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1.
Insects ; 12(5)2021 May 01.
Article in English | MEDLINE | ID: mdl-34062868

ABSTRACT

The volatile plant compounds (VPC) alter pheromone perception by insects but mixture effects inside insect olfactory landscapes are poorly understood. We measured the activity of receptor neurons tuned to Z7-12Ac (Z7-ORN), a pheromone component, in the antenna and central neurons in male Agrotis ipsilon while exposed to simple or composite backgrounds of a panel of VPCs representative of the odorant variety encountered by a moth. Maps of activities were built using calcium imaging to visualize which areas in antennal lobes (AL) were affected by VPCs. We compared the VPC activity and their impact as backgrounds at antenna and AL levels, individually or in blends. At periphery, VPCs showed differences in their capacity to elicit Z7-ORN firing response that cannot be explained by differences in stimulus intensities because we adjusted concentrations according to vapor pressures. The AL neuronal network, which reformats the ORN input, did not improve pheromone salience. We postulate that the AL network evolved to increase sensitivity and to encode for fast changes of pheromone at some cost for signal extraction. Comparing blends to single compounds indicated that a blend shows the activity of its most active component. VPC salience seems to be more important than background complexity.

2.
J Insect Physiol ; 127: 104159, 2020.
Article in English | MEDLINE | ID: mdl-33127358

ABSTRACT

Pheromones are chemical communication signals known to elicit stereotyped behaviours and/or physiological processes in individuals of the same species, generally in relation to a specific function (e.g. mate finding in moths). However, recent research suggests that pheromones can modulate behaviours, which are not directly related to their usual function and thus potentially affect behavioural plasticity. To test this hypothesis, we studied the possible modulatory effects of pheromones on olfactory learning and memory in Agrotis ipsilon moths, which are well-established models to study sex-pheromones. To achieve this, sexually mature male moths were trained to associate an odour with either a reward (appetitive learning) or punishment (aversive learning) and olfactory memory was tested at medium- and long-term (1 h or 1.5 h, and 24 h). Our results show that male moths can learn to associate an odour with a sucrose reward, as well as a mild electric shock, and that olfactory memory persists over medium- and long-term range. Pheromones facilitated both appetitive and aversive olfactory learning: exposure to the conspecific sex-pheromone before conditioning enhanced appetitive but not aversive learning, while exposure to a sex-pheromone component of a heterospecific species (repellent) facilitated aversive but not appetitive learning. However, this effect was short-term, as medium- and long-term memory were not improved. Thus, in moths, pheromones can modulate olfactory learning and memory, indicating that they contribute to behavioural plasticity allowing optimization of the animal's behaviour under natural conditions. This might occur through an alteration of sensitization.


Subject(s)
Appetitive Behavior , Moths/physiology , Punishment , Sex Attractants/metabolism , Smell , Animals , Learning , Male , Memory
3.
Front Physiol ; 10: 1423, 2019.
Article in English | MEDLINE | ID: mdl-31849694

ABSTRACT

Adult moths need energy and nutrients for reproducing and obtain them mainly by consuming flower nectar (a solution of sugars and other compounds). Gustatory perception gives them information on the plants they feed on. Feeding and food perception are integrated in the proboscis extension response, which occurs when their antennae touch a sugar solution. We took advantage of this reflex to explore moth sugar responsiveness depending on different parameters (i.e., sex, age, satiety, site of presentation, and composition of the solution). We observed that starvation but not age induced higher response rates to sucrose. Presentation of sucrose solutions in a randomized order confirmed that repeated sugar stimulations did not affect the response rate; however, animals were sometimes sensitized to water, indicating sucrose presentation might induce non-associative plasticity. Leg stimulation was much less efficient than antennal stimulation to elicit a response. Quinine prevented and terminated sucrose-elicited proboscis extension. Males but not females responded slightly more to sucrose than to fructose. Animals of either sex rarely reacted to glucose, but curiously, mixtures in which half sucrose or fructose were replaced by glucose elicited the same response rate than sucrose or fructose alone. Fructose synergized the response when mixed with sucrose in male but not female moths. This is consistent with the fact that nectars consumed by moths in nature are mixtures of these three sugars, which suggests an adaptation to nectar perception.

