Types Of Receptor Neurons Research Articles

Structure and diversity in mammalian accessory olfactory bulb

The accessory olfactory bulb (AOB) is the first neural integrative center for the olfactory-like vomeronasal sensory system. In this article, we first briefly present an overview of vomeronasal system organization and review the history of the discovery of mammalian AOB. Next, we briefly review the evolution of the vomeronasal system in vertebrates, in particular the reptiles. Following these introductory aspects, the structure of the rodent AOB, as typical of the well-developed mammalian AOB, is presented, detailing laminar organization and cell types as well as aspects of the homology with the main olfactory bulb. Then, the evolutionary origin and diversity of the AOB in mammalian orders and species is discussed, describing structural, phylogenetic, and species-specific variation in the AOB location, shape, and size and morphologic differentiation and development. The AOB is believed to be absent in fishes but present in terrestrial tetrapods including amphibians; among the reptiles AOB is absent in crocodiles, present in turtles, snakes, and some lizards where it may be as large or larger than the main bulb. The AOB is absent in bird and in the aquatic mammals (whales, porpoises, manatees). Among other mammals, AOB is present in the monotremes and marsupials, edentates, and in the majority of the placental mammals like carnivores, herbivores, as well as rodents and lagomorphs. Most bat species do not have an AOB and among those where one is found, it shows marked variation in size and morphologic development. Among insectivores and primates, AOB shows marked variation in occurrence, size, and morphologic development. It is small in shrews and moles, large in hedgehogs and prosimians; AOB continues to persist in New World monkeys but is not found in the adults of the higher primates such as the Old World monkeys, apes, and humans. In many species where AOB is absent in the adult, it often develops in the embryo and fetus but regresses in later stages of development. Finally, new areas in vomeronasal system research such as the diversity of receptor molecules and the regional variation in receptor neuron type as well as in the output neurons of the AOB and their projection pathways are briefly discussed. In view of the pronounced diversity of size, morphologic differentiation, and phylogenetic development, the need to explore new functions for the vomeronasal system in areas other than sexual and reproductive behaviors is emphasized. Microsc. Res. Tech. 43:476–499, 1998. © 1998 Wiley-Liss, Inc.

The macroglomerular complex of the antennal lobe in the tobacco budworm moth Heliothis virescens : specified subdivision in four compartments according to information about biologically significant compounds

The functional organisation of the male specific macroglomerular complex in Heliothis virescens has been studied by tip recordings of sensilla trichodea type 1 combined with cobalt-lysine stainings and by intracellular recordings of antennal lobe projection neurons combined with neurobiotin stainings. The antennal lobe, the macroglomerular complex and the stained axons/dendrites were reconstructed by camera-lucida. Some were further computer reconstructed in three dimensions. The results showed that: 1) The macroglomerular complex consisted of four anatomically separated compartments; 2) A large compartment (the cumulus) at the entrance of the antennal nerve received input from receptor neurons responding to the major pheromone component; 3) Another large compartment, located dorso-medially of the cumulus (the dorso-medial compartment) received input from receptor neurons tuned to the second pheromone component; 4) Two ventrally located compartments received input from two receptor neuron types, co-localized in the same sensillum. Each neuron type responded strongest to one of two interspecifically acting signals, shown to interrupt the pheromone attraction. 5) The function of the dorso-medial compartment was further verified by selective arborizations in this compartment by a projection neuron showing strong response to antennal stimulation with the second pheromone component. At low concentration, the neuron responded synergistically to stimulation with the binary pheromone mixture.

Inhibitory receptor binding events among the components of complex mixtures contribute to mixture suppression in responses of olfactory receptor neurons of spiny lobsters.

