Activity modulation in cockroach sensillum: the role of octopamine

The plasticity of sensory perception is provided partially by modulation of receptor cells. The electrical activity of American cockroach chemoreceptor cells in response to sex pheromone was measured under the influence of octopamine treatment and tracheal anoxia. Both experimental procedures caused decreased electroantennograms but affected spike activity differently: octopamine treatment increased firing rate, whereas anoxia decreased it. Spike frequency under octopamine treatment was elevated in response to pheromone stimulation and at background activity. Experiments with perfusion of isolated antennae showed a direct effect of octopamine on spike activity of pheromone sensilla, and excluded the possibility of indirect effects via octopamine-dependent release of other biologically active substances. The suggested mechanism of octopamine action is receptor cell membrane depolarization.     

Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants

Effects of octopamine on responses of olfactory receptor neurons of Bombyx mori males and females, specialized to the reception of pheromone components and general odorants, respectively, were compared. Injections of octopamine had no effect on the transepithelial potential of antennal sensilla trichodea in both sexes. In males, octopamine increased significantly the amplitude of receptor potentials and nerve impulse responses elicited by the pheromone components bombykol and bombykal. However, the responses of homologous female general odorant-sensitive neurons to linalool and benzoic acid were not affected. In control experiments, injection of physiological saline did not increase the responses in any neuron type.     

Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons

Effects of octopamine and its antagonist epinastine on electrophysiological responses of receptor neurons of Antheraea polyphemus specialised to the pheromone components (E,Z)-6,11-hexadecadienyl acetate and (E,Z)-6,11-hexadecadienal were investigated. Injections of octopamine and epinastine into the moths had no effect on the transepithelial potential of the antennal-branch preparation nor on the spontaneous nerve impulse frequency in either type of receptor neuron. However, in the presence of continuous low-intensity pheromone stimulation, octopamine significantly increased the nerve impulse frequency in the acetate receptor neuron, but not in the aldehyde receptor neuron. Octopamine and epinastine had no significant effect on the receptor potential amplitudes elicited in both receptor neuron types by pheromone stimulation. However, the peak nerve impulse frequency in the response of both receptor neuron types to pheromone was significantly affected: decreased by epinastine and increased by octopamine over a broad range of pheromone concentrations. In control experiments, injection of physiological saline did not significantly alter the peak nerve impulse frequency. The effect of octopamine was established within 1 h after injection and persisted for about 4 h. The possibility of a direct action of octopamine on the nerve impulse generation by the receptor neurons is discussed. Accepted: 8 January 2000     

Cloning and expression pattern of a putative octopamine/tyramine receptor in antennae of the noctuid moth <Emphasis Type="Italic">Mamestra brassicae</Emphasis>

In insects, biogenic amines have been shown to play an important role in olfactory plasticity. In a first attempt to decipher the underlying molecular mechanisms, we report the molecular cloning and precise expression pattern of a newly identified octopamine/tyramine-receptor-encoding gene in the antennae of the noctuid moth Mamestra brassicae (MbraOAR/TAR). A full-length cDNA has been obtained through homology cloning in combination with rapid amplification of cDNA ends/polymerase chain reaction; the deduced protein exhibits high identities with previously identified octopamine/tyramine receptors in other moths. In situ hybridization within the antennae has revealed that MbraOAR/TAR is expressed at the bases of both pheromone-sensitive and non-sensitive olfactory sensilla and in cells with a neurone-like shape. In accordance with previous physiological studies that have revealed a role of biogenic amines in the electrical activity of the receptor neurones, our results suggest that biogenic amines (either octopamine or tyramine) target olfactory receptor neurones to modulate olfactory coding as early as the antennal level.     

Octopamine modulates activity of neural networks in the honey bee antennal lobe

Neuronal plasticity allows an animal to respond to environmental changes by modulating its response to stimuli. In the honey bee (Apis mellifera), the biogenic amine octopamine plays a crucial role in appetitive odor learning, but little is known about how octopamine affects the brain. We investigated its effect in the antennal lobe, the first olfactory center in the brain, using calcium imaging to record background activity and odor responses before and after octopamine application. We show that octopamine increases background activity in olfactory output neurons, while reducing average calcium levels. Odor responses were modulated both upwards and downwards, with more odor response increases in glomeruli with negative or weak odor responses. Importantly, the octopamine effect was variable across glomeruli, odorants, odorant concentrations and animals, suggesting that the octopaminergic network is shaped by plasticity depending on an individual animal’s history and possibly other factors. Using RNA interference, we show that the octopamine receptor AmOA1 (homolog of the Drosophila OAMB receptor) is involved in the octopamine effect. We propose a network model in which octopamine receptors are plastic in their density and located on a subpopulation of inhibitory neurons in a disinhibitory pathway. This would improve odor-coding of behaviorally relevant, previously experienced odors.     

