A further study of the fine structure and membrane properties of neuroglia in the optic nerve of Necturus

The optic nerve of Necturus maculosus consists of a homogeneous population of astroglia and bundles of unmyelinated axons. The glial cell processes ramify within the nerve roughly delineating fascicles of axons and come together at the periphery to form a complete external limiting membrane interrupted only by narrow clefts between adjacent processes. They are frequently “attached” to one another, forming specialized junctions. Blood vessels are entirely outside the nerve which is surrounded by a basal lamina. The temperature dependence of the glial membrane potential is accurately predicted by the Nernst relation. The membrane potential is unaffected by changes in Cl, Na, Li, and guanidinium which are apparently impermeant. The permeability of the glial membrane to other cations is in the sequence Tl> K> Rb> Cs> NH₄. This suggests that the chemical nature of the site of potassium permeability in glial cells is similar to that in the neuron.     

Sodium channels in axons and glial cells of the optic nerve of Necturus maculosa

Experiments investigating both the binding of radioactively labelled saxitoxin (STX) and the electrophysiological response to drugs that increase the sodium permeability of excitable membranes were conducted in an effort to detect sodium channels in glial cells of the optic nerve of Necturus maculosa, the mudpuppy. Glial cells in nerves from chronically enucleated animals, which lack optic nerve axons, show no saturable uptake of STX whereas a saturable uptake is clearly present in normal optic nerves. The normal nerve is depolarized by aconitine, batrachotoxin, and veratridine (10(-6)-10(-5) M), whereas the all-glial preparation is only depolarized by veratridine and at concentrations greater than 10(-3) M. Unlike the depolarization caused by veratridine in normal nerves, the response in the all-glial tissue is not blocked by tetrodotoxin nor enhanced by scorpion venom (Leiurus quinquestriatus). In glial cells of the normal nerve, where axons are also present, the addition of 10(-5) M veratridine does lead to a transient depolarization; however, it is much briefer than the axonal response to veratridine in this same tissue. This glial response to veratridine could be caused by the efflux of K+ from the drug-depolarized axons, and is similar to the glial response to extracellular K+ accumulation resulting from action potentials in the axon.     

Structure of the intramural nerves of the rat bladder

The bladder of adult female rats receives ～16,000 axons (i.e., is the target of that many ganglion neurons) of which at least half are sensory. In nerves containing between 40 and 1200 axons cross-sectional area is proportional to number of axons; >99% of axons are unmyelinated. A capsule forms a seal around nerves and ends abruptly where nerves, after branching, contain ～10 axons. A single blood vessel is present in many of the large nerves but never in nerves of <600 axons. The number of glial cells was estimated through the number of their nuclei. There is a glial nucleus profile every 76 axonal profiles. Each glial cell is associated with many axons and collectively covers ～1,000 μm of axonal length. In all nerves a few axonal profiles contain large clusters of vesicles independent of microtubules. The axons do not branch; they alter their relative position along the nerve; they vary in size along their length; none has a circular profile. All the axons are fully wrapped by glial cells and never contact each other. The volume of axons is larger than that of glial cells (55%–45%), while the surface of glial cell is twice as extensive as that of axons; there are ～2.27 m² of axolemma and ～4.60 m² of glial cell membrane per gram of nerve. Of the mitochondria of a nerve ～3/4 are in axons and ～1/4 in glial cells.     

Sensory innervation of the tentacles of the polychaete,Sabella pavonina

Summary Following observation of conical groups of stiff, but motile cilia on the tentacles of the branchial crown of Sabella pavonina, these were examined with the electron microscope. The bundles consist of about 40 unenclosed standard cilia supported by one or two primary sense cells with centrally directed axons of 0.1–0.2 diameter. Axons in the distal portions of the branchial crown occur in small bundles surrounded by a basement membrane. More centrally, glial elements appear and the nerves are surrounded by a collagenous sheath. The branchial nerve trunk shows similarities in organisation to other previously investigated annelid central nervous tissue in that the whole nerve is surrounded by a fibrous sheath central to which there is a layer of glial cells with processes penetrating a central neuropile. The 0.1–0.2 axons commonly occur in glial-enveloped groups of < 40 whilst other axons of larger and mixed diameter are found together.Each tentacle has two branchial nerves on the oral side, and each nerve gives rise to two small 75-axon branches running to each pinnule. The branchial nerves fuse to form the branchial nerve trunk running to the supra-oesophageal ganglia.Sections of the branchial nerves of the branchial crown at progressively more central levels show that the branchial nerve trunk contains enough axons of 0.1–0.2 diameter to account for all the sensory cells on the tentacles. This is taken as evidence for the sensory cells having axons terminating within the central nervous system and that there is no peripheral confluence or fusion of these afferent axons.     