4.
Front Physiol ; 10: 1518, 2019.
Article in English | MEDLINE | ID: mdl-31920719

ABSTRACT

In several insects, sex-pheromones are essential for reproduction and reproductive isolation. Pheromones generally elicit stereotyped behaviors. In moths, these are attraction to conspecific sex-pheromone sources and deterrence for heterospecific sex-pheromone. Contrasting with these innate behaviors, some results in social insects point toward effects of non-sex-pheromones on perception and learning. We report the effects of sex-pheromone pre-exposure on gustatory perception and habituation (a non-associative learning) in male Agrotis ipsilon moths, a non-social insect. We also studied the effect of Z5-decenyl acetate (Z5), a compound of the sex-pheromone of the related species Agrotis segetum. We hypothesized that conspecific sex-pheromone and Z5 would have opposite effects. Pre-exposure to either the conspecific sex-pheromone or Z5 lasted 15 min and was done either immediately or 24 h before the experiments, using their solvent alone (hexane) as control. In a sucrose responsiveness assay, pre-exposure to the conspecific sex-pheromone had no effect on the dose-response curve at either delays. By contrast, Z5 slightly improved sucrose responsiveness 15 min but not 24 h after pre-exposure. Interestingly, the conspecific sex-pheromone and Z5 had time-dependent effects on gustatory habituation: pre-exposing the moths with Z5 hindered learning after immediate but not 24-h pre-exposure, whereas pre-exposure to the conspecific sex-pheromone hindered learning at 24-h but not immediate pre-exposure. They did not have opposite effects. This is the first time a sex-pheromone is reported to affect learning in a non-social insect. The difference in modulation between conspecific sex-pheromone and Z5 suggests that con- and hetero-specific sex-pheromones act on plasticity through different cerebral pathways.

5.
Front Physiol ; 10: 1539, 2019.
Article in English | MEDLINE | ID: mdl-31969831

ABSTRACT

Animal personality and individuality are intensively researched in vertebrates and both concepts are increasingly applied to behavioral science in insects. However, only few studies have looked into individuality with respect to performance in learning and memory tasks. In vertebrates, individual learning capabilities vary considerably with respect to learning speed and learning rate. Likewise, honeybees express individual learning abilities in a wide range of classical conditioning protocols. Here, we study individuality in the learning and memory performance of cockroaches, both in classical and operant conditioning tasks. We implemented a novel classical (olfactory) conditioning paradigm where the conditioned response is established in the maxilla-labia response (MLR). Operant spatial learning was investigated in a forced two-choice task using a T-maze. Our results confirm individual learning abilities in classical conditioning of cockroaches that was reported for honeybees and vertebrates but contrast long-standing reports on stochastic learning behavior in fruit flies. In our experiments, most learners expressed a correct behavior after only a single learning trial showing a consistent high performance during training and test. We can further show that individual learning differences in insects are not limited to classical conditioning but equally appear in operant conditioning of the cockroach.

6.
Biol Lett ; 14(8)2018 08.
Article in English | MEDLINE | ID: mdl-30158140

ABSTRACT

Honeybees maintain their colony throughout the cold winters, a strategy that enables them to make the most of early spring flowers. During this period, their activity is mostly limited to thermoregulation, while foraging and brood rearing are stopped. Less is known about seasonal changes to the essential task of defending the colony against intruders, which is regulated by the sting alarm pheromone. We studied the stinging responsiveness of winter bees exposed to this scent or a control (solvent). Surprisingly, winter bees, while maintaining their responsiveness in control conditions, did not increase stinging frequency in response to the alarm pheromone. This was not owing to the bees not perceiving the pheromone, as shown by calcium imaging of the antennal lobes. As the alarm pheromone is thought to act through an increase in brain serotonin levels, ultimately causing heightened defensiveness, we checked if serotonin treatments would affect the stinging behaviour of winter bees. Indeed, treated winter bees became more inclined to sting. Thus, we postulate that loss of responsiveness to the sting alarm pheromone is based on a partial or total disruption of the mechanism converting alarm pheromone perception into high serotonin levels in winter bees.


