Outer Dendritic Segments Research Articles

The thermo-/hygrosensitive sensilla of the silkmoth, Bombyx mori: morphological changes after dry- and moist-adaptation

The thermo-/hygrosensitive sensilla styloconica of the silk moth Bombyx mori were studied using cryofixation and freez-substitution. These sensilla are characterized by a short poreless cuticular peg, which is double-walled in its distal part. The central lumen is innervated by the unbranched outer dendritic segments of the two presumed hygroreceptor cells. The presumed thermoreceptor cell displays lamellae below the peg base. Within the peg lumen, the dendrites are surrounded by the peridendritic dense coat and the lowdensity matrix. Below the peg base, these structures continue as the dendrite sheath, which is separated from the outer sensillum-lymph space by a layer of the trichogen cell. The central lumen, therefore, is only connected with the inner sensillum-lymph space, but the appearance of the low-density matrix, within the peg, differs from that of the sensillum lymph below the peg. In moist-adapted (24 h) sensilla, the two hygroreceptor dendrites invade the peg for three quarters and one half of its length, respectively, and fill the cross-sectional area of the lumen by 50–80%. In dry-adapted (24 h) sensilla, the dendrites terminate more proximally and fill the cross-section by ∼35%. The volume of the low-density matrix increases under dry conditions and decreases under humid conditions. At intermediate ambient humidity, the morphology of these sensilla is halfway between the dry-adapted and the moist-adapted state. The effect of dry-adaptation is reversible, so that sensilla that were first dry-adapted and then moist-adapted (24 h each) before cryofixation cannot be distinguished from moist-adapted sensilla. The reduction of the exposed length of the dendrites is interpreted as a shift of the working range of the receptors and/or protection against desiccation. The current theories of sensory transduction in hygroreceptors, in particular the hygrometer and evaporimeter hypotheses, are discussed with respect to the present findings.

Localization of 5?-ectonucleotidase/phosphatase activity within the olfactory sensilla of the spiny lobster, Panulirus argus

Previous electrophysiological studies have shown that the olfactory organ (antennule) of the spiny lobster, Panulirus argus, has external chemoreceptors, which are selectively stimulated by adenosine 5′-monophosphate (AMP) when present in seawater. Subsequent biochemical investigations revealed that AMP can be rapidly dephosphorylated by 5′-ectonucleotidase/phosphatase activity associated with the olfactory sensilla (aesthetascs). In this study the deposition of cerium phosphate was used to examine the ultrastructural distribution of 5′-ectonucleotidase/phosphatase activity in aesthetascs. Utilizing AMP as substrate, we found dephosphorylating activity to be associated with the outer membranes of both dendrites and auxiliary cells. Moreover, this activity was specifically localized to a narrow band that approximately corresponds to the transitional zone where dendrites develop cilia and branch extensively to form the outer dendritic segments. A similar distribution of the cerium phosphate reaction product was found when β-glycerol phosphate was substituted for AMP. The alkaline-phosphatase inhibitor, levamisole, had no apparent effect on the deposition of reaction product when either AMP or β-glycerol phosphate was used as substrate. The ectoenzymatic activity in the transitional zone may be of importance in clearing exogenous chemoexcitatory nucleotides from this region.

Structure and differentiation of the sensilla of the ventral sensory field on the maxillary palps ofPeriplaneta americana (Insecta, Blattodea), paying special attention to the ciliogenesis of the sensory cells

The embryonic development of palpal contact chemosensitive sensilla was studied from 42% of development up to the hatching of the larvae. Ciliogenesis of the sensory cells can be observed at the earliest stages investigated. A complex consisting of two basal bodies and a cap-like ciliary vesicle is localized in the dendritic inner segment. It migrates apically and fuses with the cytoplasmic membrane. At the same time, microtubule doublets of the distal basal body elongate, thus generating the dendritic outer segment. Furthermore, the typical accessory structures of a motile cilium are formed. Although the central pair of microtubules is lacking, the dendritic outer segment can be considered as a modified motile cilium. At about 84% of development the hair structure starts to be formed. Whereas the socket is generated by the tormogen cell, the trichogen cell produces the hair shaft and terminal porus. The dendrite sheath, which rises above the newly formed hair, is attached apically to the embryonic cuticle forming an irregular pore. In larvae and imagines, the inner surface of the dendrite sheath is highly differentiated. A range of circular ledges and filamentous structures wrapping around the dendritic outer segments can be distinguished. These may have a stabilizing function. Furthermore, in cryofixed specimens, the dendritic outer segments possess regularly spaced swellings which are about 1 μm in length and about 0.5 μm in diameter. Their functional significance is still unclear.

