Olfactory conditioning of the proboscis extension in bumble bees

The neuronal basis of complex social behavior is still poorly understood. In honeybees, reproductive investment decisions are made at the colony-level. Queens develop from female-destined larvae that receive alloparental care from nurse bees in the form of ad-libitum royal jelly (RJ) secretions. Typically, the number of raised new queens is limited but genetic breeding of “royal jelly bees” (RJBs) for enhanced RJ production over decades has led to a dramatic increase of reproductive investment in queens. Here, we compare RJBs to unselected Italian bees (ITBs) to investigate how their cognitive processing of larval signals in the mushroom bodies (MBs) and antennal lobes (ALs) may contribute to their behavioral differences. A cross-fostering experiment confirms that the RJB syndrome is mainly due to a shift in nurse bee alloparental care behavior. Using olfactory conditioning of the proboscis extension reflex, we show that the RJB nurses spontaneously respond more often to larval odors compared with ITB nurses but their subsequent learning occurs at similar rates. These phenotypic findings are corroborated by our demonstration that the proteome of the brain, particularly of the ALs differs between RJBs and ITBs. Notably, in the ALs of RJB newly emerged bees and nurses compared with ITBs, processes of energy and nutrient metabolism, signal transduction are up-regulated, priming the ALs for receiving and processing the brood signals from the antennae. Moreover, highly abundant major royal jelly proteins and hexamerins in RJBs compared with ITBs during early life when the nervous system still develops suggest crucial new neurobiological roles for these well-characterized proteins. Altogether, our findings reveal that RJBs have evolved a strong olfactory response to larvae, enabled by numerous neurophysiological adaptations that increase the nurse bees' alloparental care behavior.

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Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Learning & Memory ◽

10.1101/lm.024711.111 ◽

2012 ◽

Vol 19 (2) ◽

pp. 54-66 ◽

Cited By ~ 183

Author(s):

M. Giurfa ◽

J.-C. Sandoz

Keyword(s):

Learning And Memory ◽

Olfactory Conditioning ◽

Proboscis Extension Response ◽

Invertebrate Learning ◽

Proboscis Extension

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Honey bees can store and retrieve independent memory traces after complex experiences that combine appetitive and aversive associations

10.1101/2021.10.12.464105 ◽

2021 ◽

Author(s):

Martin Klappenbach ◽

Agustin E Lara ◽

Fernando F Locatelli

Keyword(s):

Honey Bees ◽

Differential Conditioning ◽

Training Session ◽

Aversive Conditioning ◽

Appetitive Conditioning ◽

Olfactory Conditioning ◽

Proboscis Extension Response ◽

Conditioning Paradigm ◽

Aversive Events ◽

Proboscis Extension

Real-world experiences do often mix appetitive and aversive events. Understanding the ability of animals to extract, store and use this information is an important issue in neurobiology. We used honey bees as model to study learning and memory after a differential conditioning that combines appetitive and aversive training trials. First of all, we describe an aversive conditioning paradigm that constitutes a clear opposite of the well known appetitive olfactory conditioning of the proboscis extension response. A neutral odour is presented paired with the bitter substance quinine. Aversive memory is evidenced later as an odour-specific impairment in appetitive conditioning. Then we tested the effect of mixing appetitive and aversive conditioning trials distributed along the same training session. Differential conditioning protocols like this were used before to study the ability to discriminate odours, however they were not focused on whether appetitive and aversive memories are formed. We found that after a differential conditioning, honey bees establish independent appetitive and aversive memories that do not interfere with each other during acquisition or storage. Finally, we moved the question forward to retrieval and memory expression to evaluate what happens when appetitive and the aversive learned odours are mixed during test. Interestingly, opposite memories compete in a way that they do not cancel each other out. Honey bees showed the ability to switch from expressing appetitive to aversive memory depending on their satiation level.

