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Two muscles are involved in upper eyelid elevation: the tarsal smooth muscle of Müller that has an accessory role limited to the tonic control of eyelid position, and the levator palpabrae, a skeletal muscle innervated by a subdivision of the oculomotor nerve.1 The levator palpabrae shares several features with the superior rectus. Both muscles are often activated in conjunction, allowing for eyelid coordination during vertical eye movements, they have common embryological stages,2 and their motor neurons remain close to each other from the orbit to the mesencephalon. This anatomical parallelism persists at the nuclear level, at least in lateral eyed mammals. In these species, both levator palpabrae and superior rectus nuclei are paired and have crossing axons.1 However, in higher frontal eyed mammals, levator palpabrae innervation is provided by a single medial nucleus, the central caudal nucleus, although the crossed pattern of innervation of the superior rectus remains.3 Anatomical studies have shown that, in most frontal eyed mammals including primates, cell bodies of both levator palpabrae are bilaterally distributed and totally intermixed within the central caudal nucleus.3Furthermore, branching axons—that is, levator motor neurons connected with both levator palpabrae, are absent,3 or extremely rare (2%).4 Very little is known about the premotor network that controls the central caudal nucleus. A recently identified region in the rostral mesencephalon, medial to the rostral interstitial nucleus of medial longitudinal fasciculus, sends pathways to the central caudal nucleus, and could provide an excitatory signal for the upper eyelid, involved in eyelid coordination.5 Another structure, the nucleus of the posterior commissure probably provides inhibitory inputs to the central caudal nucleus, as a lesion of this region results in upper eyelid retraction.6 Each nucleus of the posterior commissure is connected with its contralateral counterpart through the posterior commissure, but does not project directly to the central caudal nucleus. Linkage between the nucleus of the posterior commissure and levator palpabrae motor neurons could be realised in the so called supraoculomotor area.6 This region, located dorsolaterally to the oculomotor nucleus, within the periaqueductal grey, receives nucleus of the posterior commissure afferents and contains dendrites coming from central caudal nucleus cell bodies.6 However, the exact pattern of connectivity between the nucleus of the posterior commissure and levator palpabrae neurons within the supraoculomotor area is unknown.
We here report on a patient with a circumscribed brainstem infarction and a consecutive nuclear oculomotor nerve syndrome with normal ipsilateral eyelid position and motility and contralateral eyelid retraction. This unusual pattern of eyelid dysfunction allows for deductions on supranuclear central caudal nucleus pathways involved in levator palpabrae inhibition.
A 44 year old man was admitted after sudden onset of a left hemiplegia. A cerebral CT showed a right thalamopeduncular haematoma. Neuro-ophthalmological examination showed a right sided oculomotor palsy, with a large 5 mm non-reactive pupil, and a vertical gaze and adduction palsy. However, there was no ptosis: the right eyelid had a normal position in resting condition, and showed upward and downward displacements during attempted vertical eye movements. Abduction was normal. On the left side, there was a tonic downward deviation of the eye that could not be elevated above the horizontal plane, even during vertical oculocephalic manoeuvres. Downward movements, abduction, and adduction were normal. The pupil was of normal size (2.5 mm) and reactive to light. The eyelid was markedly retracted, a 4 mm band of upper sclera being uncovered in resting conditions (figure A). Manual opening or closure of the right eyelid did not influence lid retraction on the left side.
When the patient was seen on follow up 2 months later, the ocular motor syndrome was unchanged. Written consent was obtained from the patient for photographs. Brain MRI was performed and showed a lesion in the right thalamus and in the right paramedian mesencephalon. At this level, the lesion involved the region of the red nucleus and extended posteriorly towards the sylvian aqueduct but remained anterior to the posterior commissure (figure B).
The clinical features of this patient are consistent with a lesion of the right oculomotor nucleus.1 Complete elevation palsy on the side contralateral to the lesion is explained by the crossed innervation of the superior rectus. The downward deviation of the eye on the normal side has been previously reported and results from the unopposed action of the intact left inferior rectus muscle. Normal reactivity of the left pupil indicates that the lesion did not reach the unpaired Edinger-Westphal nucleus, located at the rostral pole of the oculomotor nucleus. Therefore, right-sided mydriasis resulted from an involvement of ipsilateral Edinger-Westphal nucleus efferent fibres. Conversely, absence of ptosis on the right side indicates that the central caudal nucleus and its efferent fibres (in the right oculomotor nerve) were intact. Such levator sparing in patients with an oculomotor nucleus lesion has already been reported,7 and is probably related to the mediocaudal location of the central caudal nucleus. The striking clinical feature of this patient was the existence of a contralateral eyelid retraction without ipsilateral ptosis, a condition that has not been previously reported in the context of a stroke. This retraction was unlikely to result from an levator palpabrae overactivation (as it would be expected according to Hering's law) as it was not influenced by manual elevation of the contralateral lid.1
Various patterns of eyelid disorders may be encountered in patients with focal mesencephalic lesions. Ptosis may be unilateral when central caudal nucleus efferent fibres are damaged, or bilateral, if the central caudal nucleus itself is involved.1 A bilateral eyelid retraction results from a lesion that involves either the posterior commissure or the nucleus of the posterior commissure itself.6 Lastly, a mixed pattern, the plus-minus lid syndrome, consists in ipsilateral ptosis and contralateral eyelid retraction.8 It is ascribed to a lesion involving both central caudal nucleus efferent (ipsilateral ptosis) and afferent (contralateral eyelid retraction) fibres.8 However, in this latter case, the ipsilateral ptosis could mask an eyelid-retraction. Therefore, in our patient, absence of ipsilateral ptosis shows that, at least in this case, eyelid retraction was strictly contralateral. According to anatomical data, it may be suggested that eyelid retraction in our patient resulted from a lesion involving central caudal nucleus afferent fibres—that is, inputs from the nucleus of the posterior commissure, most probably in the region of the supraoculomotor area.6 It may thus be inferred that inhibitory connections between the nucleus of the posterior commissure and central caudal nucleus (through the supraoculomotor area) are unilateral, and crossed. A similar crossed pattern may also exist for excitatory afferents to the central caudal nucleus, as hemispheric lesion resulting in contralateral ptosis have been reported.1
Inhibition of the levator palpabrae occurs mainly in conjunction with orbicularis oculi activation,1 a phenomenon that is controlled by monocular pathways. Thus, this push-pull system would have an homogenous unilateral organisation. Lastly, the crossed pattern of these inhibitory connections is reminiscent of the crossed levator palpabrae innervation which exists in phylogenetically lower mammals.9
In summary, it may be inferred from this finding and from anatomical data that the central caudal nucleus receives inhibitory inputs from the contralateral nucleus of the posterior commissure, and that lesion of these pathways leads to contralateral eyelid retraction.
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