSNA with each inspiration, associated with a
drop in BP, and a rhythmic MSNA activation with
each expiration, associated with an increase in
BP. E, expiration; 1, inspiration; Y,
yawning
Correspondence and reprint requests: Dr
J.J.M. Askenasy, Sleep Medicine Institure, Sheba
Medical Centre, Tel Hashomer 52621, Israel. Tel:
(+972) 3 530 3219. Fax: (+972) 3 534
9368