Regional sex differences in spine density along the apical shaft of visual cortex pyramids during postnatal development

Dendritic spines from the apical shaft of layer V pyramids were counted on Golgi-stained sections of the monocular subfield of the primary visual cortex of 10-, 20-, 40- and 60-day-old male and female rats. Dendritic segments located in layer IV and at 100–300 μm from the soma had a significantly higher spine content in 10-day-old females when compared to males. This sex difference was extended to outer dendritic segments with increasing age, and became restricted to dendritic segments of outer layers (II–III) located at 400–550 μm from the perikaryon in 40-day-old rats. Sex differences in spine content finally disappear by day 60. These results show the existence of specific laminar and temporal sex differences in the development of dendritic spines in the apical shaft of visual cortex pyramids.

Morphogenesis of the antenna of the male silkmoth. Antheraea polyphemus, III. Development of olfactory sensilla and the properties of hair-forming cells

During adult development of the male silkmoth Antheraea polyphemus, the anlagen of olfactory sensilla arise within the first 2 days post-apolysis in the antennal epidermis (stage 1–3). Approximately on the second day, the primary dendrites as well as the axons grow out from the sensory neurons (stage 4). The trichogen cells start to grow apical processes approximately on the third day, and these hair-forming ‘sprouts’ reach their definite length around the ninth day (stages 5–6). Then the secretion of cuticle begins, the cuticulin layer having formed on day 10 (stage 7a). The primary dendrites are shed, the inner dendritic segments as well as the thecogen cells retract from the prospective hair bases, and the inner tormogen cells degenerate around days 10/11 (stage 7b). The hair shafts of the basiconic sensilla are completed around days 12/13 (stage 7c), and those of the trichoid sensilla around days 14/15 (stage 7d). The trichogen sprouts retract from the hairs after having finished cuticle formation, and the outer dendritic segments grow out into the hairs: in the basiconic sensilla directly through, and in the trichoid sensilla alongside, the sprouts. The trichogen sprouts contain numerous parallel-running microtubules. Besides their cytoskeletal function, these are most probably involved in the transport of membrane vesicles. During the phase of cuticle deposition, large numbers of vesicles are transported anterogradely from the cell bodies into the sprouts, where they fuse with the apical cell membrane and release their electron-dense contents (most probably cuticle precursors) to the outside. As the cuticle grows in thickness, the surface area of the sprouts is reduced by endocytosis of coated vesicles. When finally the sprouts retract from the completed hairs, the number of endocytotic vesicles is further increased and numerous membrane cisterns seem to be transported retrogradely along the microtubules to the cell bodies. Here the membrane material will most probably be used again in the formation of the sensillum lymph cavities. Thus, the trichogen cells are characterized by an intensive membrane recycling. The sensillum lymph cavities develop between days 16–20 (stage 8), mainly via apical invaginations of the trichogen cells. The imago emerges on day 21.

Ultrastructure of a possible new type of crustacean cuticular strain receptor in Carcinus maenas (crustacea, decapoda).

A hitherto unknown sensillum type, the "intracuticular sensillum" was identified on the dactyls of the walking legs of the shore crab, Carcinus maenas. Each sensillum is innervated by two sensory cells with dendrites of "scolopidial" (type I) organization. The ciliary segment of the dendrite is 5-6 μm long and contains A-tubules with an electron-dense core and dynein arm-like protuberances; the terminal segment is characterized by densely packed microtubules. The outer dendritic segments pass through the endo- and exocuticle enclosed in a dendritic sheath and a cuticulax tube (canal), which is suspended inside a slit-shaped cavity by cuticular lamellae. The dendrites and the cavity terminate in a cupola-shaped invagination of the epicuticle. External cuticular structures are lacking. Three inner and four to six outer enveloping cells are associated with each intracuticular sensillum. The innermost enveloping cell contains a large scolopale that is connected to the ciliary rootlets inside the inner dendritic segments by desmosomes. Scolopale rods are present in enveloping cell 2. Since type I dendrites and a scolopale are regarded as modality-specific structures of mechanoreceptors, and since no supracuticular endorgan is present, the intracuticular sensilla likely are sensitive to cuticular strains. The intracuticular sensilla should be regarded as analogous to insect campaniform sensilla and arachnid slit sense organs.

