Yawning is a phylogenetically ancient
phenomenon coordinated by a network of
supratentorial and infratentorial centres
located in brainstem, hypothalamus, and limbic
regions [1]. Movements of plegic limbs
during yawning in patients with stroke are
common [2]. The first descriptions come
from the 18th and 19th centuries by Darwin and
by Abercrombie, respectively [3, 4].
These movements have always been described as
involuntary and stereotyped, however
[5]. We report a novel phenomenon: a
stroke patient who could voluntarily control the
movements of his plegic limb during
yawning.
A 59-year-old right-handed male was admitted
in the emergency department presenting right
facial palsy, dysarthria, right hemiplegia, and
right pain anesthesia of sudden onset. The
relevant medical antecedents were diabetes
mellitus and arterial hypertension. The
presentation suggested a sensorimotor lacunar
syndrome due to a subcortical stroke. The
diagnosis of acute left Middle Cerebral Artery
infarct was made and he was submitted to
endovenous thrombolysis. The inferior limb
deficit improved; however, the right superior
limb remained plegic&emdash;grade 0 (MRC scale)
in all segments, including abduction/adduction,
flexion/extension, and medial/lateral rotation
of the shoulder and flexion/extension and
supination/pronation of the elbow. The only
exception was the elevation of the shoulder, in
which the patient could perform a full range of
motion if the force gravity was eliminated
(grade 2).
Since the first hours of stroke onset, the
patient presented a reflexive, stereotyped
movement of flexion of the right elbow while
yawing. Remarkably, at day 6, the patient
started to have voluntary control over that
movement. Ability to touch the chin or the left
arm with the right hand according to the request
of the observer was documented (Online Resource
1). The patient noticed an association between
the duration of yawning and the range of
movements that he was able to do, such that
during more sustained yawning, he could even
perform more complex movements of distal
joints&emdash;grabbing objects purposely, for
instance. These movements could also be
volitionally suppressed. They were impossible
without yawning or when he simulated yawning. He
did not notice an increase in the frequency of
yawning, fatigue of the movement during multiple
episodes of yawning, and his limb was not
spastic.
MRI showed an infarct involving lenticular
nucleus, anterior and posterior limbs of
internal capsule, body of caudate nucleus, and
corona radiata (Fig. 1a).
Tractography and transcranial magnetic
stimulation confirmed the disruption on the left
pyramidal tract (Fig. 2).
The topography of his lesion was compared to
controls. The controls were selected
prospectively and had: (a) an acute ischemic
lesion on brain MRI of the left
lenticulocapsulo-radiate region; (b) an upper
limb paresis ² 2; (c) yawned during admission.
Of the four controls selected, two did not
present any movement during yawning and two
presented involuntary movements
exclusively.
Brain images were normalized to MNI152
space. The volume of lesion of the case was 8461
mm3 and that of the controls ranged from 3747 to
9858 mm3. The overlay of lesions of case and
controls showed that some areas of the anterior
limb of internal capsule, and of the anterior,
posterior, and inferior regions of putamen were
infarcted only in the described case, while some
areas of the posterior limb of the internal
capsule were lesioned in all controls but not in
the case (Fig. 1b). The results were similar
when controlling for patients with involuntary
movements exclusively.
Disconnectome maps were created using BCB
toolkit [6, 7]. Subtraction of the sum
of disconnectome maps of controls from the
disconnectome map of the case revealed two main
areas of disconnection only present in the case:
(a) gyrus rectus and middle orbitofrontal gyrus;
(b) lateral orbitofrontal gyrus and frontal
inferior gyrus pars triangularis (Fig. 1c).
Controlling only for patients with exclusively
involuntary movements revealed an additional
cluster of disconnection in the temporal
lobe.
