Disorders of Eyelid-Eye Coordination

Lid-eye coordination is preserved in most pathological eye movements. For example, in vertical nystagmus the lid usually accompanies the eye movement [146]. Disorders of eyelid-eye coordination occur when lid saccades are impaired but eye saccades preserved. Involuntary lid movement without accompanying vertical eye movement, e.g. in lid nystagmus, is less frequent. Lid nystagmus without vertical nystagmus may be elicited on horizontal gaze, e.g. reported in a case of midbrain astrocytoma [98]. In midbrain lesions in the monkey, vestibular stimulation caused an upward lid nystagmus, although the upbeat nystagmus was abolished [101].

In accordance with the anatomical connections outlined above, lid nystagmus may imply lesions of the M group, the nPC, or their reciprocal connections.

Lid lag and lid retraction are the most common disorders of impaired eye- lid-eye coordination [147]. Whereas lid lag is a dynamic sign, which can be observed on downgaze, lid retraction is a static phenomenon.

Lid retraction is diagnosed when the sclera is seen above the corneal limbus during steady fixation. It indicates inappropriate LP muscle activity, presumably related to neurogenic disinhibition of LP [19], but EMG evidence is still missing. The basal tonic LPM activity is likely to be under the inhibitory control of the nPC [12]. Deficient inhibition would result in lid retraction on gaze straight ahead or lid lag with downgaze [147]. A clinicopathological retrospective correlation study based on animal [18, 148] and human [149] case studies delineated the nPC as the most likely lesion site for lid retraction [19]. This is consistent with very few eyelidand vertical saccade-related burst neurons that have been recorded in nPC [150].

Although lid lag and lid retraction may occur together [151], a feasible pathomechanism has to account for lesions that cause only either lid lag or lid retraction. A single case report showing a patient with slow vertical saccades and lid lag but no lid retraction [152] suggests separate pathways for both clinical signs. This lesion spared the nPC but probably affected the M group. It remains open whether dynamic and static lid-eye coordination is controlled by separate pathways. Lid retraction is seen in ischemic midbrain lesions, e.g. Parinaud’s syndrome, and extrapyramidal syndromes, e.g. PD and PSP [153, 154]. The prevalence of lid retraction/lid lag in PD patients is not exactly known, but preliminary data indicate up to 37% of patients [147].

In incomplete vertical gaze palsy caused by midbrain lesions, the lid appears to follow the eye, but it may also cause a lid saccade [19, 155]. In the case of upward gaze palsy, the lids may retain the ability to elevate during attempted vertical upgaze, i.e. so-called ‘pseudoretraction’. In turn, the lid may lower during attempted downgaze in downgaze saccade palsy, leading to ‘pseudoptosis’ [19]. Eye-lid coordination in mesencephalic lesions has not yet been systematically examined in detail.