Responses of olfactory receptor neurons of spiny lobsters Panulirus argus to two-component mixtures can be shaped by inhibitory events such as odor-activated hyperpolarizations and inhibition of odor-receptor binding (Daniel et al. 1996). In the current study, we extend this analysis to complex mixtures by examining responses of spiny lobster olfactory receptor neurons to mixtures containing up to seven odorants, consisting of adenosine-5'-monophosphate, ammonium, betaine, L-cysteine, L-glutamate, DL-succinate, and taurine. The response to a mixture was often less than the response to its most excitatory component. The effect of adding an excitatory odorant to a mixture depended on olfactory receptor neuron type, composition of the mixture, and which compound was added. In some cases the added excitatory compound had no effect or even decreased the mixture's response intensity, thus demonstrating nonlinear contributions of the components. Response intensities predicted by a noncompetitive model, which is most representative of these olfactory receptor neurons, were improved when the model included a term for empirical measurements of inhibitory binding interactions, suggesting that inhibitory binding interactions are one mechanism contributing to mixture suppression. This model's predictions were accurate for binary mixtures but not for larger mixtures, suggesting that additional inhibitory mechanisms are needed to account for mixture interactions in complex mixtures.

Receptor neuron responses to potential sex pheromone components in the caddisfly Rhyacophila nubila (Trichoptera: Rhyacophilidae)

Olfactory single sensillum responses of male and female caddisflies Rhyacophila nubila (Trichoptera: Rhyacophilidae) were examined with the tungsten penetration technique to investigate the presence of receptor neurons tuned to potential sex pheromone components. The compounds tested in the experiment were heptan-2-one, nonan-2-one, ( R)-heptan-2-ol, and ( R)-nonan-2-ol, which have all been found to be present in female abdominal glands, plus the two antipodes ( S)-heptan-2-ol and ( S)-nonan-2-ol. Four types of receptor neurons were found in equal proportions in males and females. One type responded primarily to heptan-2-one. A second type responded primarily to ( R)-heptan-2-ol and a third type primarily to its enantiomer ( S)-heptan-2-ol. The fourth type of receptor neuron responded to nonan-2-one, ( R)-nonan-2-one, and ( S)-nonan-2-ol, with a bias to nonan-2-one. The receptor neurons responding to the tested compounds made up a great majority of the contacted neurons in both males and females.

Encoding of plant odours by receptor neurons in the pine weevil (Hylobius abietis) studied by linked gas chromatography-electrophysiology

Receptor neuron responses to plant volatiles, trapped by head-space procedures, were examined in the pine weevil Hylobius abietis, using gas chromatography linked with electrophysiological recordings from single neurons. Seventy-two receptor neurons were tested 173 times for various plant volatile mixtures, either via a polar or a non-polar column. 1) All responses appeared as increased firing rates which followed the concentration profiles of the GC-eluted compounds. 2) The neurons were classified separately for the two column types in 17 and 19 groups respectively, according to the compounds they responded to. It suggests that the plant odour information is encoded by a large, but limited number of receptor neuron types. 3) Most neurons responded to a limited number of compounds (1–5) and showed a marked best response to one of them, whereas additional responses to several other components which seems to be structurally similar, was recorded for some neurons. It suggests that the plant odour receptor neurons are rather narrowly than broadly tuned, and that each neuron is specialized for receiving information about one or a few related compounds. 4) Most neurons responded to monoterpenes, whereas the other neurons responded to compounds of other categories. 5) Both major and minor plant volatile components activated specifically receptor neurons.

The significance of major pheromone components and interspecific signals as expressed by receptor neurons in the oriental tobacco budworm moth, Helicoverpa assulta

Receptor neuron specificities for intra- and interspecific chemical signals were determined in males of Helicoverpa assulta, by testing single neurons for twelve heliothine produced compounds and two chemical analogues. Three types of receptor neurons were identified in the male specific sensilla trichodea type 1. 1. One large group of neurons (29 out of 63) was tuned to the major pheromone component (Z)-9-hexadecenal, in contrast to results obtained previously in a related species, where the information from this compound seems to be mediated via neurons tuned to (Z)-9-tetradecenal. 2. Another group of neurons (28/63) was tuned to (Z)-9-tetradecenal which is not produced by the conspecific females. These neurons and those tuned to the major pheromone component, always appearing together, are probably located in the same sensillum. Their large number suggests that (Z)-9-tetradecenal mediates an important message in this species, probably causing interspecific interruption. 3. The third group of neurons (6/63) was tuned to the second principal pheromone component (Z)-11-hexadecenal. These neurons showed similar specificities as the corresponding type of neurons in related species, indicating a conservation of their membrane receptors through evolution. In contrast, the (Z)-9-tetradecenal receptor neurons in H. assulta showed a different specificity than their counterparts in the related species, suggesting that their receptor proteins have evolved differently.

