Nonclassical neuronal communications

Examples from classical neuronal communications are discussed in the light of biochemical and anatomical data. These are the nonsynaptic axo-axonic interactions of the enkephalinergic neurons on nerve terminals of peptidergic primary sensory afferents and dopaminergic nigrostriatal fibers. Examples of dendrites as presynaptic sites are discussed in three very different situations, namely, the dopaminergic dendrites of the substantia nigra neurons, the gamma-aminobutyric acid--ergic dendrites involved in reciprocal dendro-dendritic synapses in the olfactory bulb, and the peripheral branches of the substance P-containing primary sensory neurons.     

Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion

BACKGROUND: Understanding how dendrites establish their territory is central to elucidating how neuronal circuits are built. Signaling between dendrites is thought to be important for defining their territories; however, the strategies by which different types of dendrites communicate are poorly understood. We have shown previously that two classes of Drosophila peripheral da sensory neurons, the class III and class IV neurons, provide complete and independent tiling of the body wall. By contrast, dendrites of class I and class II neurons do not completely tile the body wall, but they nevertheless occupy nonoverlapping territories. RESULTS: By developing reagents to permit high-resolution studies of dendritic tiling in living animals, we demonstrate that isoneuronal and heteroneuronal class IV dendrites engage in persistent repulsive interactions. In contrast to the extensive dendritic exclusion shown by class IV neurons, duplicated class III neurons showed repulsion only at their dendritic terminals. Supernumerary class I and class II neurons innervated completely overlapping regions of the body wall, and this finding suggests a lack of like-repels-like behavior. CONCLUSIONS: These data suggest that repulsive interactions operate between morphologically alike dendritic arbors in Drosophila. Further, Drosophila da sensory neurons appear to exhibit at least three different types of class-specific dendrite-dendrite interactions: persistent repulsion by all branches, repulsion only by terminal dendrites, and no repulsion.     

The organization of the malleolar sensory system in the solpugid, Chanbria sp

Five malleoli extend ventrally from the proximal segments of each hind leg of mature and immature solpugids. Each malleolus contains the dendrites of 72,000 bipolar sensory neurons with somata in a ganglion in the leg just dorsal to the malleolus. The dendrites terminate in a sensory groove which extends along the ventral edge of the sense organ. The sensory groove has a slit-like opening to the outside, suggesting that these sense organs are chemoreceptors. The malleoli also contain long processes from microvillar cells with somata in the sensory ganglion. The microvillar cell processes extend into the malleolus to the ciliary ending of the dendrites where each process has an enlarged microvillar ending which surrounds the outer segments of 15 to 22 dendrites and releases a sense secretion.     

Microtubules have opposite orientation in axons and dendrites of Drosophila neurons

In vertebrate neurons, axons have a uniform arrangement of microtubules with plus ends distal to the cell body (plus-end-out), and dendrites have equal numbers of plus- and minus-end-out microtubules. To determine whether microtubule orientation is a conserved feature of axons and dendrites, we analyzed microtubule orientation in invertebrate neurons. Using microtubule plus end dynamics, we mapped microtubule orientation in Drosophila sensory neurons, interneurons, and motor neurons. As expected, all axonal microtubules have plus-end-out orientation. However, in proximal dendrites of all classes of neuron, approximately 90% of dendritic microtubules were oriented with minus ends distal to the cell body. This result suggests that minus-end-out, rather than mixed orientation, microtubules are the signature of the dendritic microtubule cytoskeleton. Surprisingly, our map of microtubule orientation predicts that there are no tracks for direct cargo transport between the cell body and dendrites in unipolar neurons. We confirm this prediction, and validate the completeness of our map, by imaging endosome movements in motor neurons. As predicted by our map, endosomes travel smoothly between the cell body and axon, but they cannot move directly between the cell body and dendrites.     

Establishment of vagal sensorimotor circuits during fetal development in rats

The differentiation of vagal motor neurons and their emerging central relationship with vagal sensory afferents was examined in fetal rats. To identify peripherally projecting sensory and motor neurons, 1,1′-dioctadecyl 3,3,3′,3′-tetramethylindocarbocyanine perchloarate (DiI) was inserted into the proximal gut or cervical vagus nerve in fixed preparations. At embryonic day (E) 12, labeled vagal sensory neurons are present in the nodose ganglia and a few sensory axons project into the dorsolateral medulla. Central sensory processes become increasingly prevalent between E13 and E14 but remain restricted to the solitary tract. Vagal motor neurons are first labeled at E13, clustered within a region corresponding to the nucleus ambiguus (NA). Additional motor neurons appear to be migrating toward the NA from the germinal zone of the fourth ventricle. Motor neurons in the dorsal motor nucleus of the vagus (DMV) first project to the gut at E14 and have processes that remain in physical contact with the ventricular zone through E16. Sensory axons emerge from the solitary tract at E15 and project medially through the region of the nucleus of the solitary tract (NST) to end in the ventricular zone. A possible substrate for direct vagovagal, sensorimotor interaction appears at E16, when vagal sensory fibers arborize within the DMV and DMV dendrites extend into the NST. By E18, the vagal nuclei appear remarkably mature. These data suggest specific and discrete targeting of vagal sensory afferents and motor neuron dendrites in fetal rats and define an orderly sequence of developmental events that precedes the establishment of vagal sensorimotor circuits. © 1993 John Wiley & Sons, Inc.     

