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

2012 ◽  
Vol 19 (2) ◽  
pp. 54-66 ◽  
Author(s):  
M. Giurfa ◽  
J.-C. Sandoz
2021 ◽  
Author(s):  
Martin Klappenbach ◽  
Agustin E Lara ◽  
Fernando F Locatelli

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.


2001 ◽  
Vol 8 (2) ◽  
pp. 70-78
Author(s):  
Nina Deisig ◽  
Harald Lachnit ◽  
Martin Giurfa ◽  
Frank Hellstern

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.


2006 ◽  
Vol 56 (2) ◽  
pp. 259-278 ◽  
Author(s):  
Dorothea Eisenhardt

AbstractThe honeybee (Apis mellifera) is a model organism for the study of learning and memory formation and its underlying mechanisms. Honeybees have a rich behaviour that can be studied in the field as well as in the laboratory. In the latter case, olfactory conditioning of the proboscis extension response (PER) has been intensively studied with respect to the neuronal and molecular mechanisms underlying acquisition and memory formation. Quite a lot is known about the neuronal pathways of both the unconditioned and the conditioned stimulus, and molecular mechanisms that lead to memory formation have been identified. In particular, the role of the cAMP-protein kinase A pathway in memory formation has been analysed. Present knowledge about the molecular basis of memory formation is outlined here. The role of the cAMP-dependent signalling cascade in memory formation is summarised and the activation of this pathway by non-associative and associative learning is discussed.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Daniele Carlesso ◽  
Stefania Smargiassi ◽  
Elisa Pasquini ◽  
Giacomo Bertelli ◽  
David Baracchi

AbstractFloral nectar is a pivotal element of the intimate relationship between plants and pollinators. Nectars are composed of a plethora of nutritionally valuable compounds but also hundreds of secondary metabolites (SMs) whose function remains elusive. Here we performed a set of behavioural experiments to study whether five ubiquitous nectar non-protein amino acids (NPAAs: β-alanine, GABA, citrulline, ornithine and taurine) interact with gustation, feeding preference, and learning and memory in Apis mellifera. We showed that foragers were unable to discriminate NPAAs from water when only accessing antennal chemo-tactile information and that freely moving bees did not exhibit innate feeding preferences for NPAAs. Also, NPAAs did not alter food consumption or longevity in caged bees over 10 days. Taken together our data suggest that natural concentrations of NPAAs did not alter nectar palatability to bees. Olfactory conditioning assays showed that honey bees were more likely to learn a scent when it signalled a sucrose reward containing either β-alanine or GABA, and that GABA enhanced specific memory retention. Conversely, when ingested two hours prior to conditioning, GABA, β-alanine, and taurine weakened bees’ acquisition performances but not specific memory retention, which was enhanced in the case of β-alanine and taurine. Neither citrulline nor ornithine affected learning and memory. NPAAs in nectars may represent a cooperative strategy adopted by plants to attract beneficial pollinators.


2020 ◽  
Vol 20 (6) ◽  
Author(s):  
Heather Christine Bell ◽  
Corina N Montgomery ◽  
Jaime E Benavides ◽  
James C Nieh

Abstract The health of insect pollinators, particularly the honey bee, Apis mellifera (Linnaeus, 1758), is a major concern for agriculture and ecosystem health. In response to mounting evidence supporting the detrimental effects of neonicotinoid pesticides on pollinators, a novel ‘bee safe’ butenolide compound, flupyradifurone (FPF) has been registered for use in agricultural use. Although FPF is not a neonicotinoid, like neonicotinoids, it is an excitotoxic nicotinic acetylcholine receptor agonist. In addition, A. mellifera faces threats from pathogens, such as the microsporidian endoparasite, Nosema ceranae (Fries et al. 1996). We therefore sought 1) to increase our understanding of the potential effects of FPF on honey bees by focusing on a crucial behavior, the ability to learn and remember an odor associated with a food reward, and 2) to test for a potential synergistic effect on such learning by exposure to FPF and infection with N. ceranae. We found little evidence that FPF significantly alters learning and memory at short-term field-realistic doses. However, at high doses and at chronic, field-realistic exposure, FPF did reduce learning and memory in an olfactory conditioning task. Infection with N. ceranae also reduced learning, but there was no synergy (no significant interaction) between N. ceranae and exposure to FPF. These results suggest the importance of continued studies on the chronic effects of FPF.


Honey Bees ◽  
2002 ◽  
pp. 67-84 ◽  
Author(s):  
M Pham-Del√®gue ◽  
A Decourtye

2019 ◽  
Author(s):  
Boaz Yuval ◽  
Paola Lahuatte ◽  
Arul J. Polpass ◽  
Charlotte Causton ◽  
Edouard Jurkevitch ◽  
...  

AbstractPhilornis downsi (Diptera: Muscidae) is a nest parasitic fly that has invaded the Galapagos archipelago and exerts an onerous burden on populations of endemic land birds. As part of an ongoing effort to develop tools for the integrated management of this fly, our objective was to determine its long and short-range responses to bacterial and yeast cues associated with adult P. downsi. We hypothesized that the bacterial and yeast communities will elicit attraction at distance through volatiles, and appetitive responses upon contact. Accordingly, we amplified bacteria from guts of adult field-caught individuals and bird feces, and yeasts from fermenting papaya juice (a known attractant of P. downsi), on selective growth media, and assayed the response of flies to these microbes or their exudates. In the field, we baited traps with bacteria or yeast and monitored adult fly attraction. In the laboratory, we used the Proboscis Extension Response (PER) to determine the sensitivity of males and females to tarsal contact with bacteria or yeast. Long range trapping efforts yielded two female flies over 112 trap nights (one in extracts from bird faeces and one in extracts from gut bacteria from adult flies). In the laboratory, tarsal contact with bacterial stimuli from gut bacteria from adult flies elicited significantly more responses than did yeast stimuli. We discuss the significance of these findings in context with other studies in the field and identify targets for future work.


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