Chemical communication in heliothine moths

1. Projection patterns of olfactory receptor neurons, specifically tuned to the two principal components of the female H. virescens sex pheromone blend, and to a third pheromone-like compound of possible antagonistic significance, were examined using a combined electrophysiological and morphological technique. 2. The macroglomerular complex consists of four major glomerular subdivisions. 3. In the sensillum type containing a receptor neuron detecting the main pheromone component, Z11-16: AL, two cells were present. When the sensillum was stimulated with Z11-16:AL, a single axon, stained by a method that selectively stains active neurons, was seen projecting into the large a glomerulus. The b glomerulus was innervated by a second neuron in a few double stainings. 4. In a second sensillum type, one receptor neuron tuned to the second major pheromone component, Z9-14:AL, was found. In these sensilla, one or two receptor neurons of unknown specificity were also observed. When the sensillum was stimulated with Z9-14: AL, a single neuron projecting into glomerulus a or two neurons projecting into glomerulus a were most often observed. 5. In the third sensillum type, one neuron specifically tuned to Z11-16:AC projected to glomerulus c, and a second cell of unknown specificity projected to the same area. 6. The axonal arborizations of different physiological receptor neuron types involved in the detection of the pheromone blend do not display a clearcut morphological separation into different glomeruli in the MGC. A separation between neurons detecting attracting and repelling odours was, however, present.

Microscopic structure of the olfactory organ of the clearnose skate, Raja eglanteria

The olfactory organ of juvenile clearnose skates (Raja eglanteria) was studied with the light and electron microscopes. The organ is ovoid in shape, and its free surface is complicated by the presence of some 20 lamellae. Each lamella has a folded surface lined by a typical neurosensory olfactory epithelium. Bipolar olfactory receptor neurons, ciliated sustentacular cells, and basal cells are the pre-eminent cellular components of the epithelium. Two types of receptor neurons, both bearing microvilli but not cilia, were identified. The type 1 neuron is similar to that previously described in other fishes. The type 2 neuron has a characteristic morphology justifying a separate description. Its dendritic knob is larger than that of type 1, and its microvilli, which are shorter and thicker, are straight and regularly arranged. Tight bundles of filaments provide a skeleton to each microvillus, and these filament bundles reach more than 5 microns down into the dendrite. Type 2 receptor neurons have a well-developed Golgi complex and sparse rough endoplasmic reticulum (rER), whereas type 1 receptor neurons have a less well-developed Golgi complex and a conspicuous system of rER lamellae. The mucous layer on the epithelial surface is provided by the secretion of goblet cells that are situated mostly in the peripheral regions of each lamella. Secretory granules in the sustentacular cells and glands in the lamina propria were not observed.

Correlation between dendrite diameter and action potential amplitude in sex pheromone specific receptor neurons in male Ostrinia nubilalis (Lepidoptera: Pyralidae)