Subject(s)
Bees/drug effects , Pheromones/metabolism , Seasons , Serotonin/metabolism , Animals , Bees/physiology , Behavior, Animal , Calcium/metabolism , Insect Bites and Stings , Olfactory Bulb/metabolism , Social Behavior
8.
Front Physiol ; 8: 79, 2017.
Article in English | MEDLINE | ID: mdl-28239358

ABSTRACT

Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then transmitted to the pheromone processing macroglomerular complex (MGC) within the primary olfactory center, the antennal lobe, where it is processed by local interneurons and projection neurons. Ultimately a behavioral response, orientation toward the pheromone source, is elicited. Volatile plant compounds (VPCs) are detected by other functional types of olfactory receptor neurons (ORNs) projecting in another area of the antennal lobe. However, Phe-ORNs also respond to some VPCs. Female-produced sex pheromones are emitted within a rich environment of VPCs, some of which have been shown to interfere with the detection and processing of sex pheromone information. As interference between the different odor sources might depend on the spatial and temporal features of the two types of stimuli, we investigated here behavioral and neuronal responses to a brief sex pheromone blend pulse in a VPC background as compared to a control background in the male noctuid moth Agrotis ipsilon. We observed male orientation behavior in a wind tunnel and recorded responses of Phe-ORNs and MGC neurons to a brief sex pheromone pulse within a background of individual VPCs. We also recorded the global input signal to the MGC using in vivo calcium imaging with the same stimulation protocol. We found that VPCs eliciting a response in Phe-ORNs and MGC neurons masked responses to the pheromone and decreased the contrast between background odor and the sex pheromone at both levels, whereas α-pinene did not interfere with first order processing. The calcium signal produced in response to a VPC background was tonic, lasting longer than the VPC stimulus duration, and masked entirely the pheromone response. One percent heptanal and linalool, in addition to the masking effect, caused a clear delay in responses of MGC neurons to the sex pheromone. Upwind flight toward the pheromone in a wind tunnel was also delayed but otherwise not altered by different doses of heptanal.

9.
Proc Biol Sci ; 283(1824)2016 Feb 10.
Article in English | MEDLINE | ID: mdl-26842577

ABSTRACT

Insect pest management relies mainly on neurotoxic insecticides, including neonicotinoids, leaving residues in the environment. There is now evidence that low doses of insecticides can have positive effects on pest insects by enhancing various life traits. Because pest insects often rely on sex pheromones for reproduction, and olfactory synaptic transmission is cholinergic, neonicotinoid residues could modify chemical communication. We recently showed that treatments with different sublethal doses of clothianidin could either enhance or decrease behavioural sex pheromone responses in the male moth, Agrotis ipsilon. We investigated now effects of the behaviourally active clothianidin doses on the sensitivity of the peripheral and central olfactory system. We show with extracellular recordings that both tested clothianidin doses do not influence pheromone responses in olfactory receptor neurons. Similarly, in vivo optical imaging does not reveal any changes in glomerular response intensities to the sex pheromone after clothianidin treatments. The sensitivity of intracellularly recorded antennal lobe output neurons, however, is upregulated by a lethal dose 20 times and downregulated by a dose 10 times lower than the lethal dose 0. This correlates with the changes of behavioural responses after clothianidin treatment and suggests the antennal lobe as neural substrate involved in clothianidin-induced behavioural changes.


Subject(s)
Guanidines/pharmacology , Insecticides/pharmacology , Moths/drug effects , Sex Attractants/metabolism , Thiazoles/pharmacology , Animals , Central Nervous System/drug effects , Central Nervous System/physiology , Dose-Response Relationship, Drug , Male , Moths/physiology , Neonicotinoids , Olfactory Receptor Neurons/drug effects , Olfactory Receptor Neurons/physiology , Sexual Behavior, Animal/drug effects
10.
Front Physiol ; 6: 148, 2015.
Article in English | MEDLINE | ID: mdl-26029117