Histology and ultrastructure of the olfactory organ of the freshwater pulmonate Helisoma trivolvis

Summary The olfactory organ of Helisoma trivolvis is located on the surface of the body at the base of the cephalic tentacles. An evagination of skin, the olfactory plica, at the base of the tentacle extends over the olfactory organ dorsally. The epithelium of the olfactory organs contains unspecialized epithelial cells, ciliated epithelial cells, basal cells, mucous secretory cells, and sensory dendrites. The surface of the epithelium has a complex brush border of thick plasmatic processes, which branch to form several terminal microvillar twigs. Long slender cytoplasmic processes form a dense spongy layer among the plasmatic processes beneath the level of the terminal twigs. Bipolar primary sensory neurons clustered beneath the epithelium of the olfactory organ send dendrites through the epithelium to the free surface. Some sensory endings have a few short cilia, but most bear only microvilli. Cilia of sensory endings and epithelial cells extend beyond the brush border of the epithelium. Small axons arise from the perikarya of the sensory neurons and enter a branch of the olfactory nerve. HRP tracing indicates that the axons pass to the cerebral ganglion without interruption. Histochemical tests indicate that the sensory neurons are neither aminergic nor cholinergic.     

Transplantation of neurons reveals processing areas and rules for synaptic connectivity in the cricket nervous system

In order to assess the nature of spatial cues in determining the characteristic projection sites of sensory neurons in the CNS, we have transplanted sensory neurons of the cricket Acheta domesticus to ectopic locations. Thoracic campaniform sensilla (CS) function as proprioceptors and project to an intermediate layer of neuropil in thoracic ganglia while cercal CS transduce tactile information and project into a ventral layer in the terminal abdominal ganglion (TAG). When transplanted to ectopic locations, these afferents retain their modality-specific projection in the host ganglion and terminate in the layer of neuropil homologous to that of their ganglion of origin. Thus, thoracic CS neurons project to intermediate neuropil when transplanted to the abdomen and cercal CS neurons project to a ventral layer of neuropil when transplanted to the thorax. We conclude that CS can be separated into two classes based on their characteristic axonal projections within each segmental ganglion. We also found that the sensory neurons innervating tactile hairs project to ventral neuropil in any ganglion they encounter after transplantation. Ectopic sensory neurons can form functional synaptic connections with identified interneurons located within the host ganglia. The new contacts formed by these ectopic sensory neurons can be with normal targets, which arborize within the same layer of neuropil in each segmental ganglion, or with novel targets, which lack dendrites in the normal ganglion and are thus normally unavailable for synaptogenesis. These observations suggest that a limited set of molecular markers are utilized for cell–cell recognition in each segmentally homologous ganglion. Regenerating sensory neurons can recognize novel postsynaptic neurons if they have dendrites in the appropriate layer of neuropil. We suggest that spatial constraints produced by the segmentation and the modality-specific layering of the nervous system have a pivotal role in determining synaptic specificity. © 1993 John Wiley & Sons, Inc.     

Morphological differentiation of the embryonic peripheral neurons in Drosophila

Summary The stereotyped segmental and dorso-ventral organization of the peripheral nervous system (PNS) of Drosophila embryos allows the identification of all the neurons in the body wall. Distinct classes of neurons are distinguishable according to their location, the targets they innervate, the particular shape of their dendrites and their cell size. Those neurons innervating external sensory structures (es) and chordotonal organs (ch) have single dendrites and have been previously described (Ghysen et al. 1986; Dambly-Chaudiere and Ghysen 1986; Campos-Ortega and Hartenstein 1985). We describe here the identity and morphological features of three other classes of neurons in the body segments which have multiple dendrites (md neurons): 1) neurons that give rise to elaborate dendritic arborisations (da neurons); 2) neurons that have bipolar dendrites (bd neurons); 3) neurons that arborize around particular tracheal branches (td neurons). The thoracic hemisegment (T2 and T3) contains 13 da, one bd, one td, 21 es and four ch neurons; the abdominal hemisegment (A1 to A7) contains 14 da, three bd, three td, 15 es and eight ch neurons. The arrangement of the segmented peripheral neurons is highly invariant and provides a favorable assay system for the genetic analysis of neurodevelopment.     

Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons

Functionally similar neurons can share common dendrite morphology, but how different neurons are directed into similar forms is not understood. Here, we show in embryonic and larval development that the level of Cut immunoreactivity in individual dendritic arborization (da) sensory neurons correlates with distinct patterns of terminal dendrites: high Cut in neurons with extensive unbranched terminal protrusions (dendritic spikes), medium levels in neurons with expansive and complex arbors, and low or nondetectable Cut in neurons with simple dendrites. Loss of Cut reduced dendrite growth and class-specific terminal branching, whereas overexpression of Cut or a mammalian homolog in lower-level neurons resulted in transformations toward the branch morphology of high-Cut neurons. Thus, different levels of a homeoprotein can regulate distinct patterns of dendrite branching.     

A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb

The mammalian vomeronasal system is specialized in pheromone detection. The neural circuitry of the accessory olfactory bulb (AOB) provides an anatomical substrate for the coding of pheromone information. Here, we describe the axonal projection pattern of vomeronasal sensory neurons to the AOB and the dendritic connectivity pattern of second-order neurons. Genetically traced sensory neurons expressing a given gene of the V2R class of vomeronasal receptors project their axons to six to ten glomeruli distributed in globally conserved areas of the AOB, a theme similar to V1R-expressing neurons. Surprisingly, second-order neurons tend to project their dendrites to glomeruli innervated by axons of sensory neurons expressing the same V1R or the same V2R gene. Convergence of receptor type information in the olfactory bulb may represent a common design in olfactory systems.     

Spindle-F Is the Central Mediator of Ik2 Kinase-Dependent Dendrite Pruning in Drosophila Sensory Neurons

During development, certain Drosophila sensory neurons undergo dendrite pruning that selectively eliminates their dendrites but leaves the axons intact. How these neurons regulate pruning activity in the dendrites remains unknown. Here, we identify a coiled-coil protein Spindle-F (Spn-F) that is required for dendrite pruning in Drosophila sensory neurons. Spn-F acts downstream of IKK-related kinase Ik2 in the same pathway for dendrite pruning. Spn-F exhibits a punctate pattern in larval neurons, whereas these Spn-F puncta become redistributed in pupal neurons, a step that is essential for dendrite pruning. The redistribution of Spn-F from puncta in pupal neurons requires the phosphorylation of Spn-F by Ik2 kinase to decrease Spn-F self-association, and depends on the function of microtubule motor dynein complex. Spn-F is a key component to link Ik2 kinase to dynein motor complex, and the formation of Ik2/Spn-F/dynein complex is critical for Spn-F redistribution and for dendrite pruning. Our findings reveal a novel regulatory mechanism for dendrite pruning achieved by temporal activation of Ik2 kinase and dynein-mediated redistribution of Ik2/Spn-F complex in neurons.     

The hair-peg organs of the shore crab,Carcinus maenas (Crustacea,Decapoda): Ultrastructure and functional properties of sensilla sensitive to changes in seawater concentration

Summary The hair-peg organs of the shore crab, Carcinus maenas, are modified hair-sensilla. A small hair shaft (peg) is surrounded by a tuft of solid cuticular bristles (hairs). Each hair-peg organ is innervated by 6 sensory neurons, 2 of which have scolopidial (type-I) dendrites. The outer segments of all dendrites pass through a cuticular canal extending to the articulated hair base in which the 2 type-I dendrites terminate. The other 4 (type-II) dendrites reach the clavate tip of the hair shaft and have access to a terminal pore and a large sickle-shaped aperture. Three inner and 8–12 outer enveloping cells belong to a hair-peg organ. The innermost enveloping cell contains a scolopale, which has desmosomal connections to the ciliary rootlets of the type-I dendrites. An inner and an outer sensillum lymph space are present. The ultrastructural features of the dendrites and the cuticular apparatus indicate that the hair-peg organs are bimodal sensilla, comprising 2 mechano- and 4 chemosensitive sensory neurons. Extracellular recordings from the leg nerve indicate that the chemosensitive neurons of the hair-peg organs respond to changes in seawater concentration in the physiological range of Carcinus maenas.Supported by the Deutsche Forschungsgemeinschaft (SFB 45/A1; W. Gnatzy)     

The ultrastructure of the sensory cells in the chemoreceptor of the ommatophore of Helix pomatia L.

