Human eyelid behavior is driven by segmental neural control of the orbicularis oculi

• 成果类型: Article
• 署名作者: Kim, Jinyoung; Shirriff, Ashley; Cornwell, Jordan N.; Mutis, Maria Paula Quintero; Delis, Ereni; Wang, Sophia; Rootman, Daniel B.; Clites, Tyler R.
• 署名单位: University of California System; University of California Los Angeles; University of California System; University of California Los Angeles
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-14987
• DOI: 10.1073/pnas.2508058122
• 发表日期: 2025-08-12
• 关键词: levator palpebrae superioris; electrical-stimulation; reflex blinking; movements; muscle; reanimation; voluntary; motion

摘要

The eyelid performs critical functions to protect the eye and preserve functional vision. These functions are driven by contraction of the orbicularis oculi (OO), which is a unique skeletal muscle with a circular geometry and diffuse innervation. It is thought that this distributed innervation may allow for differential segmental activation and contraction, but it is not currently understood how sequenced activation patterns relate to differential muscle contraction, nor how segmental contraction creates the kinematics that drive the eyelid's critical functions. In fact, motion of the eyelid has predominantly been modeled in only a single dimension (open-close). Here, we show that eyelid motion has important two-dimensional features that vary between eyelid behaviors. Using distributed intramuscular electromyography, we further show that activation differs segmentally across the OO, and that patterns of activation change to produce different behavior-specific eyelid kinematics. Our results demonstrate the role of segmental activation in eyelid motion, highlighting the importance of precise neural control in producing natural eyelid behavior. We anticipate that this research is a starting point for robust mechanistic models of eyelid function. This knowledge has critical implications for diagnosis and treatment of eyelid paralysis. Significance The human eyelid is an intricate structure that plays a critical role in maintaining vision, but its neuromuscular control remains poorly understood. Here, we present high-resolution intramuscular recordings of muscle activation from the orbicularis oculi, coupled with precise measurements of eyelid movement, during different behaviors. Our results show that eyelid motion is complex, behavior-specific, and driven by precise sequences of muscle activation. These findings challenge simplistic models of eyelid function and highlight the importance of fine neural control in generating natural eyelid motion. This work lays the foundation for improved diagnosis of eyelid pathology, as well as future development of neuroprosthetic devices to restore eyelid function.