ABSTRACT

Male moths rely on olfactory cues to find females for reproduction. Males also use volatile plant compounds (VPCs) to find food sources and might use host-plant odor cues to identify the habitat of calling females. Both the sex pheromone released by conspecific females and VPCs trigger well-described oriented flight behavior toward the odor source. Whereas detection and central processing of pheromones and VPCs have been thought for a long time to be highly separated from each other, recent studies have shown that interactions of both types of odors occur already early at the periphery of the olfactory pathway. Here we show that detection and early processing of VPCs and pheromone can overlap between the two sub-systems. Using complementary approaches, i.e., single-sensillum recording of olfactory receptor neurons, in vivo calcium imaging in the antennal lobe, intracellular recordings of neurons in the macroglomerular complex (MGC) and flight tracking in a wind tunnel, we show that some plant odorants alone, such as heptanal, activate the pheromone-specific pathway in male Agrotis ipsilon at peripheral and central levels. To our knowledge, this is the first report of a plant odorant with no chemical similarity to the molecular structure of the pheromone, acting as a partial agonist of a moth sex pheromone.

11.
PLoS Comput Biol ; 10(12): e1003975, 2014 Dec.
Article in English | MEDLINE | ID: mdl-25474026

ABSTRACT

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.


Subject(s)
Models, Neurological , Neurons/physiology , Olfactory Pathways/physiology , Olfactory Receptor Neurons/physiology , Animals , Computational Biology , Male , Moths/physiology , Olfactory Receptor Neurons/metabolism , Pheromones/metabolism
12.
Insects ; 5(2): 399-422, 2014 Jun 17.
Article in English | MEDLINE | ID: mdl-26462691

ABSTRACT

Insects communicating with pheromones, be it sex- or aggregation pheromones, are confronted with an olfactory environment rich in a diversity of volatile organic compounds of which plants are the main releaser. Certain of these volatiles can represent behaviorally relevant information, such as indications about host- or non-host plants; others will provide essentially a rich odor background out of which the behaviorally relevant information needs to be extracted. In an attempt to disentangle mechanisms of pheromone communication in a rich olfactory environment, which might underlie interactions between intraspecific signals and a background, we will summarize recent literature on pheromone/plant volatile interactions. Starting from molecular mechanisms, describing the peripheral detection and central nervous integration of pheromone-plant volatile mixtures, we will end with behavioral output in response to such mixtures and its plasticity.

13.
PLoS One ; 7(3): e33159, 2012.
Article in English | MEDLINE | ID: mdl-22427979

ABSTRACT

Most animals rely on olfaction to find sexual partners, food or a habitat. The olfactory system faces the challenge of extracting meaningful information from a noisy odorous environment. In most moth species, males respond to sex pheromone emitted by females in an environment with abundant plant volatiles. Plant odours could either facilitate the localization of females (females calling on host plants), mask the female pheromone or they could be neutral without any effect on the pheromone. Here we studied how mixtures of a behaviourally-attractive floral odour, heptanal, and the sex pheromone are encoded at different levels of the olfactory pathway in males of the noctuid moth Agrotis ipsilon. In addition, we asked how interactions between the two odorants change as a function of the males' mating status. We investigated mixture detection in both the pheromone-specific and in the general odorant pathway. We used a) recordings from individual sensilla to study responses of olfactory receptor neurons, b) in vivo calcium imaging with a bath-applied dye to characterize the global input response in the primary olfactory centre, the antennal lobe and c) intracellular recordings of antennal lobe output neurons, projection neurons, in virgin and newly-mated males. Our results show that heptanal reduces pheromone sensitivity at the peripheral and central olfactory level independently of the mating status. Contrarily, heptanal-responding olfactory receptor neurons are not influenced by pheromone in a mixture, although some post-mating modulation occurs at the input of the sexually isomorphic ordinary glomeruli, where general odours are processed within the antennal lobe. The results are discussed in the context of mate localization.


Subject(s)
Aldehydes/chemistry , Moths/physiology , Odorants/analysis , Sex Attractants/chemistry , Smell/physiology , Analysis of Variance , Animals , Chemotaxis/physiology , Male , Olfactory Receptor Neurons/metabolism , Sexual Behavior, Animal/physiology
14.
Eur J Neurosci ; 33(10): 1841-50, 2011 May.
Article in English | MEDLINE | ID: mdl-21488987