Electron microscopy of the mucosal plexus of the rat colon.

The ultrastructure of neurons, glial cells and axons of the mucosal plexus of the rat colon descendens was studied. Serial semithin sections and a re-embedding technique were used in order to localize the ganglia. The ganglia are free of blood vessels and connective tissue. The ratio of neurons to glial cells is approximately 1. Ganglia and nerve strands are enclosed by a basement membrane, without a well-defined perineural connective tissue. The neurons show a structure similar to other enteric plexus. Synaptic contacts were observed frequently in the neuropil, where nerve endings and varicosities show a diverse outfit in vesicles. The glial cells, which contain immunocytochemically detectable glial fibrillary protein, possess the same ultrastructural attributes in the intra- and extraganglionic localizations. In the nerves, axonic profiles and varicosities appear in close relation with glial cells or their processes. The distance between the nerves and their target cells, i.e. the enterocytes, is 0.5 microns or more with interposed basement membranes and fibroblasts.     

Wrapping it up: the cell biology of myelination

During nervous system development, oligodendroglia in the central nervous system (CNS) and Schwann cells in the peripheral nervous system (PNS) synthesise large amounts of specific proteins and lipids to generate myelin, a specialised membrane that spirally ensheathes axons and facilitates fast conduction of the action potential. Myelination is initiated after glial processes have attached to the axon and polarisation of the plasma membrane has been triggered. Myelin assembly is a multi-step process that occurs in spatially distinct regions of the cell. We propose that assembly of myelin proteins and lipids starts during their transport through the biosynthetic pathway and continues at the plasma membrane aided by myelin-basic protein (MBP). These sequential processes create the special lipid and protein composition necessary for myelin to perform its insulating function during nerve conduction.     

Effects of batrachotoxin on membrane potential and conductance of squid giant axons

The effects of batrachotoxin (BTX) on the membrane potential and conductances of squid giant axons have been studied by means of intracellular microelectrode recording, internal perfusion, and voltage clamp techniques. BTX (550–1100 nM) caused a marked and irreversible depolarization of the nerve membrane, the membrane potential being eventually reversed in polarity by as much as 15 mv. The depolarization progressed more rapidly with internal application than with external application of BTX to the axon. External application of tetrodotoxin (1000 nM) completely restored the BTX depolarization. Removal or drastic reduction of external sodium caused a hyperpolarization of the BTX-poisoned membrane. However, no change in the resting membrane potential occurred when BTX was applied in the absence of sodium ions in both external and internal phases. These observations demonstrate that BTX specifically increases the resting sodium permeability of the squid axon membrane. Despite such an increase in resting sodium permeability, the BTX-poisoned membrane was still capable of undergoing a large sodium permeability increase of normal magnitude upon depolarizing stimulation provided that the membrane potential was brought back to the original or higher level. The possibility that a single sodium channel is operative for both the resting sodium, permeability and the sodium permeability increase upon stimulation is discussed.     

A developmental and ultrastructural study of the optic chiasma in Xenopus

The structure of the optic chiasma in Xenopus tadpoles has been investigated by light and electron microscopy. Where the optic nerve approaches the chiasma, a tongue of cells protrudes from the periventricular cell mass into the dorsal part of the nerve. Glial processes from this tongue of cells ensheath fascicles of optic axons as they enter the brain. Coincident with this partitioning, the annular arrangement of axons in the optic nerve changes to the laminar organization of the optic tract. Beyond the site of this rearrangement, all newly growing axons accumulate in the ventral-most part of the nerve and pass into the region between the periventricular cells and pia which we have called the 'bridge'. This region is characterized by a loose meshwork of glial cell processes, intercellular spaces and the presence of both optic and nonoptic axons. In the bridge, putative growth cones of retinal ganglion cell axons are found in the intercellular spaces in contact with both the glia and with other axons. The newly growing axons from each eye cross in the bridge at the midline and pass into the superficial layers of the contralateral optic tracts. As the system continues to grow, previous generations of axon, which initially crossed in the existing bridge, are displaced dorsally and caudally, forming the deeper layers of the chiasma. At their point of crossing in the deeper layers, these fascicles of axons from each eye interweave in an intimate fashion. There is no glial segregation of the older axons as they interweave within the chiasma.     