Octopamine and tyramine modulate pheromone-sensitive olfactory sensilla of the hawkmoth <Emphasis Type="Italic">Manduca sexta</Emphasis> in a time-dependent manner

In moths octopamine improved pheromone-dependent mate search time dependently. In the nocturnal hawkmoth Manduca sexta long-term tip recordings of trichoid sensilla were performed to investigate whether biogenic amines modulate pheromone transduction time dependently. At three Zeitgebertimes octopamine, tyramine and the octopamine antagonist epinastine were applied during non-adapting pheromone-stimulation. At ZT 8-11, during the photophase, when sensilla were adapted, octopamine and to a lesser extent tyramine increased the bombykal-dependent sensillar potential amplitude and initial action potential (AP) frequency. In addition, during the photophase, when sensilla are less able to resolve pheromone pulses, octopamine rendered pheromone responses more phasic and sensitive, and raised the spontaneous AP frequency. During the late scotophase, at ZT 22-1, when the antenna appeared maximally sensitized for pheromone pulse detection and endogenous octopamine levels are high, exogenously applied octopamine was ineffective. Epinastine blocked the pheromone-dependent AP response at ZT 8-11 and slightly affected it at ZT 22-1, while it had no effect on the sensillar potential amplitude. Epinastine decreased the spontaneous AP activity during photophase and scotophase and rendered pheromone responses more tonic in the scotophase. We hypothesize that the presence of octopamine in the antenna is obligatory for the detection of intermittent pheromone pulses at all Zeitgebertimes.     

DUM neurons in locust flight: a model system for amine-mediated peripheral adjustments to the requirements of a central motor program

In both vertebrates and invertebrates, multiple effects of biogenic amines on neuromuscular transmission, muscle contraction kinetics and metabolism have been described. Nevertheless, it is not yet known whether and how these different effects work in concert during the performance of a specific behavior. In the locust flight system, the biogenic amine octopamine is released as a neurohormone into the haemolymph, and also delivered directly onto specific target muscles by individually identified dorsal unpaired median neurons. Determining the connectivity of these neurons and their activation during behavior, we show for the first time that different types of dorsal unpaired median neurons are differentially connected to certain components of the flight circuitry. During flight, all types of pterothoracic dorsal unpaired median neurons innervating flight muscles receive inhibitory inputs from tegula proprioceptive afferents and from the central flight circuitry, whereas all other types of dorsal unpaired median neurons are excited by wind-sensitive pathways and by the central pattern generator. Considering the results of other studies which investigated metabolic effects of octopamine, we propose a model in which the differential activation of dorsal unpaired median neurons during flight may lead to an adequately controlled release or removal of octopamine to adjust metabolic processes to the requirements of a specific motor program. Accepted: 24 February 1999     

Flight and fight: a comparative view of the neurophysiology and genetics of honey bee defensive behavior

Honey bee nest defense involves guard bees that specialize in olfaction-based nestmate recognition and alarm-pheromone-mediated recruitment of nestmates to sting. Stinging is influenced by visual, tactile and olfactory stimuli. Both quantitative trait locus (QTL) mapping and behavioral studies point to guarding behavior as a key factor in colony stinging response. Results of reciprocal F1 crosses show that paternally inherited genes have a greater influence on colony stinging response than maternally inherited genes. The most active alarm pheromone component, isoamyl acetate (IAA) causes increased respiration and may induce stress analgesia in bees. IAA primes worker bees for 'fight or flight', possibly through actions of neuropeptides and/or biogenic amines. Studies of aggression in other species lead to an expectation that octopamine or 5-HT might play a role in honey bee defensive response. Genome sequence and QTL mapping identified 128 candidate genes for three regions known to influence defensive behavior. Comparative bioinformatics suggest possible roles of genes involved in neurogenesis and central nervous system (CNS) activity, and genes involved in sensory tuning through G-protein coupled receptors (GPCRs), such as an arrestin (AmArr4) and the metabotropic GABA(B) receptor (GABA-B-R1).     

