Collagen fiber recruitment: A microstructural basis for the nonlinear response of the posterior pole of the eye to increases in intraocular pressure.

Our goal was to quantify and characterize how the collagen fiber crimp waviness of the lamina cribrosa (LC) and peripapillary sclera (PPS) changes with intraocular pressure (IOP). Thirteen sheep (ovine) eyes were immersion and perfusion fixed while maintaining IOP at 0, 10, 15, 20, or 50 mmHg. Coronal optic nerve head (ONH) sections (30 µm) were imaged with polarized light microscopy (PLM) and analyzed for collagen fiber orientation and waviness (SD of fiber orientation). In the LC, the waviness of every LC beam was measured. In the PPS, at least 900 collagen bundles were measured per eye. Using the waviness at 50 mmHg IOP, we defined tissue-specific thresholds to determine the fraction of loaded or recruited fibers. We found that fiber waviness decreased with IOP (P < 0.001). At every IOP, the waviness of the collagen fibers, and the fraction of fibers recruited in the LC were smaller or equal than those of the PPS (P < 0.001). At 15 mmHg IOP, both LC and PPS had ¾ recruited fibers and ¼ left in reserve. The decreased waviness with IOP and associated fiber recruitment is experimental evidence of fiber-based nonlinear biomechanical behavior of the ONH. At all IOPs the PPS had an equal or larger fraction of fibers recruited than the LC. That both LC and PPS had the same fraction of recruited and reserve fibers at normal IOP suggests that this may be an optimal fraction of recruitment for healthy eyes. Whether this extends to human eyes remains unknown. STATEMENT OF SIGNIFICANCE: Collagen fibers exhibit a natural waviness or crimp that largely determine the nonlinear biomechanics of soft tissue. Experimental measurements of crimp morphology in the sheep eye, and how it changes with intraocular pressure (IOP), however, are exceedingly sparse. We quantified how posterior eye crimp changes with increasing IOP. We found that the lamina cribrosa and peripapillary sclera have fundamentally different crimp, and with increasing IOP, have different proportions of fibers that straighten, or get recruited, versus remaining wavy, or in reserve. Interestingly, at physiologic IOP of 15 mmHg, both tissues had about ¾ fibers recruited and ¼ fibers in reserve, indicating there may be an optimal fraction of fibers.