Research paperThe border between the central and the peripheral nervous system in the cat cochlear nerve: A light and scanning electron microscopical study☆
Highlights
► The peripheral and central nerve border of the VIIth nerve is sharply delimited. ► The nodes of Ranvier at the border are in register. ► The border is a potential weak point as it fractures easily during sample preparation. ► This region is relevant clinically in head injury leading to hearing loss and in Schwannoma surgery. ► Understanding this region is also relevant to strategies for regeneration of the cochlear nerve.
Introduction
The transition between the central (CNS) and peripheral nervous system (PNS) in cranial and spinal nerve roots, referred to here as the CNS–PNS border, has interested anatomists since the 19th century (Thomsen, 1887, Skinner, 1931, Tarlov, 1937, Berthold and Carlstedt, 1977a, Fraher, 1992). Recently, it has also gained clinical interest because of its relevance to nerve root disorders and regeneration. During development, nerve fibers cross the CNS–PNS border in either direction (Berthold and Carlstedt, 1977b, OBrien et al., 2001) whilst in mature animals, the border is a barrier to regenerating nerve fibers (Carlstedt, 1997, Fraher, 2000), an important issue given the possibility of neural stem cell transplantation into the PNS (see e.g., Altschuler et al., 2008). However, fibers may pass through the border after its removal and subsequent reimplantation of the root (Carlstedt, 1997) or after treatment with trophic factors (Fraher, 2000, Ramer et al., 2000). The CNS–PNS border is normally also a barrier to Schwann cells. However, migration of Schwann cells into the CNS occurs during certain pathological conditions (Dal Canto and Barbano, 1984, Duncan and Hoffman, 1997). An understanding of the microanatomy and blood supply is also relevant to vascular decompression treatment of root related disorders such as trigeminal neuralgia (Peker et al., 2006).
The shape and location of the CNS–PNS border varies between nerve roots and species (Skinner, 1931, human including nIII, nV, nVI, nVII and nVIII; Berthold and Carlstedt, 1977a, cat spinal rootlets; Sloniewski et al., 1999, nX; Tomii et al., 2003, nVII; Peker et al., 2006, nV; Fraher, 1992, review). The border is usually dome shaped with the CNS compartment extending distally along the axis of the root. The segment of the root containing both CNS and PNS tissue is called the transitional region (Berthold and Carlstedt, 1977a) or transitional zone (Fraher, 1992). In most roots, it is located within a few millimeters of the CNS surface.
At the CNS–PNS border the axons continue uninterrupted from one compartment to the other whereas there is an abrupt change in type of myelin, supporting elements, and vascularization. Because central myelin is formed by oligodendrocytes and peripheral myelin by Schwann cells, the myelinated fibers are equipped with a node of Ranvier, called the borderline node, at their site of passage. In the PNS compartment, the individual myelinated fibers are separated by a matrix of loose connective tissue forming the endoneurium. In the CNS compartment, on the contrary, the myelinated fibers are tightly packed and held together by astrocytes with only narrow extracellular spaces as in CNS white matter in general. Proximal to the CNS–PNS border, astrocytes and their densely interwoven processes form the so-called mantle zone which is pierced by the nerve fibers but otherwise resembles the external glial limiting membrane of the CNS with which it is continuous. The astrocytes of the mantle zone may send processes, called glial fringes, distally into the endoneurial tissue spaces (Berthold and Carlstedt, 1977a).
Whilst oligodendrocytes make many myelin segments, each called an internode, Schwann cells make only one. The PNS compartment therefore exhibits a higher density of cell nuclei. It is also supplied with more vessels. The cochlear nerve fibers are fasciculated (Arnesen and Osen, 1978). In the PNS the fascicles are surrounded by a multilayered cellular membrane, the perineurium, and held together by a dense connective tissue, the epineurium.
The CNS–PNS border has a complicated microstructure which might be easier to understand when imaged 3-dimensionally by scanning electron microscopy. The present study was inspired by a previous anatomical investigation of the cochlear nerve in adult cat (Arnesen and Osen, 1978). During dissection, the nerve tended to fracture near the base of the cochlear nuclear complex at the expected site of the CNS–PNS border. The location of this breakage, which proved to be at the border, and the microanatomy underlying it, has been investigated here. A better understanding of the cytoarchitecture of this region may provide clues to the treatment of cochlear nerve disorders and could be useful for animal models of regeneration across the border.
