Histologic Evaluation of Nonvisual Afferent Sensory Upper Eyelid Proprioception

Abstract

The authors describe proprioception in the upper eyelid: A histologic analysis. Purpose: Recent research has suggested a possible role for proprioception in ipsilateral frontalis activation in the setting of ptosis; however, there has not been any robust histologic or anatomic evidence to support this theory. To further elucidate proprioceptive structures in the eyelid, this investigation uses validated histologic techniques to explore the presence of proprioceptive structures or afferent neural networks in the Levator Palpebrae Superioris (LPS) and Müller muscle. Methods: Müller muscle and LPS samples were evaluated by a laboratory with extensive experience with the histology of extraocular muscle proprioception. Immunofluorescence and confocal laser scanning microscopy were used to analyze the tissue samples. Results: Thirty-four Müller muscle samples and 10 LPS samples were analyzed. Golgi tendon bodies and muscle spindles were not identified in the Müller muscle and LPS samples. This result is expected in the Müller muscle given that these structures are not typically present in smooth muscle, but noteworthy in the skeletal muscle of the LPS. Previously undescribed synaptophysin-positive free nerve terminals within the intermuscular connective tissue of the Müller muscle were identified. Conclusions: The nerve terminals identified are anatomically consistent with free nerve endings present in the extraocular muscles that have been implicated in proprioception. These findings advance our current knowledge of the ultrastructure of Müller muscle and the LPS and suggest a possible mechanism for proprioception in the upper eyelid that may have a role in ipsilateral brow elevation in the setting of ptosis.

Muscle Spindles in the Levator Palpebrae Superioris Muscle of Human Adults

“…1 In comparison, another study done in the US did not find any muscle spindles at all in the LPS muscles of human adults aged 47 to 77 years. 8 The difference between this study and ours may be due to racial and methodological disparities. 8 All muscle spindles were found in the most proximal section (the muscle origin) of the LPS muscle in this study.…”

“…3,4 In contrast, muscle spindles in the levator palpebrae superioris (LPS) muscle have little been elucidated in human adults. 4,5,8 A previous report examined muscle spindles in the LPS muscle but this study was conducted in human foetuses. 1 Studies that examined muscle spindles in the LPS muscle in human adults either found no muscle spindles in the LPS 8 or did not discuss their findings at all.…”

“…4,5,8 A previous report examined muscle spindles in the LPS muscle but this study was conducted in human foetuses. 1 Studies that examined muscle spindles in the LPS muscle in human adults either found no muscle spindles in the LPS 8 or did not discuss their findings at all. 4,5 We examined the number and distribution of muscle spindles in the LPS muscles of human adults.…”

Anophthalmic Socket Syndrome: Prevalence, Impact and Management Strategies

“…80 Ipsilateral frontalis muscle activation in anophthalmic patients with ptosis is an interesting phenomenon that demonstrates the presence of non-visual stimuli in frontalis recruitment, showing that a sensory trigger -and not a visual stimulus -might be responsible for frontalis recruitment in these patients. 81,82 Histologic studies have confirmed the presence of Golgi tendon organs, muscle spindles, and myotendinous cylinders within the levator muscle, 83 and neural structures have been demonstrated in Müller's muscle fibers. 84 These nerve terminals may be implicated in proprioception, and the pathway for frontalis contraction might originate in proprioceptive fibers in the Müller's muscle through the trigeminal ganglion.…”

“…82 The eyelid, in close contact with the prosthesis, may provide an alternative pathway to stimulate ipsilateral frontalis recruitment. [83][84][85]…”