Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations

Abstract

Aims: To describe the anatomy and the arrangement of the arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve and to consider their possible clinical relevance for cerebrospinal fluid dynamics and fluid pressure in the subarachnoid space of the human optic nerve.

Methods: Postmortem study with a total of 12 optic nerves harvested from nine subjects without ocular disease. All optic nerves used in this study were obtained no later than 7 hours after death, following qualified consent for necropsy. The study was performed with transmission (TEM) and scanning electron microscopy (SEM).

Results: The subarachnoid space of the human optic nerve contains a variety of trabeculae, septa, and stout pillars that are arranged between the arachnoid and the pia layers of the meninges of the nerve. They display a considerable numeric and structural variability depending on their location within the different portions of the optic nerve. In the bulbar segment (ampulla), adjacent to the globe, a dense and highly ramified meshwork of delicate trabeculae is arranged in a reticular fashion. Between the arachnoid trabeculae, interconnecting velum-like processes are observed. In the mid-orbital segment of the orbital portion, the subarachnoid space is subdivided, and can appear even loosely chambered by broad trabeculae and velum-like septa at some locations. In the intracanalicular segment additionally, few stout pillars and single round trabeculae are observed.

Conclusion: The subarachnoid space of the human optic nerve is not a homogeneous and anatomically empty chamber filled with cerebrospinal fluid, but it contains a complex system of arachnoid trabeculae and septa that divide the subarachnoid space. The trabeculae, septa, and pillars, as well as their arrangement described in this study, may have a role in the cerebrospinal fluid dynamics between the subarachnoid space of the optic nerve and the chiasmal cistern and may contribute to the understanding of the pathophysiology of asymmetric and unilateral papilloedema. All the structures described are of such delicate character that they can not even be visualised with high resolution magnetic resonance imaging (MRI).

Figure 1

Schematic drawing of the optic nerve demonstrating the location of the (a) bulbar segment (containing trabeculae), (b) mid-orbital segment (containing septae and pillars), and (c) canalicular portion (containing pillars). The bulbar segment and the mid-orbital segment together form the orbital portion (modified according to Liu and Kahn13).

Figure 2

SEM appearance of the subarachnoid space in the bulbar segment. (A) Overview of the subarachnoid space showing the complex network of trabeculae. The arrows point to veil-like cytoplasmic extensions between adjacent trabeculae (bar = 150 μm). (B, C) Delicate subarachnoid space network formed by branching trabeculae (bar = 50 μm). The arrow points to a trabeculum with a blood vessel. Note again the veil-like cytoplasmic extensions connecting adjacent trabeculae (bar = 2 μm). Surface of trabeculae covered by flattened cells with distinct intercellular clefts and fenestrations (bar = 0.2 μm).

Figure 3

TEM morphology of arachnoid trabeculae in the bulbar segment. The trabeculae are completely surrounded by arachnoid cells. (A) Note the thin cytoplasmic bridges (arrows) connecting adjacent trabeculae (bar = 2 μm). (B) At higher magnification multiple layers of cytoplasmic extensions from arachnoid cells are detectable at the surface of a trabeculum. Note the desomosomes (arrows) between the arachnoid cells and the broad basal lamina-like extracellular matrix supporting the leptomeningeal cells (arrowheads) (bar = 0.25 μm).

Figure 4

SEM morphology of the subarachnoid space in the mid-orbital segment. (A) Overview of the subarachnoid space subdivided by well defined septa (arrows), N = optic nerve (bar = 150 μm). (B) Arachnoid septum within the subarachnoid space; note the septal perforations connecting adjacent subarachnoid space chambers (bar = 25 μm). (C) Pillar bridging the subarachnoid space and extending into the dura layer of the arachnoid (bar = 30 μm). (D) Detail of a septum with typical intercellular clefts (bar = 0.5 μm).

Figure 5

SEM morphology of the subarachnoid space in the intracanalicular segment. (A) Overview of the subarachnoid space; A = ophthalmic artery, N = optic nerve (bar = 15 μm) (the optic nerve is turned 180°). (B) Pillars (arrows) and trabeculae (arrowheads) transversing the subarachnoid space (bar = 30 μm). (C) Trabeculae within the subarachnoid space found at the orbital opening of the optic canal (bar 30 μm). (D) Leucocyte at the surface of a pillar in the intracanalicular segment (bar = 5 μm).