Section snippets
Materials and methods
The study is based on the cochlear nerves of four adult cats of both sexes, body weight 2–4 kg. Four nerves were used for scanning electron microscopy, the remainder for light microscopy. Experimental protocols were approved by the Norwegian Institutional Animal Care and Use Committee and conform to the UK Animal (Scientific Procedures) Act 1986 although the tissue was obtained before the latter set of regulations came into place. This study involves the reuse of data from tissue obtained for a
Results
The term ‘cat cochlear nerve’ is used here to indicate both its CNS and PNS compartments. It thus substitutes for the term ‘cochlear nerve root’ which in previous studies (e.g., Osen, 1969) has been used to describe the extension of the fiber fascicles into the cochlear nuclear complex. The cochlear nerve is directed anteriorly from the base of the cochlear nuclear complex and is approximately 5–6 mm long if measured to the apex of the modiolus. The proximal 2 mm is situated within the internal
Discussion
The primary aim of the present study was to provide a scanning electron microscopic view of the plane of transition between the peripheral and central compartments of the cat cochlear nerve, referred to here as the CNS–PNS border. The dry-fracturing technique for scanning electron microscopy has been employed because it furnishes the opportunity for direct, high resolution observation of the interior of soft tissues (Flood, 1975). The study was successful because the CNS–PNS border proved to be
Acknowledgments
The experimental part of this study, including the scanning electron microscopy, was performed at the Institute of Medical Biology, University of Tromsø, Norway, in the 1970s. We dedicate this article to the late Atle Rønning Arnesen, Ear Nose and Throat Department, Oslo City Hospital (now Oslo University Hospital), who participated in the experiments. We are indebted to Enrico Mugnaini, Department of Behavioral Sciences, University of Connecticut (now at Northwestern University Institute of
References (48)
- et al.
Stem cell transplantation for auditory nerve replacement
Hear. Res.
(2008) - et al.
Age-related loss of spiral ganglion neurons
Hear. Res.
(2010) - et al.
Nerve fiber regeneration across the PNS–CNS interface at the root-spinal cord junction
Brain Res. Bull.
(1989) - et al.
Migration of neural precursor cells derived from olfactory bulb in cochlear nucleus exposed to an augmented acoustic environment
Hear. Res.
(2007) The CNS–PNS transitional zone of the rat. morphometric studies at cranial and spinal levels
Prog. Neurobiol.
(1992)- et al.
Transgenic BDNF induces nerve fiber regrowth into the auditory epithelium in deaf cochleae
Exp. Neurol.
(2010) - et al.
The cochlear nerve in the cat. Topography, cochleotopy, and fiber spectrum
J. Comp. Neurol.
(1978) - et al.
Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. II. General organization of the transitional region in S1 dorsal rootlets
Acta Physiol. Scand. Suppl.
(1977) - et al.
Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. V. A light microscopical and histochemical study of S1 dorsal rootlets in developing kittens
Acta Physiol. Scand. Suppl.
(1977) The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. II. Parenchymal distribution
Amer. J. Anat.
(1965)
Junctions between intimately apposed cell membranes in the vertebrate brain
J. Cell Biol.
Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. I. A preparatory procedure useful for electron microscopy of the lumbosacral dorsal rootlets
Acta Physiol. Scand. Suppl.
Nerve fiber regeneration across the peripheral – central transitional zone
J. Anat.
Remyelination during remission in Theiler’s virus infection
Am. J. Pathol.
Schwann cell invasion of the central nervous system of myelin mutants
J. Anat.
Dry-fracturing techniques for the study of soft internal biological tissues in the scanning electron microscope
The transitional zone and CNS regeneration
J. Anat.
Axons and glial interfaces: ultrastructural studies
J. Anat.
Plasticity and regeneration in the peripheral nervous system
Ital. J. Anat. Embryol.
Microvascular decompression of cochlear nerve for tinnitus incapacity: pre-surgical data, surgical analyses and long-term follow-up of 15 patients
Eur. Arch. Otorhinolaryngol.
On internodal length
J. Anat.
Collagen nerve protector in rat sciatic nerve repair: a morphometric and histological analysis
Microsurgery
Experimental traction injuries of cervical spinal roots: a scanning EM study of rupture patterns in fresh tissue
Neuropathol. Appl. Neurobiol.
Pathogenesis of hearing loss in head injury
Arch. Otolaryngol.
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The results have been published previously in abstract format (Osen and Arnesen, 1979).