FREEZE-FRACTURING OF NERVE GROWTH CONES AND YOUNG FIBERS : A Study of Developing Plasma Membrane

Neural and non-neural cellular processes have been studied in organotypic cultures of spinal cord and olfactory bulb by means of the freeze-fracturing technique. Identification of specific cellular elements in replicas has been achieved by comparison with thin-sectioned material in which differences in shape and contents are evident. Freeze-fracturing reveals that neural growth cones may be distinguished from glial pseudopodia by the low number of intramembranous particles within their plasma membrane; the counts of particles within the growth cone membrane average 85/µm² (for the inner leaflet) as opposed to hundreds per square micrometer in glial pseudopodia. Whereas the intramembranous particle number in glial pseudopodia is only slightly lower than in their perikaryal plasmalemma, the number of particles in outgrowing axons increases about eightfold from the periphery towards the perikaryon. Furthermore, with prolonged time of growth in culture, the particle density in the young nerve fibers increases by about the same factor. The same phenomenon, i.e. a low intramembranous particle level at earlier stages and an increase in numbers as the nerve fiber matures, is observed in fetal nerve tissue in vivo. These findings suggest that the plasmalemma of the outgrowing nerve, and especially of the growth cone, is immature and that maturation is accompanied by the insertion of intramembranous particles. Furthermore, these data indicate that the chemistry of the growth cone membrane is distinct from that of the neuron soma which may be significant for the mechanisms of guidance and recognition in the growing nerve tip.     

The Fine Structure of Nerve Cells and Fibers, Neuroglia, and Sheaths of the Ganglion Chain in the Cockroach (Periplaneta americana)

The abdominal nerve cord of Periplaneta americana was studied utilizing light and electron microscopes. In the nerve cells, delicate granules, similar to those probably responsible for cytoplasmic basophilia, are evenly distributed in "dark" cells and clumped in "light" cells. Neuroglial cells are stained metachromatically by cresyl violet. The neuroglial cells have many processes which ramify extensively and are enmeshed to form overlapping layers. These imbricated processes ensheath the nerve cells; the inner layer of the sheath penetrates into the neuron and is responsible for the appearance of the trophospongium of Holmgren. Nerve fibers are embedded within glial cells and surrounded by extensions of the plasma membrane similar to mesaxons. Depending on their size, two or several nerve fibers may share a single glial cell. Nerve fibers near their terminations on other nerve fibers contain particles and numerous, large mitochondria. The ganglion is ensheathed by a thick feltwork of connective tissue and perilemmal cells. The abdominal connective has a thinner connective tissue sheath which is without perilemmal cells. The nerve fibers and sheaths in the connective become thinner as they pass through ganglia.     

The fine structure of nerve cells and fibers,neuroglia, and sheaths of the ganglion chain in the cockroach (Periplaneta americana)

The abdominal nerve cord of Periplaneta americana was studied utilizing light and electron microscopes. In the nerve cells, delicate granules, similar to those probably responsible for cytoplasmic basophilia, are evenly distributed in "dark" cells and clumped in "light" cells. Neuroglial cells are stained metachromatically by cresyl violet. The neuroglial cells have many processes which ramify extensively and are enmeshed to form overlapping layers. These imbricated processes ensheath the nerve cells; the inner layer of the sheath penetrates into the neuron and is responsible for the appearance of the trophospongium of Holmgren. Nerve fibers are embedded within glial cells and surrounded by extensions of the plasma membrane similar to mesaxons. Depending on their size, two or several nerve fibers may share a single glial cell. Nerve fibers near their terminations on other nerve fibers contain particles and numerous, large mitochondria. The ganglion is ensheathed by a thick feltwork of connective tissue and perilemmal cells. The abdominal connective has a thinner connective tissue sheath which is without perilemmal cells. The nerve fibers and sheaths in the connective become thinner as they pass through ganglia.     

