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Coordinations of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs
J Morin, D Viala
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 Convergence of central respiratory and locomotor rhythms onto single neurons of the lateral reticular nucleus
Ezure K, Tanaka I  
Mechanical links between locomotion and breathing: can you breathe with your legs?
H Lee, R Banzett












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European J of Neurology
Involuntary stretching during yawning in patients with pyramidal tract lesions: further evidence for the existence of an independent emotional motor system
R. Topper, M. Mull, W. Nacimiento
Department of Neurology and Neuroradiology, Aachen Technical University,Germany


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Introduction : Yawning is a stereotyped behavioural pattern which begins with an inspiration associated with marked dilatation of the pharynx. At the peak of inspiration there are associated facial movements and the final part of yawning is passive expiration. Yawning is accompanied by lacrimation, salivation, and reflex vasoconstriction in the skin (Barbizet, 1958; Appenzeller, 1969). Ultrasound has revealed that yawning occurs even in fetuses in utero (Egerman and Emerson, 1996).
Not much is known about the function of yawning. Folk wisdom commonly associates yawning with drowsiness and boredom. The few scientific studies which have attempted to unravel the physiological function of yawning have not succeeded in formulating a convincing hypothesis. The popular opinion, that yawning is a respiratory manoeuvre to increase oxygenation and decrease C02 in the blood has not been verified in normal subjects. In an experimental setting the subject had either to breathe 100% 02 or a gas mixture with higher than normal levels of C02. In both conditions the frequency of yawning remained unchanged, which makes it unlikely that yawning serves any specific respiratory function (Provine et al., 1987). Others have argued that yawning may serve as a paralinguistic signal of drowsiness in man. An argument in support of this hypothesis is the fact that yawning is contagious. Seeing somebody yawning is a powerful stimulus to evoke a yawn in the observer. When analysing group behaviour ethnologists suggested that yawning may help to synchronize the physiological and behavioural state of a group (Eibl-Eibesfeld, 1975).
In humans and animals, yawning is often accompanied by generalized limb extension. In laboratory animals a variety of dopaminergic and cholinergic substances have been found that induce a stereotyped motor pattern which consists of yawning, stretching and penile erection (Dourish and Cooper, 1990). In humans yawning may occur without associated limb extension (Provine et al., 1987). An involuntary stretching of an otherwise plegic arm is, however, often observed in neurological patients, for example in patients with hemiplegia. Other reflexive associated movements, also known as synkinesias, have been observed in plegic limbs. These include raising of the arm and flexion of the thigh whilst sneezing or moving the arm during micturition (Walshe, 1923). The first detailed study of synkinesias came from the German neurologist Westphal (quoted in Zülch and Müller, 1969), who attributed the reflexive movement of the otherwise plegic arm to the action of the ipsilateral, uncrossed pyramidal tract. Whilst other types of synkinesias, such as mirror movements, received some attention in the neurological literature (Zülch and Müller, 1969), associated movements during yawning have only rarely been described. There are a few case reports of stroke patients who experienced stretching of the arm whilst yawning (Bauer et al., 1980; Wimalaratna and Capildeo, 1988;Blin et al., 1994), but according to one report this phenomenon might be rather common: in this study 31 of 40 patients questioned reported that their plegic arm moved during yawning (Mulley, 1982). The anatomical pathways which underlie this involuntary motor response have, however, yet to be clarified. We report three patients with radiologically characterized lesions at différent levels of the pyramidal tracts who experienced involuntary movements of the otherwise plegic arm, during yawning.
Case reports
Patient 1 : A 62-year-old patient was admitted with a left sided hemiparesis and a hemianopia to the left. A brain CT obtained on admission revealed an infarction in the right posterior artery territory and early signs of an extensive infarction in the territory of the right middle cerebral artery. Consecutive CT scans obtained over the following days showed an extensive swelling of the ischaemic brain tissue with a shift of midline structures to the left. The ischaemic oedema did not respond to vigorous medical therapy including hyperventilation and osmotherapy. An extensive craniotomy was therefore performed 6 days following the onset of symptoms. After 12 days of artificial ventilation the tracheal tube was removed. A CT scan at that time revealed a complete infarction of brain tissue in the territory of the right middle cerebral artery. On neurological examination the patient had a complete left sided hemianopia and a left-sided spatial neglect. There was a complete left-sided hemiplegia with increased muscle tone, exaggerated reflexes and a positive Babinski sign on the left. During ward rounds the patient reported spontaneous movements of his left arm during yawning. Due to the severity of his spatial neglect the associated movements of his left arin gave hiin a rather strange feeling, especially when his left arm becarne visible for him on the right side of his body.
Patient 2 : A 51-year-old man was admitted to the neurology department because of a dense hemiparesis of his right arm and leg with sudden onset during physical exercise. His medical history was remarkable for uncontrolled arterial hypertension. On neurological examination the patient was alert and orientated. He had a central facial paresis and a complete right sided hemiplegia. The speech was dysarthric, but there was no aphasia. A brain CT scan obtained on the day of admission showed a haemorrhage centred in the left thalamus which extended into the posterior portion of the internal capsule. The diagnosis of a hypertensive intracerebral haemorrhage was made. A neurosurgical intervention was discussed but it was decided to treat the patient conservatively. Approximately 2 weeks after the stroke a neurology resident observed involuntary movements of the patient's plegic arm during yawning. These movements consisted of a tonic abduction of the arm at the shoulder and an extension of the forearm and the fingers. The appearance of these associated movements was consecutive with the appearance of spastic muscle tone.
