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6 décembre 2001
 J. Neurol.
Involuntary Motor Phenomena in the Locked-In Syndrome
G. Bauer, F. Gerstenbrand, and W. Hengl
Universitätsklinik für Neurologie, Innsbruck, Austria
Stimulus evoked oral automatisms in the Locked-in syndrome


Yawning and stroke

The locked-in syndrome (LIS) denotes a neurological condition due to bilateral transsection of pyramidal tracts at the level of pons or cerebral peduncles leading to complete immobility, except for vertical gaze. The syndrome shows several varieties in terms of the symptoms and course, the subject of a previous paper .

In locked-in patients a number of movements had been observed that were incompatible with the extent of voluntary paralysis. Since the LIS represents a unique natural transsection experiment with preserved consciousness, the investigation of those motor phenomena promised some insight in the organization and localization of nonpyramidal motor systems. The present paper gives a description and list of these movements and outlines the possible explanations.

Case 6. S.A., a woman aged 67. During the acute phase of the nearly classical LiS groaning was noted. It occurred spontaneously and also secondary to attempted verbal communication. Seven days after admission, yawning accompanied by typical generalized body stretching was noted. The observation was made while recording an EEG. The tracing was judged within normal limits, and cerebral electrical activity remained unchanged during the yawning. The patient's condition improved to an incomplete LIS. Ocular motility became free. some crude sounds could be uttered voluntarliv, and quadriplegla was also slightly improved. During this phase the patient exhibited compulsory munic reactions by far exceeding the extent of motions already possible by voluntary innervation. Those compulsory mimic reactions were frequently, but not invariably, accompanied by a penetratingly loud crying. Urging the patient to stop was never successful, and it never became clear whether the crying was secondary to external or internal distress. The next month crying was frequently repeated each day. The repetition seemed to follow an endogenous pattern linked with the well developed steep cycles. There were hours of regular crying at a rate of once or twice a minute. In clinical jargon we coined the terrn "cat crying" for this rather trouble some symptom. When paralysis of cranial nerve muscles further improved cat crying and eventually compulsory mimic reactions disappeared.


Normal motor functions are the result of an interaction of sensory input, of processing by integrative cortical areas, and of programing by the primary motor cortex. This program is carried out with the support of the extrapyramidal system, of the cerebellum, or primordial motor patterns built-in at different levels of the brain stem, and of reflexes mediated by the spinal cord. Under pathological conditions abnormal involuntary motor phenomena appear or normal movements occur in an uncontrolled autornatic fashion. The studies of those motor phenomena have brought remarkable insights in the organization of the motor svstem, occasionally marred by somewhat whimsical speculations about the biological goal of these patterns. However, motor phenomena might be divided into normal reactions, complex automatic behavior, and simple reflexes.

Normal reactions are variable and represent appropriate responses to the changing demands of the environment. Automatic motor patterns such as motorische Schablonen or motorische Primitivschablonen appear in a stereotyped fashion and are considered primordial behavior organized somewhere in the subcortical structures and released under pathological conditions by the lacking influence of cortical inhibiting systems. Therefore, automatic motor patterns have been observed in coma, in chronic vegetative state or apallic syndrome, in cases of bilateral supranuclear palsy [34], in cerebral malformations, and in normal inborns. The examination of' motor phenomena in high pyramidal transsections like the LIS can be of great value to disclose the localization of the so-called centers of such motor patterns. In LIS, it seems to be easy to differentiate involuntary motor phenomena from remnants of pyramidal movements. The conscious patients use the later ones for communication. However, most of the pathological patterns are stimulussensitive, and it might be hard to decide in a particular case, whether the move ments are secondary to. command or to nonspecific stimulation. Repeated examination and the consideration of the unvariable type of the pathological motor pattern may lead to the proper diagnosis.

Extensor spasms (decerebrate posturing) were frequently seen with the LIS (Table 1) and were in.variably stimulus-sensitive. Neck deflection was especially effective (case 2). Extensor spasms are identical with Jackson's cerebellar fits and are a constitutional sign of midbrain affection due to transtentorial hernation or functional dissolution down to the midbrain level due to metabolic or anoxic encephalopathies. Gamper showed both extensor and flexor spasms in the ancephalic midbrain. Since extensor spasms were also seen in localized brain stem lesions with intact cortical functions, the term decerebrate posturing is intrinsically fallacious. This statement is strongly supported by the observations in LIS. Extensor spasms disappear with dissolution of bulbar brain functions. These clinical observations suggest that extensor spasms are stimulus-sensitive-composed reflexes built-in within the bulbar brain and released by interruption of inhibiting pyramidal influences somewhere above the midbrain level. These limits were already established by the experimental work of Sherrington.The closer localization lies within the multisynaptic system of the brain stem intimately related to the ascending reticular activating system . A connection of the stretch reflex with a diffuse activating system in the brain stem was aiready suspected as early as 1926 by Gamper.