Axonal degeneration within the tympanal nerve of Schistocerca gregaria

This study describes time course and ultrastructural changes during axonal degeneration of different neurones within the tympanal nerve of the locust Schistocerca gregaria. The tympanal nerve innervates the tergit and pleurit of the first abdominal segment and contains the axons of both sensory and motor neurones. The majority of axons (approx. 97%) belong to several types of sensory neurones: mechano- and chemosensitive hair sensilla, multipolar neurones, campaniform sensilla and sensory cells of a scolopidial organ, the auditory organ. Axons of campaniform sensilla, of auditory sensory cells and of motor neurones are wrapped by glial cell processes. In contrast, the very small and numerous axons (diameter <1 microm) of multipolar neurones and hair sensilla are not separated individually by glia sheets. Distal parts of sensory and motor axons show different reactions to axotomy: 1 week after separation from their somata, distal parts of motor axons are invaded by glial cell processes. This results in fascicles of small axon bundles. In contrast, distal parts of most sensory axons degenerate rapidly after being lesioned. The time to onset of degeneration depends on distance from the lesion site and on the type of sensory neurone. In axons of auditory sensory neurones, ultrastructural signs of degeneration can be found as soon as 2 days after lesion. After complete lysis of distal parts of axons, glial cell processes invade the space formerly occupied by sensory axons. The rapid degeneration of distal auditory axon parts allows it to be excluded that they provide a structure that leads regenerating axons to their targets. Proximal parts of severed axons do not degenerate.     

The ultrastructure of the cardiac ganglion of the desert scorpion,Paruroctonus mesaensis (Scorpionida: Vaejovidae)

Light and electron microscopy of the pacemaker ganglion of the scorpion heart indicate that it is about 15 mm long and 50 μm in diameter and extends along the dorsal midline of the heart. The largest cell bodies (30–45 μm in diameter) occur in clusters along the length of the ganglion. The ganglion appears to be innervated with fibers from the subesophageal and first three abdominal ganglia. The cardiac ganglion is surrounded by a neurilemma and a membranous sheath. The latter is apparently derived from connective tissue cells seen outside the ganglion. Nerve fibers other than those in the neuropil areas are usually surrounded by membrane and cytoplasm of glial cells. Often there are several layers of glial membrane, forming a loose myelin. The cardiac nerves to the heart muscle are also surrounded by a neurilemma, and the axons are surrounded by glia. The motor nerves contain lucent vesicles 60–100 nm and opaque granules 120–180 nm in diameter. In the cardiac ganglion, some nerve cell bodies have complex invaginations of glial processes forming a peripheral trophospongium. In the neuropil areas, nerve cell processes are often in close apposition. The septilaminar configuration typical of gap junctions is common, with gap distances of 1–4 nm. In tissues stained with lanthanum phosphate during fixation, we found gaps with unstained connections (1–2 nm diameter) between nerve-nerve and glial-nerve cell processes. Annular or double-membrane vesicles in various stages of formation were also seen in some nerve fibers in ganglia stained with lanthanum phosphate. Nerve endings with electron-lucent vesicles 40–60 nm in diameter are abundant in the cardiac ganglion, suggesting that these contain the excitatory transmitter of intrinsic neurons of the ganglion. Less abundant are fibers with membrane-limited opaque granules, circular or oblong in shape and as much as 330 nm in their longest dimension. Also seen were some nerve endings with both vesicles and granules.     

Development of a glial network in the olfactory nerve: role of calcium and neuronal activity

In adult olfactory nerves of mammals and moths, a network of glial cells ensheathes small bundles of olfactory receptor axons. In the developing antennal nerve (AN) of the moth Manduca sexta, the axons of olfactory receptor neurons (ORNs) migrate from the olfactory sensory epithelium toward the antennal lobe. Here we explore developmental interactions between ORN axons and AN glial cells. During early stages in AN glial-cell migration, glial cells are highly dye coupled, dividing glia are readily found in the nerve and AN glial cells label strongly for glutamine synthetase. By the end of this period, dye-coupling is rare, glial proliferation has ceased, glutamine synthetase labeling is absent, and glial processes have begun to extend to enwrap bundles of axons, a process that continues throughout the remainder of metamorphic development. Whole-cell and perforated-patch recordings in vivo from AN glia at different stages of network formation revealed two potassium currents and an R-like calcium current. Chronic in vivo exposure to the R-type channel blocker SNX-482 halted or greatly reduced AN glial migration. Chronically blocking spontaneous Na-dependent activity by injection of tetrodotoxin reduced the glial calcium current implicating an activity-dependent interaction between ORNs and glial cells in the development of glial calcium currents.     

