Che Chi

The Glial Cells of Insects

To state that neuroglial cells are those ubiquitous companions of neurons is a generality not too helpful in characterizing insect neuroglia. We now know that in insect nervous systems, glial cells are not “ubiquitous” and that naked axons do exist (e.g., Trujillo-Cenoz, 1962). In addition, some types of insect glia are so specialized or evolved that they do not directly contact the neuron, but rather overlie another kind of glial cell, the latter being the true contiguous associate of the neuron.

Membrane specializations in the first optic neuropil of the housefly,Musca domestica L. II. Junctions between glial cells

SummaryThin section and freeze-fracture replicas of the first optic neuropil (lamina ganglionaris) of the flyMusca were studied to determine the types, extent and location of membrane specializations between neurons. Five junctional types are found, exclusive of chemical synapses. These are gap, tight and septate junctions, close appositions between retinular (R) axons and capitate projections (in which an epithelial glial cell invaginates into an R axon). Junctional types and their cellular associations follow: gap junctions, between lamina (L) interneurons, L1–L2; tight junctions, between L1–L2; L3–L4; L4-epithelial glial cell; and R7–R8. Septate junctions, between L1–L2, L3–L4, L3-β, L4-β, α-β, and an unidentified fibre making septate junctions with L1 and L2. Close appositions are found between R axons in the distal portion of the optic cartridges of this neuropil prior to extensive R chemical synapses with L1, L2. These loci (seen in freeze-fracture replicas) have rhomboidal patches of hexagonally arrayed P face particles.Intermembranous clefts between R axons are about 50 Å and are invariably electron lucent. These points of near contact between R terminals are probably the sites of low electrical resistance measured by Shaw (1979). Capitate projections are for the first time revealed in freeze fracture surfaces. Here epithelial glia send many, short, mushroom-shaped processes invaginating into R axons forming a tenacious structural bond. All four membrane leaflets (P and E faces of R axon and glial membrane) in the capitate projection possess particles in higher densities than in the surrounding nonspecialized regions. The known, general functions of each membrane specialization were correlated with the functional capacities of those lamina neurons possessing them in an effort to interpret better the integrative capacity of this neuropil. These data provide some fine structural bases for a putative ‘blood-brain’ barrier between lamina and haemolymph, between lamina and peripheral retina, and possibly between lamina and second optic neuropil.

Close apposition of photoreceptor cell axons in the house fly

Abstract Transmission electron microscopy of the first optic ganglion of the house fly Musca domestica reveals that retinular (R) axons branch and interdigitate throughout the external plexiform layer. Axonal membranes of neighboring cells are in close apposition to each other, usually without junctional modifications. In some cases R axonal membranes exhibit greater electron density in the areas of contiguity. Adjacent axons may show a near confluency of axoplasm at points where membrane boundaries are interrupted or obscured. Physiological implications of these ultrastructural findings are discussed.

Lanthanum and freeze fracture studies on the retinular cell junction in the compound eye of the housefly

SummaryThe retinular (R) cell junction between adjacent photoreceptor cells in the house-fly ommatidium was characterized by freeze fracture, thin section and tracer (lanthanum) studies. Focal tight junctions occur between cells, and some P face ridge-E face groove correspondences are present in this intramembranal area. When colloidal lanthanum was introduced into the extracellular space (ECS) of the peripheral retina of the housefly, this electrondense tracer moved from the ECS (extra-ommatidial space), through the R-cell junctions and belt desmosomes, into the ommatidial cavity (OC = intrarhabdomal space) of each ommatidium. In the OC, lanthanum outlined a meshwork structure that pervaded this space. The evidence of this tracer movement suggests that there may be ionic continuity between the “traditional” ECS and the fluid bathing the individual rhabdomeres. The volume of the OC is calculated and we suggest that this space is part of the ECS. The functional implications of this postulate are considered in the light of: (1) the different functions of the peripheral and central cells; (2) the dissimilarity of rhabdomal membrane surface facing the OC compared to the “unmodified” plasma membrane of the photoreceptor cell facing the extra-ommatidial cavity; (3) the permeability properties of the R cell junction; and (4) the total ECS containing an ion store capable of sustaining current for the generator potential.

Membrane specializations in the peripheral retina of the housefly Musca domestica L.

SummaryMembrane specializations of the peripheral retina of the housefly (Musca domestica) are revealed in thin sections and freeze fracture/etch replicas. Septate junctions are abundant in corner areas of the pseudocone enclosure bonding: between homologous corneal pigment cells (CPC); between homologous large pigment cells (LPC); between CPC-LPC; between Semper cells (SC); between SC-CPC. Spot desmosomes are present between Semper cells. It is likely that septate junctions function as strengthening adhesions in this area. A new membrane specialization similar to a continuous junction was observed between retinular cells of the same or adjacent ommatidium. This junction has indistinct septa in the 115Å intermembrane cleft and is intermittent in character. When this junction is absent, the apposed cells gape apart. In freeze fracture studies, this junction is characterized by bridges composed of fused membrane particles and randomly arranged particles on the P face, and non-corresponding grooves on the E face. The ridges are elongate and roughly parallel and sometimes they form enclosures. Mitochondria line up along these junctions, often within 90Å of the unit membrane. This membrane specialization has characteristics of tight and continuous junctions. In line with previous findings, we suggest that this junction assists in retinular cell orientation, possibly in enforcing the ommatidial twist and in maintaining localized ionic concentration gradients between retinular cells.