Effect of tyramine and stress on sex-pheromone production in the pre- and post-mating silkworm moth, Bombyx mori

Tyramine (TA) increased significantly after mating, whereas there were no significant differences in octopamine (OA) and dopamine (DA) levels in the brain-suboesophageal ganglion (SOG) complexes between virgin and mated females. The effects of various biogenic amines were tested on pheromone production of virgin and mated females of the silkworm moth, Bombyx mori. After 8h a significant reduction by TA (46%) was observed. Meanwhile, when OA or DA was injected, a significant increase of pheromone titer was observed in both virgin and mated females. This study also presents evidence for an increase in levels of OA and DA in the brain-SOG complexes in response to mechanical stress in B. mori female. TA suppressed pheromone production in an in vitro pheromone gland (PG) homogenate preparation, thus suggesting that the target of TA is the PG. TA inhibited pheromone production in vitro in a dose-dependent manner and DA had a lower inhibitory activity than TA, whereas OA had no effect, suggesting that TA is a candidate for regulating pheromone production in the PG, although other factors could be responsible for the pheromonostatic function.     

Modulation by octopamine of olfactory responses to nonpheromone odorants in the cockroach, Periplaneta americana L

Olfactory receptor cells in insects are modulated by neurohormones. Recordings from cockroach olfactory sensilla showed that a subset of sensory neurons increase their responses to selected nonpheromone odorants after octopamine application. With octopamine application, recordings demonstrated increased firing rates by the short but not the long alcohol-sensitive sensilla to the nonpheromone volatile, hexan-1-ol. Within the same sensillum, individual receptor cells are shown to be modulated independently from each other, indicating that the octopamine receptors reside in the receptor not in the accessory cells. A uniform decrease in the amplitude of electroantennogram, which is odorant independent, is suggested to reflect the rise in octopamine concentration in the antennal hemolymph. Perception of general odorants measured as behavioral responses changed qualitatively under octopamine treatment: namely, repulsive hexan-1-ol became neutral, whereas neutral eucalyptol became attractive. Octopamine induced a change in male behavioral responses to general odors that were essentially the same as in the state of sexual arousal. Our findings suggest that sensitivity to odors having different biological significances is modulated selectively at the peripheral as well as other levels of olfactory processing.     

Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons

In the olfactory system of male moths, a specialized subset of neurons detects and processes the main component of the sex pheromone emitted by females. It is composed of several thousand first-order olfactory receptor neurons (ORNs), all expressing the same pheromone receptor, that contact synaptically a few tens of second-order projection neurons (PNs) within a single restricted brain area. The functional simplicity of this system makes it a favorable model for studying the factors that contribute to its exquisite sensitivity and speed. Sensory information—primarily the identity and intensity of the stimulus—is encoded as the firing rate of the action potentials, and possibly as the latency of the neuron response. We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs. Modelling showed that the increased sensitivity of PNs can be explained by the ORN-to-PN convergent architecture alone, whereas their faster response also requires cell-to-cell heterogeneity of the ORN population. So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate). Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.     

Glomerular interactions in olfactory processing channels of the antennal lobes

An open question in olfactory coding is the extent of interglomerular connectivity: do olfactory glomeruli and their neurons regulate the odorant responses of neurons innervating other glomeruli? In the olfactory system of the moth Manduca sexta, the response properties of different types of antennal olfactory receptor cells are known. Likewise, a subset of antennal lobe glomeruli has been functionally characterized and the olfactory tuning of their innervating neurons identified. This provides a unique opportunity to determine functional interactions between glomeruli of known input, specifically, (1) glomeruli processing plant odors and (2) glomeruli activated by antennal stimulation with pheromone components of conspecific females. Several studies describe reciprocal inhibitory effects between different types of pheromone-responsive projection neurons suggesting lateral inhibitory interactions between pheromone component-selective glomerular neural circuits. Furthermore, antennal lobe projection neurons that respond to host plant volatiles and innervate single, ordinary glomeruli are inhibited during antennal stimulation with the female’s sex pheromone. The studies demonstrate the existence of lateral inhibitory effects in response to behaviorally significant odorant stimuli and irrespective of glomerular location in the antennal lobe. Inhibitory interactions are present within and between olfactory subsystems (pheromonal and non-pheromonal subsystems), potentially to enhance contrast and strengthen odorant discrimination.     

