Posture-Dependent Collapse of the Optic Nerve Subarachnoid Space: A Combined MRI and Modeling Study

Abstract

Purpose We hypothesize that a collapse of the optic nerve subarachnoid space (ONSAS) in the upright posture may protect the eyes from large translamina cribrosa pressure differences (TLCPD) believed to play a role in various optic nerve diseases (e.g., glaucoma). In this study, we combined magnetic resonance imaging (MRI) and mathematical modeling to investigate this potential ONSAS collapse and its effects on the TLCPD. Methods First, we performed MRI on six healthy volunteers in 6° head-down tilt (HDT) and 13° head-up tilt (HUT) to assess changes in ONSAS volume (measured from the eye to the optic canal) with changes in posture. The volume change reflects optic nerve sheath (ONS) distensibility. Second, we used the MRI data and mathematical modeling to simulate ONSAS pressure and the potential ONSAS collapse in a 90° upright posture. Results The MRI showed a 33% decrease in ONSAS volume from the HDT to HUT ( P < 0.001). In the upright posture, the simulations predicted an ONSAS collapse 25 mm behind lamina cribrosa, disrupting the pressure communication between the ONSAS and the intracranial subarachnoid space. The collapse reduced the simulated postural increase in TLCPD by roughly 1 mm Hg, although this reduction was highly sensitive to ONS distensibility, varying between 0 and 4.8 mm Hg when varying the distensibility by ± 1 SD. Conclusions The ONSAS volume along the optic nerve is posture dependent. The simulations supported the hypothesized ONSAS collapse in the upright posture and showed that even small changes in ONS stiffness/distensibility may affect the TLCPD.

Mathematical modelling of the CSF system: effects of microstructures and posture on optic nerve subarachnoid space dynamics

“…One main assumption in our default model [ 18 ] is that we extrapolate the distensibility results from 13 to 90 degrees. Imposing a lower limit on the calculated porosity is a way to remedy this, and to investigate the effects of this assumption (Fig.…”

“…Intraocular pressure is denoted as . In between compartments we have the resistances and for ONSAS and craniospinal flow, respectively, where the former is dependent on the ONSAS pressure (through MRI—derived ONS distensibility at different sections along the ONSAS [ 18 ]). Flow rates and their directions are indicated with arrows.…”

“…These 14 sections together cover 4 regions; bulbar, midorbital 1, midorbital 2, and intra-canicular parts of the optic nerve (see Table 3 ). Subdivision of the ONSAS into several sections is important as the ONSAS decreases in size in upright postures [ 18 , 36 ], introducing substantial flow resistance in this position. Thus, allowing for variations in size, distensibility and microstructural content along the ONSAS will be crucial for the estimation of this resistance.…”

“…The distensibility was acquired from MRIs of healthy volunteers [ 18 ]. Since each of the 13 ONSAS segments each had a unique distensibility ( ), the in Eq.…”

“…As craniospinal CSF pressures and volumes change between different postures due to gravity [ 15 – 17 ], the pressure and flow in the ONSAS are altered in upright postures compared to horizontal postures. Based on MRI data of the ONSAS, we previously predicted a potential compartmentalization of the ONSAS in the upright posture, hindering flow and pressure transmittance between the eye and brain [ 18 ], possibly protecting the eye from low CSF pressures. However, the predictive model used in this previous study did not include the effects of the complex system of microstructures occupying the ONSAS [ 19 ].…”