We speculate that increased brainstem
monoaminergic activation associated with yawn
can permit movements, otherwise absent due to
the corticospinal tract lesion. The putative
change in the function of putamen as an element
of basal ganglia motor circuits secondary to the
lesion or to the disconnection to the
ventromedial prefrontal cortex, and the
disconnection to inhibitory areas, such as
ventrolateral prefrontal cortex, observed in the
described case, can be responsible for the
volitional control [8, 9]. We believe
that this first description can contribute to
the identification of other similar cases.
Although the use of dopaminergic medications has
not been effective in motor rehabilitation after
stroke, their specific use in similar cases
might be promising [10]. Further studies
with possible new cases and controlling for a
higher number of patients with exclusively
involuntary movements during yawning can
contribute to a better understanding of the
underlying physiopathology of this paradoxical
phenomenon.
References
1. Krestel H, Bassetti CL, Walusinski O
(2018) Yawning, its anatomy, chemistry, role,
and pathological considerations. Prog
Neurobiol.
6. Thiebaut De Schotten M, Dell'Acqua F,
Ratiu P et al (2015) From Phineas Gage and
monsieur Leborgne to H.M.: revisiting
disconnection syndromes. Cereb Cortex
25:4812&endash;4827
7. Foulon C, Cerliani L, Kinkingnehun S et
al (2017) Advanced lesion symptom mapping
analyses and implementation as BCBtoolkit.
bioRxiv.
8. Leung H-C, Cai W (2007) Common and
differential ventrolateral prefrontal activity
during inhibition of hand and eye movements. J
Neurosci 27:9893&endash;9900
9. Leisman G, Braun-Benjamin O, Melillo R
(2014) Cognitive-motor interactions of the basal
ganglia in development. Front Syst Neurosci
8:1-18
10. Ford G, Bhakta B, Cozens A et al (2015)
DARS (dopamine augmented rehabilitation in
stroke): longer-term results for a randomised
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routine occupational and physical therapy after
stroke. Abstracts of the UK Stroke Forum 2015.
Int J Stroke 10(Suppl. 5):6
Le bras
droit paralysé amène
volontairement la main sur l'épaule
gauche pendant le
bâillement
Les auteurs rapporte un nouveau cas de
parakinéise brachiale oscitante avec une
particularité notable, la capacité
acquise par le malade de mobiliser son bras
paralysé au cours d'un bâillement,
vers un but volontairement choisi.
Ce malade de 59 ans, diabètique et
hypertendu, se présente aux urgenecs
atteint d'une hémiplégie droite
avec paralysie faciale centrale et dysarthrie,
et insensiblilité de l'hémicorps
lors de l'installation du trouble. L'imagerie
cérébrale confirme un infactus
sous cortical secondaire à une occlusion
de l'artère cérébrale
moyenne, pour laquelle il a reçu un
traitement thrombolytique.
Secondairement la paralysie du membre
inférieur a régressé mais
pas celle du bras qui demeure totalement
paralysé. Depuis les premières
heures de l'attaque, le patient a
remarqué que son bras effectuait un
mouvement stéréotypé lors
de chaque bâillement, à type de
flexion du coude et élévation de
la main vers la bouche. D'une manière
originale, le patient s'est aperçu au
sixième jour de sa maladie que, par sa
volonté, il pouvait modifier la
trajectoire du mouvement du bras paralysé
(voir la vidéo) lui permettant de toucher
soit son menton, soit l'épaule gauche
avec sa main droite et ce, à la demande
explicite de son médecin.
L'IRM et la tractographie ont montré
une interruption de la voie pyramidale
[3] Blin
O, Rascol O, AzulayJ, Serratrice G, Nieoullon
A. A single report of hemiplegic arm
stretching related to yawning: further
investigation using apomorphine administration.
J Neurol Sci 1994;126(2):225-7.
[41 Topper
R, Mull M, Nacimiento W. Involuntary
stretching during yawning in patients with
pyramidal tract lesions: further evidence for
the existence of an independent emotional motor
system. Eur J Neurol 2003;10(5): 495-9.