Outer dendritic segments of olfactory receptor neurons tuned to sex pheromone components were measured morphometrically on the antenna of male European corn borers. Ostrinia nubilalis, to determine if a correlation exists between the diameter of the outer dendritic segment and the spike amplitude. The olfactory sensilla investigated each contained three receptor cells. Two cells were each specific for one of the two pheromone components, (Z)-11-tetradecenyl acetate (Z11-14:OAc) and ( E)-11-tetradecenyl acetate (E11-14:OAc). Two strains of cornborers (Z and E) differ as to which of the two pheromone components is the main one. In both strains a large difference could be observed between the spike amplitudes elicited in the receptor cells by the two pheromone components, the main component always eliciting the large spike. In F1-hybrids (EZ) of these two strains, producing both pheromone components in similar quantities, the spike amplitudes were equal in the two pheromone-specific receptor cells. The third cell responded specifically to a behavioural antagonist. ( Z)-9-tetradecenyl acetate (Z9-14:OAc) in both the parental and hybrid strains, and always showed the smallest spike amplitude. In a morphometric study, the outer dendritic segments were shown to differ more in diameter between the largest and second largest cell in the two parental strains than in the hybrid strain, while the smallest diameter cell did not differ between the different strains. These results imply that receptor cells with larger diameter produce spikes with greater amplitude. The data also show that all three types of receptor neurons display outer dendritic segments with strong variation in the diameter along the length of the segment, and with a pronounced taper towards the tip.

Electrophysiological and field activity of halogenated analogs of (E,E)-8,10-dodecadien-1-ol, the main pheromone component, in codling moth (Cydia pomonella L.)

Pest monitoring and control of the codling moth,Cydia pomonella L., have been developed using the main pheromone component of this species, (E,E)-8,10-dodecadienol (codlemone). However, the activity of codlemone is not satisfactory for pest control by mating disruption. Thus, we have synthesized halogenated analogs of codlemone to see if they could be used as new agents for pest control of the codling moth. Their biological activity was measured by electrophysiological techniques. In EAG screening, codlemone was the most active compound. F(10,11)-codlemone [(E,E)-10,11-difluoro-8,10-dodecadienol] and Cl-codlemone [(E,E)-11-chloro-8,10-undecadienol] elicited significant EAG responses, F(10,11)-codlemone triggering responses not significantly different from responses to codlemone. EAG cross-adaptation experiments and single sensillum recordings revealed that these compounds were detected by the same receptor neuron type as codlemone. No competitive inhibition with codlemone was observed from nonactive compounds. In field trapping, F(10,11)-codlemone and Cl-codlemone were more attractive to male codling moths than codlemone itself. Possible explanations of this activity are discussed.

Sulfhydryl-reagent inhibition of olfaction in a moth and effects of exposure to pheromone compounds or a pheromone analogue.

The effects on olfaction of N-ethylmaleimide (NEM), a specific reagent of free sulfhydryl groups, were studied in the moth Mamestra brassicae. The antennae of male M. brassicae bear two types of specialist receptor neurons involved in pheromone communication. One type is tuned to (Z)-11-hexadecenyl acetate (Z11-16:Ac), the main pheromone component; the second type is tuned to (Z)-9-tetradecenyl acetate (Z9-14:Ac), an interspecific inhibitor not produced by the females of this species. Vapours of NEM irreversibly inhibited the electro-antennographic (EAG) responses to Z11-16:Ac and Z9-14:Ac. When Z11-16:Ac was applied before and during NEM treatment, the responses to Z9-14:Ac were preserved and some protection was observed in the responses to Z11-16:Ac. In return, Z9-14:Ac partially prevented the disappearance of responses to Z11-16:Ac but not to Z9-14:Ac. A third compound, hexadecyl acetate (16:Ac), found in the pheromone gland, but not detected by the antennal receptors, did not prevent the inhibition caused by NEM.

Intermediate stages in the disassembly of synaptic ribbons in cone photoreceptors of the crucian carp, Carassius carassius

Synaptic ribbons are trilaminated plate-shaped presynaptic densities of certain types of receptor cells and neurons. In cone photoreceptors, these structures dissassemble and reassemble in response to light and to a variety of other stimuli. We used the lithium-ionenhanced disassembly and reassembly of synaptic ribbons to characterize structural intermediates in these cyclic changes. A few minutes after exposure of isolated retinas from the crucian carp (Carassius carassius) to lithium, ribbons fragmented into 50-nm-sized dense globular structures. These small spheres were concentrically surrounded by synaptic vesicles attached to them by stalk-like fine bridging filaments. Disassembly always started at the free cytoplasmic edges of the ribbons and proceeded toward the membrane-associated edges. As the disassembly process never started at the membraneanchored site, synaptic ribbons appeared to be polarized structures with functionally different ends. Spheres were subjected to further depolymerization. They disintegrated into clusters of small granular material and disappeared after ca. 45 min of lithium treatment. Spheres were not observed during the reassembly of synaptic ribbons, indicating that the assembly of synaptic ribbons proceeds via smaller subunits.