Ultrastructure of the phallic glands of the firebrat, Thermobia domestica (packard) (Thysanura : Lepismatidae)

The exocrine glands located in the penis of Thermobia domestica (Thysanura : Lepismatidae) are composed of about 100 distinct units, each containing several cell types: one large secretory cell with an apical reservoir; 2 groups of envelope cells, an inner group of 2 superimposed cells, and an outer group of 4 cells arranged in a ring, and also 2 basal cells, called ciliary cells owing to their elongated processes, which look like the dendrite of a sensory cell. Each functional unit includes cuticular differentiations: a tubular bristle, fixed on a small tubercle; and a long “internal” ductule communicating basally with the reservoir of the glandular cell and opening distally at the tip of the bristle. A study of the modifications affecting the phallic glands during moulting, shows that the inner envelope cells deposit the cuticle that forms the ductule, the outer envelope cells elaborate the cuticule of the tubercle, while a temporary distal projection of only one of these cells ensures the formation of the bristle. In addition, a lengthening of the outer dendritic segment of the 2 ciliary cells takes place before ductule formation, but this segment partially degenerates after ecdysis. These findings are compared with data already obtained on the morphogenesis of other insect integumental glands. In T. domestica, the secretion of the phallic glands is presumed to be used, during the mating sequences, for spinning fine threads before spermatophore deposition.

Volume and surface of receptor and auxiliary cells in hygro-/thermoreceptive sensilla of moths (Bombyx mori, Antheraea pernyi, and A. polyphemus)

The thermo/hygroreceptive sensilla styloconica of the silkmoths Bombyx mori, Antheraea pernyi, and A. polyphemus were reconstructed from serial sections of cryofixed and chemically fixed specimens. The volume and surface area of the different sensillar cells were calculated from the area and circumference of consecutive section profiles. In addition, data are provided on the length and diameter of the outer and inner dendritic segments of the receptor cells. The morphometric data obtained from the three species are highly consistent and significantly different from those of olfactory sensilla trichodea of the same species. In each sensillum two type-1 receptor cells (hygroreceptors) are associated with one type-2 cell with a lamellated outer dendritic segment, a comparatively thick inner dendritic segment, and a particularly large soma (thermoreceptor). In contrast to olfactory sensilla, the thecogen cell is the largest auxiliary cell forming an extensive apical labyrinth bordering the inner sensillum-lymph space, whereas an inconspicuous trichogen cell and a medium-sized tormogen cell border a comparatively small outer sensillum-lymph cavity. Moreover, both sensillum-lymph spaces are separated from each other not only by the dendrite sheath, but also by the trichogen cell. The results are discussed with regard to recent electrophysiological observations and current hypotheses on the function of sensilla.

The fine structure of thermo-/hygrosensitive sensilla in the silkmoth Bombyx mori: Receptor membrane substructure and sensory cell contacts

The thermo-/hygroreceptive sensilla styloconica of the silkmoth Bombyx mori are located on the tips of the antennal branches. A small poreless cuticular peg is innervated by three sensory cells. The outer dendritic segments of two type-1 receptor cells, the presumed hygroreceptors, almost completely fill the peg lumen and are in close contact with each other. The outer dendritic segment of the third (type-2) receptor cell, the presumed thermoreceptor, forms lamellae below the peg base. The membranes of these lamellae are studded with knobs in orthogonal array, protruding into the extracellular space with the same orientation on facing lamellae. This Bossy Orthogonal Surface Substructure (BOSS) is assumed to play a role in thermoreceptor function. Contacts are observed between the outer dendritic segments, between the inner dendritic segments immediately below the ciliary segments, and between the sensory cell somata. These contacts, which are not found in the olfactory sensilla (s. trichodea and basiconica) of this species, indicate electrical interactions between the three sensory cells of the styloconic sensillum and possibly are involved in the antagonistic and/or bimodal response characteristics of thermo-/hygroreceptor cells.

Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta

The flagellar antenna of the male hawkmoth Manduca sexta carries about 42,000 pheromone-sensitive sensilla trichodea, which are arranged in ‘baskets’ on the single segments. Each sensillum consists of a cuticular hair up to 500 μm long and is innervated by two bipolar sensory neurons. Each neuron sends an unbranched dendrite into the hair shaft. The dendrite is subdivided by a short ciliary region into an inner and an outer segment. The inner segment is especially rich in smooth vesicles, which accumulate beneath the ciliary region where they seem to fuse with the dendritic membrane. The outer dendritic segment often shows conspicuous ‘beads’ along its length. Three auxiliary, or enveloping, cells belong to each adult sensillum. These are the thecogen, the trichogen, and the ‘outer’ cell. Most probably, the latter is not homologous with the ‘traditional’ tormogen cell from a genealogical point of view.

Morphology and ultrastructure of the sensory spine, a presumed mechanoreceptor of Sphaeroma hookeri (Crustacea, Isopoda), and remarks on similar spines in other peracarids.

The isopod Sphaeroma hookeri and many other isopods and peracarids have a sensory spine with laterally inserting sensory hair, positioned in the apical region of the propodal palm of pereopod 1. This spine is innervated by five to eight sensory cells (each giving rise to one cilium) the dendrites of which can be divided into an inner and outer dendritic segment. The cilia are surrounded by an extracellular, electron-dense dendritic sheath. Thirteen enveloping cells are present. The outer dendritic segment (structure beyond the basal bodies) contains two receptor lymph cavities; the inner one lying within the dendritic sheath is homologous with the inner receptor lymph cavity of insects. Scolopales, or tubular bodies, are lacking; their function is probably accomplished by the dendritic sheath. Apically the sensory hair does not have a pore, and the spine is heavily sclerotized. The inner dendritic segment begins with a basal body from which rootlets of different length and thickness extend into the dendrite. In the latter is an accumulation of vesicles. The dendrites keep close contact with other dendrites and the enveloping cells by desmosomal membrane structures. The possible importance of the sensory spine for phylogenetic studies is discussed.

An anomalous sensillum chaeticum with a double set of cilia and outer dendritic segments in Bombyx mori L. (Lepidoptera : Bombycidae)

An anomalous sensillum chaeticum is described in the silkmoth, Bombyx mori (Lepidoptera : Bombycidae), in which each of the 5 inner sensory dendrites gives rise to 2 ciliary and 2 outer dendritic segments. This is interpreted as an atavistic feature, because a double set of cilia is common in sensilla of apterygote insects and of non-insect arthropods. Since all the sensory cells of the sensillum were affected in the same way, determination of the number of cilia and outer segments must have occurred early in morphogenesis, i.e. before the differential cell divisions of the sensory mother cell.

Differences in degeneration of the apical scolopidial organ in the labial palp of Lepidoptera during pupal development

The apical scolopidial organ (ASO) in the labial palp of six species from four families of Lepidoptera was studied in pupal and imaginal stages using electron microscopy. The organ houses three sensory units, each of which consists of one sensory cell and two enveloping cells at early pupal stage in all the species studied. The distal part of the ASO is connected with the epidermis of the tip of the labial palp. Proximally it is attached to the primordium of the palpal nerve. The axons of the sensory cells run within this nerve to the central nervous system. There are two main differences in the differentiation of the ASO in the species examined during postembryonic development: (1) the sensory cells of the ASO degenerate at different rates; and (2) the ASO may or may not change its position within the palp. In Pieris brassicae and Pieris napi (Pieridae), all three sensory cells undergo stepwise degeneration. Consequently, no sensory cells are left in the imago in these species. However, in the Rhodogastria sp. (Arctiidae), only one sensory cell of the ASO degenerates during pupal life. Two remain, therefore, in the imaginal stage. Their dendritic outer segments and axons are normal, and their appearance does not differ from that in early pupal life. The same process was also observed in Rhodogastria bubo (Arctiidae), Autographa gamma (Noctuidae) and Aglais urticae (Nymphalidae). In addition to the degeneration of the sensory cells the ASO turns through about 180° in P. brassicae and P. napi so that its tip points to the base of the palp in the imagines of these species.

Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus

The aesthetascs of the spiny lobster, Panulirus argus, are hair sensilla located on the lateral filaments of the antennules. Each hair is about 0.8 mm long and innervated by about 320 bipolar sensory neurons, the dendrites of which project as a bundle into the hair shaft. Each of the dendrites develops two cilia. Within a very short distance each of these cilia branches repetitively and dichotomously resulting in 8000 to 10000 outer dendritic segments per hair, or about 20 to 30 branches per neuron. The branches intertwine frequently before running to the tip of the hair. Each hair also possesses inner and outer auxiliary cells. The inner auxiliary cells surround the bundle of dendrites, extending distally to the origin of the ciliary segments. Extensions of these cells project into the bundle of dendrites, separating groups of dendrites into discrete clusters. Outer auxiliary cells wrap the inner ones, but do not extend beyond the base of the hair.

Response characteristics of cold cell on the antenna ofLocusta migratoria L.

The dendritic outer segment of the cell which is most likely the cold unit in the poreless coeloconic sensilla onLocusta migratoria antennae, has finger-like projections up to 1.5 μm long and 0.13 μm thick (Fig. 1). This unit responds to constant temperature, to slowly changing temperature and to step changes. Under stationary conditions impulse frequency attained 35 imp/s. Between 14 °C and 41 °C the higher frequencies were associated with the higher temperatures (Fig. 5). In this range the differential sensitivity is positive but not large: + 0.8 (imp/s)/°C. Its resolving power for steady temperature is 4.7 °C. Downward step changes produced by shifting between airstreams at different temperatures yield far higher frequencies (Figs. 2, 3). Step amplitudes were between −0.1 °C and −12 °C; the conditioning temperature from which the steps were initiated, was between 16 °C and 33 °C. Frequency peaked during the first 50 ms after stimulus onset (Fig. 2) and reached its highest values (310–340 imp/s) at initial temperatures above 30 °C and steps larger than −10 °C (Fig. 4). The mean differential sensitivity from 23 curves was −19 (imp/s)/°C and the resolving power 0.6 °C. During slowly changing temperature the impulse frequency was governed by two parameters simultaneously: ambient temperature and its rate of change. Rates were between 0.001 °C/s or less, and 0.03 °C/s in either direction. Frequency was higher during slow cooling at a given temperature than during slow warming (Fig. 6). The average differential sensitivity to the rate of change was −210 (imp/s)/(°C/s). Further, the larger responses to cooling developed at lower ambient temperatures (differential sensitivity: −1.0 (imp/s)/°C). It is to be noted that this sign is negative, in contrast to the sign for differential sensitivity to constant temperature and also for the influence of initial temperature on the response to downward step changes.

Adaptation processes in insect olfactory receptors. Mechanisms and behavioral significance.

Adaptation was studied in single olfactory receptor cells of male moths of Bombyx mori and Antheraea polyphemus. Receptor potential and nerve impulse generators have different and very likely, spatially separate adaptation mechanisms possibly located in the outer dendritic segment and the cell soma, respectively. Restricted portions of the receptor cell dendrite can be locally adapted. The impulse generator may exhibit at least two distinct adaptation processes with different kinetics, as deduced from a consideration of the phasic-tonic response and the different adaptation properties of each of these phases. The response characteristics of cells in the same sensillum are different. The "faster" responding cell types resolve odor pulses with frequencies up to 10 per second--a performance that is probably needed for orientation during flight toward a small odor source.