Most of the sensory cells found in the chemoreceptor of the ommatophore of Helix pomatia are typical bipolar cells. The chemoreceptor is deveded by a furrow into two parts; within the ventral subdivision the layer of sensory cell bodiesis thicker than in the dorsal part. According to the differentiations of the apical surface of the dendrites, it is possible to distinguish six different classes: a) dendrites with one cilium and 75 nm thick cytofila (sometimes dendrites of identical appearance posses more than one cilium); b)dendrites with several cilial and 150 nm thick cytofila; c) dendrites with several cilia, 50 nm thick cytofila, and long, striated rootlets; d) dendrites with several cilia bur without cytofila; e) dendrites with 130 nm thick cytofila but without cilia; and f) dendrites with 65 nm thick cytofila but without cilia; dendrites of this class are the only ones with a cytoplasm more electron dense than that of the surrounding supporting cells. All these dendrites are connected to the surrounding supporting cells by terminal bars, each consisting of zonula adhaerens, aonula intermedia and zonula septata. The perikarya of the sensory cells measure approximately 15 mum by 8 mum and enclose 10 mum by 6 mum large nuclei. Axons, originating from these perikarya, extend to the branches of the digital ganglion. In the distal part of this gangloin the axons come into synaptic contact with interneurons, but in our electron micrography it was not possible to coordinate processes and synapses with the corresponding neurons.     

Immunolabeled neuroactive substances in the osphradium of the pond snail Lymnaea stagnalis

The osphradium of molluscs is assumed to be a sensory organ. The present investigation in Lymnaea stagnalis has established two ultrastructurally different types of dendrites in the sensory epithelium. Cells immunoreactive to leucine-enkephalin and FMRFamide send processes to the sensory epithelium. These neurons of the osphradial ganglion are thus considered to be part of the sensory system, as are methionine-enkephalin-immunoreactive cells in the mantle wall in the vicinity of the osphradium. The complexity of the osphradial ganglion is further demonstrated by serotonin-immunoreactive neurons innervating the muscular coat around the osphradial canal and methionine-enkephalin-immunoreactive cells sending projections to the central nervous system.     

Labial tip sensilla of Blissus leucopterus leucopterus (Hemiptera: Blissidae): Ultrastructure and behavior

The cuticular sensory receptors that are found on the apex of the labium of hemipterans play an important role in their feeding behavior. In this study we describe the ultrastructure, number, and distribution of sensilla on the labium apex of the chinch bug, Blissus leucopterus leucopterus. Each apical field of sensilla on the labium contains 11 uniporous peg sensilla and one sensillum chaeticum. The uniporous peg sensilla are innervated by 4–5 bipolar neurons that send dendrites in the lumen of each peg. Three neurons are associated with each sensillum chaeticum, two neurons have dendrites in the lumen of the sensillum, and the third dendrite ends in a tubular body at the base of the sensillum. Behavioral tests that involve chemical blockage of the sensory receptors show the importance of the labial sensilla in feeding behavior. Both morphological and behavioral evidence indicate that the labial sensilla have a chemosensitive function.     

Morphology and ultrastructure of the organ of Bellonci in the marine amphipod Gammarus setosus

The three-dimensional structure of the organ of Bellonci in the marine amphipod Gammarus setosus and the relationship between its sensory cells and concretion are described using light, transmission, and scanning electron microscopy, with chemical treatment for cell lysis, calcium chelation, glycogen staining, and lanthanum labelling. The organ is encapsulated and has three units called fuselli. Each is enclosed by two fusellar cells which generate and release calcium granule strands into the cores of the fusellar concretions, which are united in the center of the organ. The surface of each fusellus is traversed by spiral dendrites entering dorsally and ending ventrally. The spiral dendrites arise from sensory neurons contained in a palm-shaped ganglion in the center of the capsule, beyond which they are twisted like a rope before reaching the concretion. The spiral dendrites are linked in pairs by gap and tight junctions and each gives origin to two pairs of 9+0 sensory cilia 30 μm apart. The ciliary distal segments give rise to long tubules which are in contact with the calcium granule strands. The ciliary proximal segments are expanded by many long mitochondria which interdigitate with the branched striated ciliary rootlets. The concretion is suspended in the capsule cavity by axons originating from four neurons of a remote mechanoreceptor. The structure of the organ suggests that it is a sensory organ involved in the reception and integration of a variety of stimuli.     

Signaling mechanisms underlying dendrite formation

During development, the nervous system is confronted with a problem of enormous complexity; to progress from a large number of 'disconnected' neurons to a network of neuronal circuitry that is able to dynamically process sensory information and generate an appropriate output. To form these circuits, growing axons must make synapses with targets, usually the dendrites of postsynaptic neurons. Although a significant amount is known about the signals that regulate and guide developing axons, we are only now starting to understand how environmental cues like growth factors and activity regulate the formation and maintenance of dendrites in the developing and mature nervous system.     

Intracellular motility: A special delivery service

Recent studies have identified a delivery service that operates in specialised cell appendages: two motor proteins and a novel protein organelle use axonemal microtubules as tracks to shuttle essential components to the tips of flagella and the dendrites of sensory neurons.