Cloning, expression and functional analysis of an octopamine receptor from Periplaneta americana

Octopamine regulates multiple physiological functions in invertebrates. The biological effects of octopamine and the pharmacology of octopamine receptors have been extensively studied in the American cockroach, Periplaneta americana. This paper reports the cloning of the first octopamine receptor from Periplaneta americana. A cDNA encoding a putative 7 transmembrane receptor was isolated from the head of Periplaneta americana. The encoded protein contains 628 amino acids and has sequence similarity to other biogenic amine receptors. This protein was expressed in COS-7 cells for radioligand binding studies using the antagonist 3H-yohimbine. Competitive binding comparing biogenic amines that could potentially function as endogenous ligands demonstrated this receptor had the highest affinity for octopamine (Ki = 13.3 microM) followed by tyramine, dopamine, serotonin and histamine. Octopamine increased both cAMP levels (EC50 = 1.62 microM) and intracellular concentrations of calcium through the receptor expressed in HEK-293 cells. Tyramine increased levels of both of these second messengers but only at significantly higher concentrations than octopamine. The cAMP increase by octopamine was independent of the increase in calcium. Competitive binding with antagonists revealed this receptor is similar to Lym oa1 from Lymnaea stagnalis. The data indicate that this cDNA is the first octopamine receptor cloned from Periplaneta americana and therefore has been named Pa oa1.     

Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone response in male gypsy moths,Lymantria dispar

Experiments were conducted to determine whether the biogenic amines octopamine (OA) and 5-hydroxytryptamine (5-HT) exert modulatory effects on pheromone responsiveness and random locomotor activity in male gypsy moths. When injected into males, OA significantly enhanced sensitivity to pheromone, while 5-HT enhanced general locomotor activity, results that were very similar to those previously shown for the cabbage looper. Maximal effect of the amines, however, was observed when injection occurred just prior to the onset of scotophase, rather than photophase, as we had originally hypothesized for this diurnally active insect. Male gypsy moths also displayed a prominent scotophase response, with sensitivity to pheromone greater in the scotphase compared with photophase, but with the level of random locomotor activity lower in scotophase than in photophase. The upwind flight behavior of males to a pheromone source in a wind tunnel, as well as the time spent at the source, were also significantly different in the two light regimes. Furthermore, when exposed to a 1 h scotophase (instead of the normal 8), or to continuous dark conditions, while males exhibited response to pheromone and locomotor activity during the same scotophase and photophase periods as observed in a 16:8 light : dark cycle, the levels of response, as well as qualitative aspects of the upwind flight behaviors in both periods were a function of the light intensity. Our combined results suggest that male gypsy moths display a bimodal rhythm of locomotor and pheromone response over the diel cycle, with light intensity and scotophase onset providing critical cues for the expression of behaviors, as well as the modulatory action of the amines. © 1992 Wiley-Liss, Inc.     

Effects of substituted phenylethylamines on blowfly feeding behavior

The pharmacology of adult Phormia regina (Meigen) feeding behavior was explored by injecting candidate drugs into starved blowflies and then determining their responsiveness to aqueous sucrose, via the proboscis extension reflex. d-Amphetamine caused responsiveness to fall dramatically, while related drugs and biogenic amines had varying effects. When d-amphetamine-treated flies were fed 1 M sucrose, they consumed significantly more than control flies. Electrophysiological studies demonstrated that the responses of tarsal sugar receptor neurons to aqueous sucrose were not significantly altered by d-amphetamine. These observations are compatible with our hypothesis that octopamine positively modulates blowfly feeding behavior and suggest that other aromatic biogenic amines affect feeding behavior in this insect.     

Aminergical regulation of pheromone sensillae in the cockroach Periplaneta americana

Vast adaptability of insects is provided substantially by fast tining of physiological functioning of an organism to conform to the permanently changing environmental conditions. One of the mechanisms of plasticity in insects is modulation of performance of their sense organs by neurohormones. Activity of at least three out of four receptor cells located in cockroach pheromonesensitive sensilla is under influence of octopamine. Increase in firing rate of pheromone receptor cells and decrease in electroantennogram amplitude is accompanied by enhanced behavioural responses of male cockroaches to sex pheromone. The effect of octopamine on reception of a repellent (1,8-cineole) by an insect is reported for the first time. Simultaneous modulation of responses of receptor cells located in sex specific sensilla to semantically different odorants implies their cooperation in formation of insect's behaviour.     