ABSTRACT

Innate behaviours in animals can be influenced by several factors, such as the environment, experience, or physiological status. This behavioural plasticity originates from changes in the underlying neuronal substrate. A well-described form of plasticity is induced by mating. In both vertebrates and invertebrates, males experience a post-ejaculatory refractory period, during which they avoid new females. In the male moth Agrotis ipsilon, mating induces a transient inhibition of responses to the female-produced sex pheromone. To understand the neural bases of this inhibition and its possible odour specificity, we carried out a detailed analysis of the response characteristics of the different neuron types from the periphery to the central level. We examined the response patterns of pheromone-sensitive and plant volatile-sensitive neurons in virgin and mated male moths. By using intracellular recordings, we showed that mating changes the response characteristics of pheromone-sensitive antennal lobe (AL) neurons, and thus decreases their sensitivity to sex pheromone. Individual olfactory receptor neuron (ORN) recordings and calcium imaging experiments indicated that pheromone sensory input remains constant. On the other hand, calcium responses to non-pheromonal odours (plant volatiles) increased after mating, as reflected by increased firing frequencies of plant-sensitive AL neurons, although ORN responses to heptanal remained unchanged. We suggest that differential processing of pheromone and plant odours allows mated males to transiently block their central pheromone detection system, and increase non-pheromonal odour detection in order to efficiently locate food sources.


Subject(s)
Moths/physiology , Odorants , Plants/chemistry , Sex Attractants/metabolism , Sexual Behavior, Animal/physiology , Aldehydes/chemistry , Animals , Calcium/metabolism , Electrophysiology , Female , Male , Moths/anatomy & histology , Olfactory Receptor Neurons/cytology , Olfactory Receptor Neurons/physiology , Stimulation, Chemical
15.
Annu Rev Entomol ; 56: 423-43, 2011.
Article in English | MEDLINE | ID: mdl-20868283

ABSTRACT

Visual learning admits different levels of complexity, from the formation of a simple associative link between a visual stimulus and its outcome, to more sophisticated performances, such as object categorization or rules learning, that allow flexible responses beyond simple forms of learning. Not surprisingly, higher-order forms of visual learning have been studied primarily in vertebrates with larger brains, while simple visual learning has been the focus in animals with small brains such as insects. This dichotomy has recently changed as studies on visual learning in social insects have shown that these animals can master extremely sophisticated tasks. Here we review a spectrum of visual learning forms in social insects, from color and pattern learning, visual attention, and top-down image recognition, to interindividual recognition, conditional discrimination, category learning, and rule extraction. We analyze the necessity and sufficiency of simple associations to account for complex visual learning in Hymenoptera and discuss possible neural mechanisms underlying these visual performances.


Subject(s)
Insecta/physiology , Learning/physiology , Models, Animal , Animals , Cognition/physiology , Humans , Pattern Recognition, Visual
16.
Int J Dev Biol ; 55(10-12): 923-31, 2011.
Article in English | MEDLINE | ID: mdl-22252489

ABSTRACT

In amphibian embryos, calcium (Ca(2+)) signalling is a necessary and sufficient event to induce neural fate. Transient elevations of [Ca(2+)]i are recorded in neural tissue precursor cells in whole embryos during gastrulation. Using a subtractive cDNA library between control ectoderm (animal caps) and ectoderm induced toward a neural fate by Ca(2+) release, we have isolated several Ca(2+)-induced target genes. Among the isolated genes, Xp54nrb encodes a protein which exhibits the RRM domains characteristic of RNA binding proteins, and is implicated in pre-mRNA splicing steps. Here we show that the Xp54nrb transcripts are expressed throughout early developmental stages, specifically in the neural and sensorial territories and that Xp54nrb could be involved in anterior neural patterning.


Subject(s)
Calcium/chemistry , Calcium/metabolism , DEAD-box RNA Helicases/physiology , Gene Expression Regulation, Developmental , Neurons/metabolism , Xenopus Proteins/physiology , Xenopus laevis/metabolism , Amino Acid Sequence , Animals , Calcium Signaling , Cell Nucleus/metabolism , DEAD-box RNA Helicases/metabolism , Ectoderm/metabolism , Gastrulation , Gene Library , Models, Biological , Molecular Sequence Data , Neurons/pathology , RNA-Binding Proteins/chemistry , Sequence Homology, Amino Acid , Time Factors , Xenopus Proteins/metabolism
17.
J Neurophysiol ; 103(4): 2185-94, 2010 Apr.
Article in English | MEDLINE | ID: mdl-20181736