Reciprocal interactions between olfactory receptor axons and olfactory nerve glia cultured from the developing moth Manduca sexta

In olfactory systems, neuron-glia interactions have been implicated in the growth and guidance of olfactory receptor axons. In the moth Manduca sexta, developing olfactory receptor axons encounter several types of glia as they grow into the brain. Antennal nerve glia are born in the periphery and enwrap bundles of olfactory receptor axons in the antennal nerve. Although their peripheral origin and relationship with axon bundles suggest that they share features with mammalian olfactory ensheathing cells, the developmental roles of antennal nerve glia remain elusive. When cocultured with antennal nerve glial cells, olfactory receptor growth cones readily advance along glial processes without displaying prolonged changes in morphology. In turn, olfactory receptor axons induce antennal nerve glial cells to form multicellular arrays through proliferation and process extension. In contrast to antennal nerve glia, centrally derived glial cells from the axon sorting zone and antennal lobe never form arrays in vitro, and growth-cone glial-cell encounters with these cells halt axon elongation and cause permanent elaborations in growth cone morphology. We propose that antennal nerve glia play roles similar to olfactory ensheathing cells in supporting axon elongation, yet differ in their capacity to influence axon guidance, sorting, and targeting, roles that could be played by central olfactory glia in Manduca.     

Fine structure of the median eminence and the pars nervosa of the bullfrog,Rana catesbeiana

Summary The hypothalamic neurosecretory system of the bullfrog, Rana catesbeiana, was studied with light- and electron microscopy. The median eminence is roughly divided into two portions. The upper portion mostly consists of ependymal cells, glial cells and preoptico-hypophysial nerve tract, whereas in the lower portion, neurosecretory axons, glial cells, processes of glial and ependymal cells, and fine blood vessels of the hypothalamic portal vein are located. A part of the neurosecretory axons of the preoptico-hypophysial tract proceeds to the lower portion of the median eminence. These axons are arranged perpendicularly to the capillaries of the hypothalamic portal vein. The glial cells are densely located in the area of the median eminence where neurosecretory material is abundant. The neurosecretory material in the neurosecretory cells, their axons, the median eminence and the pars nervosa of the bullfrog shows a positive reaction to PAS treatment.The neurohemal area of the median eminence is occupied by many neurosecretory and non-neurosecretory axons, containing neurosecretory granules and/or synaptic vesicles. The axonal portions with the synaptic vesicles which are considered to be the nerve endings abut on the capillaries of the portal system. The size of synaptic vesicles in the axon terminals containing few neurosecretory granules is larger than those in the endings with many neurosecretory granules. Infrequently glial and ependymal processes are interposed between the nerve endings and the capillary wall.In the hilar region of the infundibulum, synapses are frequently observed between the thin fibers with or without neurosecretory granules and dendrites of non-neurosecretory neurons. The probable functions of these synapses are briefly discussed on the basis of our findings. Both in the hilar region of the infundibulum and in the pars nervosa, electron-dense neurosecretory granules of two different sizes were observed. The median eminence contains only one type of granules.The fine structure of the pars nervosa shows similar structures to those of the median eminence. Both in the median eminence and the pars nervosa, the fenestrated endothelium of the capillaries was frequently observed. The thick perivascular connective tissue space containing fibroblasts and collagen fibrils was observed both in the median eminence and the pars nervosa. Vesicles in the cytoplasm of the endothelial cells which appear to take a part in the transendothelial transport were observed.This investigation was supported in part by United States Public Health Service Research Grant, No. A-3678, to Hideshi Kobayashi from the National Institute of Arthritis and Metabolic Diseases and partly by a grant for Fundamental Scientific Research from the Ministry of Education of Japan. The authors wish to express their thanks to Prof. K. Takewaki for his kind encouragement.     