Functional Specialization of Olfactory Glomeruli in a Moth

The specific function of the glomerular structures present in the antennal lobes or olfactory bulbs of organisms ranging from insects to humans has been obscure because of limitations in neuronal marking methods. By tracing individual neurons in the moth Agrotis segetum, it was determined that physiologically distinct types of pheromone receptor neurons project axons to different regions of the macroglomerular complex (MGC). Each glomerulus making up the MGC has a specific functional identity, initially processing information about one specific pheromone component. This indicates that, at least through the first stage of synapses, olfactory information moves through labeled lines.

Pheromone reception in tobacco budworm moth,heliothis virescens

Eleclrophysiological recordings from single olfactory receptor cells were carried out in the male tobacco budworm moth,Heliothis virescens. Recordings were made primarily from the sensilla trichodea type 1, which are located in the characteristic circumferential rows on the antennae. They possess the longest sensilla hairs as revealed by scanning electron microscopy (SEM). The sensory cells of these sensilla responded specifically to pheromones. Only three types of receptor neurons were found, each tuned to one of the female-produced components. The majority (58%) of the neurons were tuned to the major component (Z)-11-hexadecenal (Z11-16:A1). Another large group (27%) responded specifically to stimulation with (Z)-9-tetradecenal (Z9-14: Al). These two compounds are the most important components of the pheromones as judged by their influence on the behavioral responses of the males. The third type of neurons responded specifically to (Z)-11-hexadecen-1-ol (Z11-16: OH), which may act either as a pheromone component or as an interspecific cue. None of the receptor neurons in the long sensilla trichodea responded specifically to the minor aldehyde components of the pheromone, which have subtle effects on behavior. Mixture experiments provided no evidence that minor components influence the receptor responses to the major components. Olfactory sensilla outside the crosswise rows were also characterized morphologically by SEM. Included in these were sensilla of different lengths, corresponding to a classification as s. basiconica and s. trichodea type 2. Electrophysiological recordings from these sensilla showed that they are involved primarily in host odor reception. However, a few of these neurons responded to pheromones.

The contribution of olfactory receptor neurons to the perception of pheromone component ratios in male redbanded leafroller moths.

(Z)-11-tetradecenyl acetate (Z-11, 14:AC) must be in a 100:9 ratio with (E)-11-tetradecenyl acetate (E-11,14:AC) to produce maximal wing fanning and attraction in male redbanded leafrollers. Earlier electrophysiological studies had indicated that mixtures of these pheromone components elicited responses from olfactory receptor neurons that appeared to differ from those expected on the basis of the responses to the individual components. Here we evaluate whether the behavioral sensitivity to particular ratios of Z- and E-11,14:AC has a correlate in the response properties of olfactory receptor neurons. The stimuli included the ratios of Z- and E-11,14:AC used in earlier behavioral work plus several different mixtures of the seven components found in the pheromone blend, and equivalent amounts of the individual components. These stimuli were presented over a range of intensities to individual trichoid sensilla on the male antenna. In common with earlier results, the receptor neuron with the larger amplitude action potential responded most strongly to Z-11,14:AC, whereas the companion receptor neuron in the sensillum responded most strongly to E-11,14:AC. In contrast with earlier results, each receptor neuron responded exclusively to its own most effective stimulus, without regard to the presence of any other compound. They failed to respond uniquely to any of the other five compounds in the female pheromone blend, or to any of the tested combinations of these compounds. These minor components also failed to modulate the responses elicited in receptor neurons by appropriate ratios of Z- and E-11,14:AC. Thus, the responses of the two types of olfactory receptor neurons found in trichoid sensilla failed to show an optimum at the pheromone ratio known to elicit peak behavioral activity.