ABSTRACT

Local networks within the primary olfactory centers reformat odor representations from olfactory receptor neurons to second-order neurons. By studying the rules underlying mixture representation at the input to the antennal lobe (AL), the primary olfactory center of the insect brain, we recently found that mixture representation follows a strict elemental rule in honeybees: the more a component activates the AL when presented alone, the more it is represented in a mixture. We now studied mixture representation at the output of the AL by imaging a population of second-order neurons, which convey AL processed odor information to higher brain centers. We systematically measured odor-evoked activity in 22 identified glomeruli in response to four single odorants and all their possible binary, ternary and quaternary mixtures. By comparing input and output responses, we determined how the AL network reformats mixture representation and what advantage this confers for odor discrimination. We show that increased inhibition within the AL leads to more synthetic, less elemental, mixture representation at the output level than that at the input level. As a result, mixture representations become more separable in the olfactory space, thus allowing better differentiation among floral blends in nature.


Subject(s)
Arthropod Antennae/physiology , Bees/physiology , Calcium Signaling/physiology , Neurons/physiology , Odorants , Olfactory Pathways/physiology , Animals , Arthropod Antennae/anatomy & histology , Bees/anatomy & histology , Discrimination, Psychological/physiology , Models, Animal , Olfactory Pathways/anatomy & histology , Time Factors
19.
Behav Brain Res ; 176(2): 314-22, 2007 Jan 25.
Article in English | MEDLINE | ID: mdl-17113657

ABSTRACT

Harnessed bees conditioned to associate odors and sucrose reward learn to discriminate between olfactory mixtures and their odor components in negative (NP: A+, B+, AB-) and positive (PP: A-, B-, AB+) patterning experiments. They thus extend the proboscis to the reinforced (CS+) but not to the non-reinforced (CS-) stimuli. Using the same protocol, we studied whether or not trials, which are spaced in time, are more effective in supporting patterning discrimination than massed trials which succeed fast to each other ('trial-spacing effect'). Training followed a NP (4 A+, 4 B+, 8 AB-) or a PP (4 A-, 4 B-, 8 AB+) schedule, with a 1:1 ratio between CS+ and CS- trials (8 CS+ and 8 CS- trials). ITIs of 1, 3, 5 and 8min were used in both tasks. Increasing ITI resulted in better differentiation between reinforced and non-reinforced CSs in both NP and PP tasks. However, whereas only the longest ITI of 8min allowed discrimination in NP, PP could already be solved with an ITI of 5min. This difference might be due to the fact that NP, but not PP, would require the formation of a unique cue and thus longer processing times. We thus show that the trial-spacing effect, previously demonstrated for single stimulus conditioning, also determines performance in patterning tasks in which three different stimuli (A, B, AB) alternate so that elements have to be discriminated from their compound.


Subject(s)
Bees/physiology , Discrimination Learning/physiology , Odorants , Olfactory Pathways/physiology , Space Perception/physiology , Analysis of Variance , Animals , Behavior, Animal/physiology , Conditioning, Classical/physiology , Extinction, Psychological/physiology , Time Factors
20.
Article in English | MEDLINE | ID: mdl-18958187

ABSTRACT

Honeybees employ a very rich repertoire of pheromones to ensure intraspecific communication in a wide range of behavioral contexts. This communication can be complex, since the same compounds can have a variety of physiological and behavioral effects depending on the receiver. Honeybees constitute an ideal model to study the neurobiological basis of pheromonal processing, as they are already one of the most influential animal models for the study of general odor processing and learning at behavioral, cellular and molecular levels. Accordingly, the anatomy of the bee brain is well characterized and electro- and opto-physiological recording techniques at different stages of the olfactory circuit are possible in the laboratory. Here we review pheromone communication in honeybees and analyze the different stages of olfactory processing in the honeybee brain, focusing on available data on pheromone detection, processing and representation at these different stages. In particular, we argue that the traditional distinction between labeled-line and across-fiber pattern processing, attributed to pheromone and general odors respectively, may not be so clear in the case of honeybees, especially for social-pheromones. We propose new research avenues for stimulating future work in this area.

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