The glial blood-brain barrier of crustacea and cephalopods: a review

1. The glial blood-brain barrier of invertebrates is an accessible, polarised glial layer that permits study of glial cells in their normal relations with neurons. Crayfish 2. The glial "perineurium" forms the blood-brain interface in crayfish, and acts as a barrier to horseradish peroxidase (HRP) and ionic lanthanum. By contrast, the perineurium of the peripheral nervous system is relatively permeable. 3. The ionic permeability of the blood-brain interface can be studied in a sucrose gap chamber, using an extra-cellular microelectrode to monitor the potential across the perineurium following changes in the bathing medium. Subtraction of the microelectrode trace from the sucrose gap records gives the change in the axonal membrane potential. 4. Raised [K+] in the bath causes a complex change in perineurial potential, with the initial transient indicating that the outer (basal) glial membrane is highly K+ selective. The axonal response shows that the time constant for K+ uptake (tau u) and efflux (tau E) across the perineurium of the order of 3-4 min, but the interstitial [K+] in the steady state, [K+] infinity is always less than in the bathing medium. The results are explained by a model incorporating a K+ sink, which may be glial. 5. Strophanthidin and ethacrynic acid have little effect on tau u or K infinity, but cause a rise of tau E. Cold temperature pulses causes changes in the perineurial potential compatible with depolarisation of the inner (apical) membrane. A model is proposed with a Na+-K+-2 Cl co-transporter on the perineurial basal membrane, and an electrogenic Na+-K+-ATPase on the apical.membrane, consistent with results from vertebrate glial/ependymal epithelia. Cephalopods 6. The brain of the cuttlefish Sepia has an extensive system of microvessels. In the vertical and optic lobes studied, a perivascular glial layer forms a barrier to HRP. The occluding structure appears not to be a classical tight junction but may involve condensation of extracellular material. There is no barrier between retinal axons and blood. 7. Studies with radiolabelled polyethylene glycol (PEG4000) and EDTA show that the Sepia blood-brain barrier is as tight as the endothelial barrier of mammals. 8. A modification of the Oldendorf arterial injection technique is used to show that glucose transport at the Sepia barrier is mediated by a Na+-independent hexose carrier resembling that of mammalian red cells and blood-brain barrier. 9. The blood-axon interface fo mantle nerves in the squid Alloteuthis is relatively impermeable to small ions.(ABSTRACT TRUNCATED AT 400 WORDS)     

Synaptic potential in the motor giant axon of the crayfish

Some electrical properties of the synapses between central giant axons (presynaptic) and the motor giant axon (postsynaptic) of the crayfish abdominal nerve cord have been investigated. Postsynaptic potential change in response to presynaptic volleys contains two components: a spike potential and a synaptic potential of very long time course. Amplitude of the synaptic potential is graded according to the number of active presynaptic axons. Conductance increase in the synaptic membrane endures over most of the period of potential change, and it is this rather than the "electrical time constant" of the membrane that in large measure determines the form of the synaptic potential. Temporal summation of synaptic potential occurs during repetitive presynaptic stimulation, and after such stimulation the rate of decay of synaptic potential is greatly slowed.     

Demonstration of the tuberoinfundibular tract of the cat

Summary The distribution of dopaminergic nerve cells in the cat hypothalamus, particularly in the arcuate and periventricular nuclei, and the projections of their axons were studied by fluorescence and electron microscopy after electrothermic coagulation. The majority of these perikarya were located in the arcuate nucleus and the periventricular nucleus dorsocaudal to the optic chiasma. Large lesions caused a wide and diffuse depletion of dopamine fluorescence within the external layer; small lesions caused ipsilateral partial depletion of the dopamine fluorescence. Electron microscopic observations in animals with a lesioned arcuate nucleus revealed that in the external layer degenerating nerve terminals are engulfed by glial processes. In some cases nerve fibers had entirely disappeared and a heavy reactive proliferation of glial processes was observed. Persistence of the form of the median eminence in spite of the extensive degeneration of its nervous elements is considered to depend upon this glial proliferation.Dedicated to Professor W. Bargmann in honour of his 70th birthday     

玉米螟幼虫侧单眼的神经鞘和胶质细胞

用透射电镜观察了欧洲玉米螟Ostrinia nubilalis(Hbner)5龄幼虫侧单眼神经的神经围膜、周神经细胞和其他神经胶质.神经围膜与若干周神经细胞包围若42根轴突.周神经细胞的原生质膜在它们的侧面和内面高度卷曲,并与相邻细胞交错对插,这是细胞与细胞间的特殊连接方式;它们的外面以桥粒和半桥粒固定在神经围膜内面.周神经细胞由神经胶质细胞演化而来,所形成的膜称神经束膜,它与神经围膜组成围在侧单眼神经外面的神经鞘.侧单眼神经内的神经胶质细胞大而平整,具有许多突起物(相当于脊椎动物的少突神经胶质细胞),每一个突起物包被一个感光轴突.神经胶质细胞包被轴突的形式有三种不同的类型:一种是相邻轴突间插入15层神经胶质细胞突起物所形成的普通轴系膜形式,另两种是神经胶质细胞突起物在一个轴突的周围,由一些褶所形成的不同形式.最后,对这些神经胶质细胞以不同形式包被轴突的功能意义进行了讨论.