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Behavioural analysis of olfactory conditioning in the moth spodoptera littoralis (Boisd.) (Lepidoptera: noctuidae)

Journal of Experimental Biology ◽

10.1242/jeb.200.23.2969 ◽

1997 ◽

Vol 200 (23) ◽

pp. 2969-2976 ◽

Cited By ~ 7

Author(s):

RJ Fan ◽

P Anderson ◽

B Hansson

Keyword(s):

Spodoptera Littoralis ◽

Sucrose Solution ◽

Neural Basis ◽

Olfactory Conditioning ◽

Wide Range ◽

The Us ◽

Learning Capabilities ◽

Control Procedures ◽

Proboscis Extension ◽

Lepidoptera Noctuidae

We studied the associative learning capabilities for behaviourally relevant cues in the moth Spodoptera littoralis. The moths were trained to associate a conditioned stimulus (CS), geraniol odour, with an unconditioned stimulus (US), a sucrose solution. The occurrence of a proboscis extension reflex (PER) was tested. The PER performance during acquisition increased steadily with the number of training trials. Non-associative control procedures did not result in learning. PER conditioning was achieved when the CS was presented 1-3 s before the US. A wide range of inter-trial intervals was able to support conditioning. Males and females learned equally well. Moths could to some degree learn the CS-US association after a single trial. These results demonstrate that S. littoralis females and males have a good capability to associate an odour with a reward. The neural basis of olfactory coding in moths has been well studied; thus, the moth provides a powerful system in which to examine the neurobiology of olfactory learning.

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Configural Olfactory Learning in Honeybees: Negative and Positive Patterning Discrimination

Learning & Memory ◽

10.1101/lm.38301 ◽

2001 ◽

Vol 8 (2) ◽

pp. 70-78

Author(s):

Nina Deisig ◽

Harald Lachnit ◽

Martin Giurfa ◽

Frank Hellstern

Keyword(s):

Antennal Lobe ◽

Discrimination Problem ◽

Sucrose Solution ◽

Olfactory Conditioning ◽

Proboscis Extension Response ◽

Activation Patterns ◽

Odor Mixtures ◽

Proboscis Extension ◽

Elemental Associations ◽

Positive Patterning

In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of sucrose solution. If an odor is presented immediately before the sucrose, an elemental association is formed that enables the odor to release the proboscis extension response (PER). Olfactory conditioning of PER was used to study whether, beyond elemental associations, honeybees are able to process configural associations. Bees were trained in a positive and anegative patterning discrimination problem. In the first problem, single odorants were nonreinforced whereas the compound was reinforced. In the second problem, single odorants were reinforced whereas the compound was nonreinforced. We studied whether bees can solve these problems and whether the ratio between the number of presentations of the reinforced stimuli and the number of presentations of the nonreinforced stimuli affects discrimination. Honeybees differentiated reinforced and nonreinforced stimuli in positive and negative patterning discriminations. They thus can process configural associations. The variation of the ratio of reinforced to nonreinforced stimuli modulated the amount of differentiation. The assignment of singular codes to complex odor blends could be implemented at the neural level: When bees are stimulated with odor mixtures, the activation patterns evoked at the primary olfactory neuropile, the antennal lobe, may be combinations of the single odorant responses that are not necessarily fully additive.

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Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation.

Journal of Experimental Biology ◽

10.1242/jeb.200.4.837 ◽

1997 ◽

Vol 200 (4) ◽

pp. 837-847 ◽

Cited By ~ 7

Author(s):

C Pelz ◽

B Gerber ◽

R Menzel

Keyword(s):

Classical Conditioning ◽

Memory Consolidation ◽

Important Determinant ◽

Proboscis Extension Reflex ◽

Olfactory Conditioning ◽

Low Concentrations ◽

Physiological Analysis ◽

Proboscis Extension ◽

High Concentrations ◽

Feature Positive

Stimulus intensity is an important determinant for perception, learning and behaviour. We studied the effects of odorant concentration on classical conditioning involving odorants and odorant-mechanosensory compounds using the proboscis-extension reflex in the honeybee. Our results show that high concentrations of odorant (a) support better discrimination in a feature-positive task using rewarded odorant-mechanosensory compounds versus unrewarded mechanosensory stimuli, (b) have a stronger capacity to overshadow learning of a simultaneously trained mechanosensory stimulus, and (c) induce better memory consolidation. Furthermore, honeybees were trained discriminatively to two different concentrations of one odorant. Honeybees are not able to solve this task when presented with rewarded low versus unrewarded high concentrations. Taken together, our results suggest that high concentrations of odorant support stronger associations (are more 'salient') than low concentrations. Our results, however, do not indicate that honeybees can treat two different concentrations of one odorant as qualitatively different stimuli. These findings fill a gap in what is known about honeybee olfactory learning and are a first step in relating behaviour to recent advances in the physiological analysis of coding for odorant concentration in honeybees.

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