Patient 3 : The last patient described in this report was a 43-year old man who was admitted with a basilar artery thrombosis. He presented with increasing clouding of consciousness, anisokoric pupils, restricted extraocular movements of both eyes and a left sided hemiplegia. An initial brain CT was normal. An emergency cerebral angiography revealed a thrombotic occlusion of the basilar artery in its upper portion. Intra-arterial application of 90 mg rtPA achieved an almost complete recanalization of the basilar artery. After completion of the thrombolytic therapy the patient remained on artificial ventilation for the next 24 h. Following extubation the neurological examination revealed a bilateral gaze evoked nystagmus, dysarthria, a complete left sided hemiplegia and sensory disturbances of the left side of the body. A cranial MRI obtained 14 days after basilar artery occlusion showed a circumscribed right sided lesion in the middle portion of the pons extending to the cerebellar peduncle (Fig). As soon as 4 days after the stroke a nurse on the neurological intensive care unit noted spontaneous movements of his plegic left arm during yawning. This observation could be confirmed by the patient who noted an abduction and extension of his left arm every time he yawned. When he imitated a yawn no associated movements could be observed.
Associated movements of the plegic arm during yawning were found in three patients with pyramidal tract lesions at the level of the motor cortex, the internal capsule and the pons. The recovery of movements after a pyramidal tract lesion is characterized by an initial phase of flaccid paresis which is followed by the reappearence of tendon reflexes as well by the appearence of pathological reflexes such as the Babinski sign and exaggerated flexor reflexes. Synkinesias such as stretching of the arm whilst yawning typically appear at this stage of the recovery process, before the reappearance of voluntary limb movements. From these observation it may be concluded that stretching during yawning is an automatic motor pattern that is usually inhibited in the presence of intact corticobulbar fibres in man. When the corticobulbar systems have been injured this automatic motor pattern appears in a stereotyped fashion.
So far there have been no convincing hypotheses concerning the anatomical pathways which are responsible for the involuntary movements of the arms in the absence of a functional pyramidal tract. In recent years yawning has gained increasing recognition from behavioural neuroscientists studying the effects of dopaminergic and cholinergic drugs on the rodent brain. In animals the yawning response to the dopamimetic apomorphine is considered a behavioural consequence of the stimulation of dopaminergic receptors in the basal ganglia, as experimental basal gangha lesions are known to abolish apomorphin-induced yawning (Dourish and Cooper, 1990). The associated movements of the extremities during yawning in man following lesions of the corticospinal tract have therefore been attributed to an activation of otherwise inhibited basal ganglia projections onto brain stem motor centres (Blin et al., 1994). An intact basal ganglia projection to the brain stem is not, however, a prerequisite for yawning with associated stretches in man. Yawning with associated movements of the extremities has been observed in locked-in patients following bilateral midbrain infarction (Karp and Hurtig, 1974; Bauer et al., 1980). In an infant born with an arhinencephalic brain yawning was also prescrit demonstrating that yawning is possible in the absence of basal ganglia structures (Gamper, 1926).
There are reports of patients which indicate that yawning is integrated in the lower brain stem. A patient with an extensive glioma in the anterior part of the pons developed a locked-in syndrome including complete paralysis of all facial muscles. Reflexive yawning with typical innervation of facial and laryngeal muscle was observed which was not, however, accompanied by reflexive stretching of the arm. (Gschwend, 1977). The anatomical substrate of the 'cerebral yawning centre' is most likely to be located in the caudal medulla, where neurones regulate respiratory activities via their projections to muscles involved in respiration. In the cat cells in the lateral reticular nucleus in the lower medulla adjacent to the ventral respiratory group have been found to have both central respiratory and locomotor rhythms (Ezure and Tanaka, 1997). These cells, if present in man, might be the anatomical basis for associated stretching during yawning.
It has been suggested that yawning represents an integrated discharge of the bulbar reticular formation corresponding to a particular level of activity of the reticular formation (Barbizet, 1958). Following this line of arguments yawning could be considered as the somatomotor manifestation of a particular emotional state characterized by disinterest and sleepiness, just as laughing is the somatomotor manifestation of mirth. Both have a distinct psychosocial significance in indicating either boredom or joy to others. From clinical observation it can be deduced that the integrated discharge of the brain stem neurones responsible for the stereotyped behavioural pattern, which corresponds to a particular emotional state, leads to an activation of bulbar and spinal motor neurones independent of the pyramidal tract input necessary for a voluntary activation of the respective muscles. Patients with lesions of the pyramidal tract at various levels who have a facial palsy or a paralysed arm may show an involuntary innervation of the face during laughing (Monrad-Krohn, 1924; Hopf et al., 1992; Tôpper et al., 1995; Waxman, 1996) or an involuntary stretching during yawning. Holtstege has recently introduced the term 'emotional motor system' into clinical neuroscience (Holtstege, 1991; Holtstege et al., 1996).
This concept implies that descending fibre tracts within the brain stem, completely distinct from those forming the somatomotor system, are involved in the elaboration of emotional behaviour. Our observations of movements of an otherwise plegic limb supports the concept of an independent emotional motor system. Careful clinical observation combined with high resolution brain imaging in patients with circumscribed brain lesions is therefore a suitable tool to study the somatomotor components of emotions, a task which is difficult to perform in laboratory animals.
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