Aminergic regulation of pheromone sensillae in the cockroach <Emphasis Type="Italic">Periplaneta americana</Emphasis>

Tremendous adaptability of insects is predominantly provided by fast tuning of physiological functioning of an organism to the permanently changing environmental conditions. One of the mechanisms of plasticity in insects is modulation of performance of their sense organs by neurohormones. Activity of at least three out of four receptor cells located in cockroach pheromonesensitive sensilla is modulated by octopamine. An increase of firing rate of pheromone receptor cells and a decrease of electroantennogram amplitude is accompanied by enhanced behavioral responses of male cockroaches to sex pheromone. The effect of octopamine on reception of a repellent (1,8-cineole, eucalyptol) by an insect is reported for the first time. Simultaneous modulation of responses of receptor cells located in sex specific sensilla to semantically different odorants indicates their cooperation in formation of insect behavior.     

Olfactory receptor neurons detecting plant odours and male volatiles in Anomala cuprea beetles (Coleoptera: Scarabaeidae)

We have identified several types of olfactory receptor neurons in male and female Anomala cuprea beetles. The receptor neurons were sensitive to female sex pheromone components, flower volatiles, green leaf volatiles and unknown volatiles from males. Olfactory sensilla were located on three lamellae forming the antennal club. There was a clear spatial separation between some types of sensilla on each lamella. Receptor neurons for the two sex pheromone components were situated in sensilla placodea covering a specific area on each lamella in both males and females. All sex pheromone receptor neurons were found in these sensilla. Most other receptor neurons were located in a longitudinal, heterogeneous streak formed by various types of sensilla. Receptor neurons for plant-derived compounds appeared to be specialists with a high sensitivity to their respective key compound. The most remarkable among these are the green leaf volatile-specific receptor neurons, which were both sensitive and selective, with the key compound being at least 1000 times as effective as any other compound. These green leaf volatile detectors are apparently homologous to detectors recently found in the scarab Phyllopertha diversa. Our results emphasize the role of single-sensillum recordings as a tool in the identification of biologically active odours.     

Adaptive value of genes controlling the level of biogenic amines in Drosophila

The effects of mutations that change the level of biogenic amines (octopamine and dopamine) on stress-reactivity and fitness of Drosophila imagoes are considered. It has been shown that (1) the biogenic amines represent an important but not triggering factor of the development of stress reaction; (2) under normal conditions, reproduction is regulated by genes that control dopamine metabolic pathways (indirectly via regulation of the juvenile hormone level). Under unfavorable conditions, reproduction is regulated by genes that control octopamine metabolism; (3) heat-stress adaptation depends on expression of genes controlling the background level of dopamine.     

Structural-functional characteristics of the adenylyl cyclase signaling system regulated by biogenic amines and peptide hormones in muscles of the earthworm Lumbricus terrestris

It has been shown for the first time that biogenic amines (catecholamines and tryptophane derivatives) stimulate dose-dependently activity of adenylyl cyclase (AC) and GTP-binding of G-proteins in muscle of the skin-muscle sac of the earthworm Lumbricus terrestris. By efficiency of their stimulating action on the AC activity, biogenic amines can be arranged in the following sequence: octopamine > tyramine > tryptamine ≈ serotonin > dopamine > isoproterenol ≈ adrenalin. The sequence of efficiency of their action on GTP-binding is somewhat different: serotonin > tryptamine > octopamine > dopamine ≈ tyramine > adrenaline > isoproterenol. Sensitivity of AC and G-proteins in the worm muscle to biogenic amines is similar with that in smooth muscle of the mollusc Anodonta cygnea (invertebrates), but differs markedly by this parameter from the rat myocardium (vertebrates). It has also been revealed that AC in the worm muscle is regulated by peptide hormones, relaxin and somatostatin, whose action is comparable with that in the mollusc muscle, but much weaker that the action of these hormones on the rat myocardium AC activity. Use of Cterminal peptides of α-subunits of G-proteins of the stimulatory (385–394 Gαs) and inhibitory (346–355 Gαi2) types that disrupt selectively the hormonal signal transduction realized via Gsand Giproteins, respectively, allowed establishing that the AC-stimulating effects of relaxin, octopamine, tyramine, and dopamine in the worm muscle are realized via the receptors coupled functionally with Gs-protein; the AC-inhibiting effect of somatostatin is realized via the receptor coupled with Gi-protein, whereas serotonin and tryptamine activate both types of G-proteins.