Introduction : We observed a
stroke patient who stretched his herniplegic
arm during spontaneous yawning. The question
thus arises of the putative mechanisms by
which yawning can induce the
hemipandiculation (paradoxical motor response
of the plegic arm in the patient), given the
large infarct of the internal capsule
interrupting the pyramidal tract noted in
this patient.
Case report : A 62-year-old man
was admitted with acute onset of pure motor
hemiplegia of the right side secondary to an
infarction in the left posterior limb of the
internal capsule. Power in upper and lower
limbs was 0/5 and 3/5, respectively. A few
days after the stroke, the patient noticed
that he involuntarily stretched his
hemiplegic arm when yawning. The movement
consisted of a slow, progressive abduction,
anteroflexion and internal rotation of the
shoulder lifting the arm from the bed. It was
associated with a mild flexion of the elbow
and extension of the three first fingers.
There was also a slight extension of the
right leg. Six weeks later the patient said
that the movement was still noticeable. There
was no recovery of the hemiplegia. No arm
movement was possible after voluntary effort
or in any other condition, except, according
to the patient, when yawning. The averall
frequency of spontaneous yawning was low and
normal. Repeated attempts to induce yawning
by imitation were unsuccessful. Voluntary
mouth movement mimicking yawning could not
induce any movement of the arm.
Since we previously demonstrated that low
doses of apomorphine induces yawning in
healthy volunteers (Blin et ai. 1990) and
patients (Blin et al. 1991) without any
discomfort, we used this pharmacological
method to further analyse the observed
paradoxical motor response in our patient.
The patient gave informed consent after the
aim and nature of the study had been
explained to him. Apomorphine (5 µg/kg)
was injected subcutaneously, the patient
being in a lying position. No
apornorphine-induced erection or other side
effects were noticed. Apomorphine induced
about fifteen repeated yawns within 20 min.
Each yawn induced a stereotyped movement of
the hemiplegic arm, as just described. A
videotape recording was made to further
analyse the apomorphine-induced responses. It
showed that the mouth was symmetrical during
yawning, that the arm movernent occurred a
few seconds after the yawning began and
lasted 5-10 sec after cessation. Again, no
voluntary control of the movement was
possible and no other type of visible
movement was detected, particularly on the
contralateral side. However, surface
electromyogram was not performed and one
cannot exclude the hypothesis of bilateral
activity, suppressed on the contralateral
side by the contraction of antagonist
muscles.
Discussion : These data are
consistent with a previous report from
Wimalaratna and Capildeo (1988), although
these authors did not directly observe the
involuntary movement because the patient did
not yawn in the presence of investigators.
Oman (1989) published a similar observation,
and Mulley (1982) reported that 31 of the 40
hemiplegic patients he questioned noticed
that their plegic arm moved during yawning,
Therefore, it is likely that our observation
could be rather common although rarely
described in the litterature. The release of
lower brain structures from the inhibitory
influence exerted by the cerebral cortex over
subcortical structures is classically
suggested to explain some types of abnormal
increases in reflex activity occurring in
decorticated monkeys and plegic patients.
Among these subcortical structures, the basal
ganglia play a key rote in controlling motor
activity. The internal capsule infarct may
thus be considered to suppress inhibitory
cortical influences over striatal areas in
our patient, leading in tum to a release of
the striatal inhibitory tone over
somatosensory response effectors.
The functional efficiency of a motor
pathway arising from the basal ganglia to
lower motor systems in the brainstem must be
considered in man. Such pathways projecting
to the pontine nuclear or reticular nuclei
and spinal motoneurons exist in the cat
(Labuzewski and Lidsky 1984). The substantia
nigra pars reticulata, which is primarily
known to project to the thalamus, also sends
descending projections to motor structures
such as the superior colliculus (Illing and
Graybiel 1985) and the tegmental
pedunculo-pontine nucleus (Beckstead et all
79). The superior colliculus sends efferents
to the spinal cord and brainstem reticular
formation and the pedunculo-pontine nucleus
sends a striat projection to the medial
medullary reticular formation, which is known
ultimately to influence alpha motor neuron
firing (Graybiel 1984). Finally the brainstem
outflow from the basal ganglia is probably
relatively small in man. It exists however
and may play a functional rote at least in
certain circumstances such as the
interruption of the pyramidal tract or
extrapyramidal disorders. In the same manner,
the interconnection of this reticular
brainstem formation, close to the ascendant
activatory reticular system, with motor
pathways might explain, in locked-in
syndrome, the paradoxical activation of
facial, lingual, jaw or breathing muscles
with either emotional stimuli (through
pre-frontal area and limbic system) or
yawning (for a review see Askenasy
1990).
It is thus possible to suggest that basal
ganglia influence cranial motor centers not
only through cortical relays but also through
reticular mechanisms. The yawning response to
apomorphine is a motor behavior related to
the stimulation of the dopaminergic receptors
in the basal ganglia. In animals,
neuroleptics and experimental lesions of the
basal ganglia suppress apomorphine-induced
yawning (cf. Blin et al. (1991). Dopaminergic
transmission could stimulate yawning
mechanisms in the basal ganglia and,
secondarily through this relay, increase the
excitability of cranial motor nerves. Such an
activation of subcortical reflex centers
would not only concern bulbar centers (mouth
opening, eyes closing) but would also involve
more general motor nuclei controlling arm
motility. The apomorphine test we used in our
observation must be considered only as a
pharmacological tool to induce yawning. No
direct relationship can be claimed between
the stimulation of the dopaminergic receptors
and the arm movement, because such a movement
occurred also during spontaneous yawning. The
arm movement described in our patient may
thus be considered to be concomitant of
rather than consecutive to yawning.
The arm stretching elicited by yawning in
our hemiplegic patient might represent a
postural adjustment to changes in neck
muscular receptor activity or labyrinthine
stimulation induced by slight head movements
associated with yawning. Indeed, previous
reports have suggested alterations in posture
of plegic arms produced by neck reflexes
(Walshed 1923). However, in our case,
simulating a yawn or passive movements of the
head and neck had no effect on plegic arm
extension. Nevertheless, the working
hypothesis, should be investigated and is of
heuristic value for further experimental
analysis of phenomenon.
Is yawning a
brainstem phenomenon ? Wimalaratana HS,
Capildeo R. A stroke patient who stretched
his hemiplegic arm during yawning
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