The perineurium of the adult housefly: Ultrastructure and permeability to lanthanum

SummaryThe ultrastructure of the perineurial cells of Musca overlying the first optic neuropile was examined by transmission electron microscopy. These cells are somewhat similar to those of other insects but cytoplasmic flanges seem to be absent, and mitochondria are relatively large and sinuous. The intercellular channel system on the lateral border of the cells is relatively spacious and highly meandering. Perineurial cells are joined by septate, gap, and tight junctions, hemidesmosomes, and desmosomes. Tight and septate junctions bond perineurial cells and glial cells. These data are evaluated on the basis of tracer studies with lanthanum. This material penetrates the extracellular space between perineurium and underlying glial and nerve cells, between epithelial glial cells and retinular axon terminals (capitate projections), and between the α-β fiber pair in the optic cartridge (gnarls). If no damage occurs to the perineurial cells during tissue preparation, this passage of lanthanum to neuronal surfaces indicates that the blood brain barrier is incomplete in this restricted area. Supportive evidence for such permeance is based on electrophysiological data, considerations of membrane specializations in the optic neuropile, and Na+/K+ ratios of dipteran hemolymph.

Ordered membrane particles in rhabdomeric microvilli of the housefly (Musca domestica L.)

Rhabdomeric microvilli of the housefly were freeze‐fractured (FF) and thin sectioned (TS) for ultrastructural examination. Ordered files of closely packed membrane particles (82 Å wide, 250 Å long) were seen (FF) on the microvillar membrane (usually E face). The long axis of each particle was canted about 45° to that of the microvillus. Occasionally particles in this array appeared on the P face. It is hypothesized that ordered particles may represent either a photopigment precursor stock, a second photolabile pigment, or the newly discovered sensitizing, UV‐absorbing, photostable visual pigment. In the underlying membrane leaflet (P face) were found spherical (85 Å diameter) unoriented particles in a concentration of about 6,000/μm2. The size, shape and density of these structures are compatible with those of rhodopsin particles. These particles also covered the basal area of each microvillus. The findings from TS material were difficult to correlate with those from FF replicas. At high magnification the former showed that the plasma membrane of the transected microvillus is composed of spherical, hollow subunits (averaging 43 Å diameter), sometimes fused to form double, 86 Å units. These substructures were closely packed and continuous around the microvillus. This beaded plasma membrane, in rare cases, was doubled around the microvillus. In other instances the plasma membranes were continuous between neighboring microvilli. The physiological implications of these ultrastructural features are discussed.

Surface fine structure of the eye of the housefly (Musca domestica): Ommatidia and lamina ganglionaris

SummaryThe compound eye of the housefly, from lens to first optic neuropile (lamina ganglionaris) was examined with a scanning electron microscope. Key findings are as follows: The pseudocone cavity is enclosed by six corneal pigment cells. The nuclei of the six cells are firmly anchored to the underside of the lens and portions remain after lens delamination from the pseudocone cavity. An eccentrically-positioned, short photoreceptor cell was observed near the region where the inferior central cell initiates its rhabdom. This eminence may represent that cells soma. The basement membrane is revealed as a two-tiered, fibrous layer with ovoid fenestrations. Each opening is sealed with a diaphragm perforated by eight retinular axons and a trachea. Conjoined distal surfaces of the satellite glial cells form a membrane-like barrier immediately underlying the basement membrane. Monopolar somata from the lamina are covered with glial cells which possibly make more intimate contact with the somata through miniscule projections. Optic cartridges with monopolar interneurons were noted. Spherical to slightly biconcave processes of these interneurons contact retinular axons. Very fine (1000 Å) filaments interweave among and contact lateral processes. Further implications are discussed as they relate to observed structures.

The housefly interfacetal hair

SummaryThe external and internal fine structure of the housefly interfacetal hair and its sensory dendrite was studied with the scanning and transmission (high and low voltage) electron microscopes. The hair shaft contains no dendrites, and is usually situated within a socket on the lens surface. Immediately beneath and directly connected to the base of each hair is a bipolar neuron whose dendrite tip is enveloped in a sheath cell which, in turn, is surrounded by a second sheath cell. Septate junctions are seen between all these cells and contiguous portions of a large pigment cell. At the hair base, the dendrite of the neuron terminates in a tubular body only 1.5 μm in diameter which is filled with about 400 microtubules in highly ordered (in parallel pentagonal and hexagonal) arrays and whose sides are fused to neurofilaments in parallel. Another filament (ca. 70 Å diameter) is in the center of each microtubule-neurofilament polygon. Structures proximal to the tubular body are typical for a scolopoid sensillum, i.e., connecting cilium (9×2+0 microtubules) with rootlet and basal bodies, unmodified dendrite, perikaryon and axon. The axon has not been traced to its synapse. The high degree of internal organization and shortness of the tubular body, as well as its eccentric insertion into the hair shaft lead to the hypothesis that this hair may be a highly sensitive mechanoreceptor. On the basis of their single innervation, these hairs could monitor flight speed from the degree of hair deflection caused by wind in general or particular laminar air currents flowing past the eyes during flight.

The Photoreceptor Cells

Insect photoreceptor cells are usually slender, cylindrical, and aggregated into various species-specific combinations beneath the corneal lens of a compound eye, ocellus, or larval stemmata. Individual cells are so sensitive to light that some are able to signal catches of a single photon (e.g., Lillywhite, 1977). This exquisite sensitivity is founded on the presence of an incompletely characterized glycoprotein (rhodopsin). Rhodopsin is the functional molecule of the photoreceptor cell, and is the major constituent of the plasma membrane of the rhabdomeric microvilli. This photopigment-containing organelle (rhabdomere) is found in the distal region of the cell (Section 5). In its more proximal reaches, the cell becomes a functional neuron with an axon (Section 7) conveying graded depolarizations to chemical and electrical synapses (Section 8).