Flexor spasm (decorticate posturing) was rarely observed in LIS. Case 4 was an incomplete LIS with motor remnants of all four extremities. From the observations in transtentorial herniations one has to draw the conclusion that flexor spasms are integrated above the midbrain-diencephalic border. This might be the reason why it is exceptionally observed in LIS and only in the incomplete form.

Pain reactions, compulsory mimic reactions (Zwangsweinen) and compulsory screaming (cat crying) have been separately listed in Table 1, although these patterns cannot be distinguished by the mere description of the motor phenomenon. The pain reaction represents a normal phenomenon secondary to specific stimulation, abolished with certain depressed cerebral states and exaggerated with others. Compulsory mimic reactions occur with nonspecific stimulation and are frequently repeated. The differentiation from an exaggerated pain reaction may be impossible and meaningless in a practical as well as in a theoretical sense. Cat crying occurs spontaneously in an automatic repetition rate with an extremely pronounced vocal component. In LIS, pain reactions were seen in four cases of the presented series during the acute phase but were reported in literature only once. Its facial and vocal components are integrated in the periaqueductal gray. Its occurrence in LIS suggests that the pathways to the corresponding cranial nerve nuclei do not use the pyramidal tracts interrupted in LIS but instead a primordial motor system within the dorsal part of the brain stem.

There are several observations of compulsory mimic reactions (Zwangsweinen) in chronified LiS. It occurs spontaneously and in a rhythmic pattern like other cases of severe supranuclear palsy . Pathological crying is organized in the brain stem and usually appears in conjunction with bilateral pyramidal or extrapyramidal motor disorders . Laughing was never observed in LIS. Therefore, it has to be integrated in the rostal brain stem above the lesions leading to a LIS. This is in line with the findings in malformations. Cat crying may be separated from the vocal component of the pain or compulsory mimic reactions. It is crude and shrill like the screaming of prematures. Neumann described spontaneous and automatic screaming in children with tumors in the rostral brain stem. Sherrington and Catel and Krauspe suppose a primordial system for vocalization in the oral brain stem whose irritation or disinhibition might also be responsible for cat crying in LIS.

Yawning was also seen in LIS. Observations in the apallic syndrome, in cerebral malformations, in inborns and prematures, and in the early phases of transtentorial herniations make it likely that it is integrated in the lower brain stem, an area undisturbed by ventral pontine syndromes. Yawning also contains generalized body stretching resembling extensor spasms, and the whole sequence of behavior is finished by swallowing.Conncections with the sleep-inducing system, the arousal system, or the respiration center were conjectured.

The REM sleep and to a lesser degree, the NREM sleep is altered in LIS. The changed sleep pattern is not due to immobility such as that in high cervical lesions but to the direct involvement of the sleep-inducing system within the brain stem. REM sleep reduction was only seen with paralyzed horizontal gaze, whereas incomplete LIS with preserved lateral eye movements had comperatively undisturbed sleep cycles . These findings prompted the assumption that the paramedian pontine reticular formation known to be responsible for conjugate gaze movements at the pontine level might also be related to induction or priming the REM sleep. However, the relation of the sleep system to yawning remains unclarified.

Breathing is certainly affected in LIS. The pattern may be very regular (cases 1 and 3) resembling the central neurogenic hyperventilation or even ataxic (cases 4 and 5). Peiper considered the nervous structures for yawning to be part of the respiratory center, suppressed under normal circumstances, but activated or released with disturbed breathing. This conjecture cannot be confirmed or rejected by the findings in LIS.

Further motor phenomena like whining, moaning, groaning, chewing, and coughing were incidentally observed in LIS. With those phenomena, the differentiation to residues of voluntary motions is particularly difficult except for coughing which appeared clearly reflexlike to tracheal suction. Chewing or other oral automatisms were never seen in the cases reported and only once in the literature. In contrast, oral motor patterns reappear tirst in apallic patients and were fully developed in cerebral malformations. This contrast indicates an important difference between primary or prolonged and acute decerebrate or cerebrobulbar disconnection syndromes.

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