Co-firing of levator palpebrae and masseter muscles links the masticatory and oculomotor system in humans

Abstract

Simultaneous co-firing of the levator palpebrae (LP) and pterygoid muscles were recorded in Marcus Gann Syndrome (MGS) patients in early clinical studies. "Release hypothesis" proposed an intrinsic masticatory oculomotor neural circuit and this kind circuit, which, however, has been observed only in amphibian. On the other hand, congenital miswiring hypothesis has overwhelmed other interpretations. However, the same phenomenon visualized in MGS cases was unveiled in human subjects without any sign of congenital oculomotor disorder. To further study co-firing of the upper eyelid and jaw muscles, we applied non-invasive EMG recording of the upper eyelid and ipsilateral masseter muscle belly in nine healthy volunteers. LP activity was determined initially by looking upward and active retraction of upper eyelid with head fixed. Then, dual channel inputs from upper eyelid and masseter muscle was recorded during tooth occlusion motivated by isometric masseter muscle contraction without jaw and face moving. The EMG recorded from upper eyelid when the subjects retracted eyelid with head fixed exhibited the same pattern as that collected during tooth occlusion, but the pattern was completely different from EMG of active eye closure. This reflects tooth occlusion evoked LP activity. Then, simultaneous co-firing of the LP and masseter muscle was recorded simultaneously during tooth occlusion without jaw movement. Finally, the aforementioned co-firing was recorded when the subjects conducted rhythmic occlusion and synchronous EMG from both muscles was acquired. In conclusions, humans may also have an intrinsic masticatory oculomotor circuit and release hypothesis may apply, at least, to some cases of MGS.

Keywords: EMG; Marcus Gann Syndrome; healthy human; tooth occlusion; upper eyelid.

Fig. 1. Positions of recording and reference electrodes and the relevant recordings.

A, the recording electrodes were placed on middle upper eyelid and above masseter muscle belly; and the reference electrode was mounted on middle forehead. B, The relevant EMG recorded from upper eyelid during active eye closure (upper trace), when subjects looked upward with the head fixed or actively retracted eyelid (middle line) and during forceful tooth occlusion driven by isometric jaw closing muscle contraction without jaw movement (lower trial). Use of the photograph was permitted by the subject.

Fig. 2. Co-fire of muscles on upper eyelid and masseter muscle.

A and D, subjects were performing tooth occlusion by isometric contraction without jaw and face movement. B and E, EMG was recorded from the upper eyelid. C and F, EMG was collected from electrode on masseter muscle belly. Use of the photograph was permitted by the subject.

Fig. 3. Rhythmic co-firing of muscles on the upper eyelid and masseter muscle.

A, a subject was carrying out rhythmic biting as if chewing, but the jaw and face did not move with only isometric contraction of jaw closing muscles (arrows). B, a clear rhythmic co-fire of muscles on upper eyelid and masseter muscle during rhythmic occlusion driven by rhythmic isometric contraction of the masseter muscle without jaw and face movement. Use of the photograph was permitted by the subject.