Fine structure of scorpion trichobothria (Arachnida, Scorpiones)

The fine structure of trichobothria in the scorpions Buthus occitanus (Amoureux, 1789) and Euscorpius carpathicus (Linne, 1767) was investigated by electron microscopy. In both species, cuticular and cellular characteristics are very similar. The articulation of the hair corresponds to that of other arachnid hair sensilla. The receptor endings are excentrically attached to the hair base. They consist of an enveloped S-shaped bundle of seven dendrites in B. occitanus and four in E. carpathicus. Neighbouring outer dendritic segments differ a great deal in diameter and ciliary modification. In B. occitanus, three enveloping cells and several additional secretory cells surround the inner dendritic segments. Structural characteristics are compared to those of other arachnid sensilla and their possible functional significance is discussed.

Ultrastructure of the galeal sensory complex in adults of the Colorado potato beetle, Leptinotarsa decemlineata

ABSTRACT. The structure of galeal sensilla of the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), is described using electron microscopical methods. Previous electro‐physiological studies indicate that these sensilla respond to amino acids, sucrose and plant saps. One physiological type is particularly sensitive to L‐alanine and gamma amino butyric acid (GABA).Three morphologically different types of sensilla occur on the galeal tip. The more numerous apical pegs are not distinguishable from one another on the basis of external structure, although they differ physiologically. Five sensory cells are associated with most apical pegs. One apical peg, the α‐sensillum, contains only four cells. All apical pegs have one cell with a tubular body. The remaining cells have unbranched dendrites and are associated with a single apical pore.Apical hairs differ from the apical pegs by having double innervation. Within the hair shaft, a dendritic sheath is lacking and the sensillar sinus extends to the base of the hair. The function of this hair type is not known.Numerous mechanosensory hairs which surround the other sensilla are singly innervated and contain a tubular body at the level of the outer dendritic segments.

Ultrastructure of the chemosensitive basiconic single-walled wall-pore sensilla on the antennae in adults and embryonic stages of Locusta migratoria L. (Insecta, Orthoptera)

The structure and embryonic development of the two types (A, B) of basiconic sensilla on the antennae of Locusta migratoria were studied in material that had been cryofixed and freeze-substituted, or chemically fixed and dehydrated. Both types are single-walled wall-pore sensilla. Type-A sensilla comprise 20–30 sensory and 7 enveloping cells. One enveloping cell (thecogen cell secretes the dendrite sheath); four are trichogen cells, projections of which form the trichogen process during the 2nd embryonic molt. The trichogen cells form two concentric pairs proximally. Two tormogen cells secrete the cuticular socket of the sensillum. The dendritic outer segments of the sensory cells are branched. Bifurcate type-A sensilla have also been observed. Type-B sensilla comprise three sensory and four enveloping cells (one thecogen, two trichogen and one tormogen). The trichogen process is formed by the two trichogen cells, each of which gives rise to two projections. The trichogen cells are concentrically arranged. The dendritic outer segments of the sensory cells are unbranched. In the fully developed sensillum, all trichogen and tormogen cells border on the outer receptor lymph cavity. It is suggested that the multicellular organization of the type-A sensilla can be regarded as being advanced rather than primitive.

Development of the hair mechanosensilla on the pupal labial palp of the butterfly, Pieris rapae L. (Lepidoptera : Pieridae)

Structure and ontogeny of the hair mechanosensilla on the distal segment of the pupal labial palp of Pieris rapae (Lepidoptera : Pieridae) were investigated in 7 successive stages between 28 hr after pupation and emergence of the imago. There are 7–8 mechanosensilla in the distal region of each palp in both sexes. These sensilla house a single sensory cell characterized by a tubular body, and 3 enveloping cells. At 28 hr after pupation, the anlagen of the hair mechanosensila are visible. Consecutive steps in the formation of the sensilla are: (1) elongation of the outer dendritic segment and of the dendritic sheath; (2) outgrowth of the trichogen cell and cuticle deposition; (3) increase in the diameter of the dendritic outer segment and in the number of microtubules within it; (4) reduction of the distal part of the dendritic outer segment and formation of the tubular body; (5) folding of the membrane of the dendritic outer segment and appearance of the receptor lymph cavity. The tubular body is formed during a period of about 80 hr. Its earliest appearance comprises groups of 3–4 microtubules, which are connected by electron-dense material. The final dense tubular body develops via microtubules linked together by electron-dense material.