Parallel Reinforcement Pathways for Conditioned Food Aversions in the Honeybee

Wright, Geraldine A.; Mustard, Julie A.; Simcock, Nicola K.; Ross-Taylor, Alexandra A.R.; McNicholas, Lewis D.; Popescu, Alexandra Luminita; Marion‐Poll, Frédéric

doi:10.1016/j.cub.2010.11.040

Cited by 171 publications

(244 citation statements)

References 41 publications

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“…Areas in the crab brain that are structurally homologous to the mushroom bodies of insects receive dopaminergic innervations and undergo plasticity related with the contextual aversive memory (7). In addition, it was shown that dopaminergic neurotransmission is necessary during aversive training to elicit formation of aversive long-term memory in crabs, as in honey bees and crickets (2,3,7,16). We found that injection of dopamine coincident with appetitive training impairs formation of long-term appetitive memory in crabs and in honey bees (7,9).…”

Section: Mutual Interference Between Appetitive and Aversive Memoriesmentioning

confidence: 71%

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Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Klappenbach

Nally

Locatelli

2017

Proc. Natl. Acad. Sci. U.S.A.

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The neurobiology of learning and memory has been mainly studied by focusing on pure aversive or appetitive experiences. Here, we challenged this approach considering that real-life stimuli come normally associated with competing aversive and appetitive consequences and that interaction between conflicting information must be intrinsic part of the memory processes. We used Neohelice crabs, taking advantage of two well-described appetitive and aversive learning paradigms and combining them in a single training session to evaluate how this affects memory. We found that crabs build separate appetitive and aversive memories that compete during retrieval but not during acquisition. Which memory prevails depends on the balance between the strength of the unconditioned stimuli and on the motivational state of the animals. The results indicate that after a mix experience with appetitive and aversive consequences, parallel memories are established in a way that appetitive and aversive information is stored to be retrieved in an opportunistic manner.long-term memory | consolidation | retrieval | appetitive | aversive I n the wild, it is crucial for animals to learn and remember which places represent a danger and which ones are associated with appetitive rewards such as food, shelter, or mate. Understanding how these associations are acquired, retained, and retrieved are major goals in neurobiology. A successful strategy suited to laboratory conditions has been simplifying learning episodes to appetitive or aversive experiences, because in those ideal cases, learning and memory can be unequivocally measured as attraction or avoidance. The present study is framed on the view that those pure appetitive or aversive experiences do not fully represent real-life situations. In nature, animals are exposed to stimuli that predict positive and negative consequences at the same time, and the conflicting information must be weighed and organized to allow expression of the most beneficial behavior. Invertebrates are convenient models to study the interaction between appetitive and aversive memory processes because neurochemical pathways and circuits involved in both types of memory have begun to be elucidated (1-5). The hypothesis that appetitive and aversive information interact during memory processes gets support from pharmacological studies in crabs (6, 7) and bees (8,9), which show that the neurotransmitter necessary for appetitive memory formation does, in turn, impair aversive memory, whereas the transmitter necessary for aversive memory impairs appetitive memory. In addition, studies in Drosophila, in which memory mechanisms can be dissected at the neuron level, provide evidence that the interaction between appetitive and aversive information occurs from the circuits that encode reward and punishment to circuits that regulate memory expression (10)(11)(12)(13)(14).In contrast to the knowledge about the interaction at the circuit level, the description about the consequence of competing experiences in regards to the content of ...

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Section: Mutual Interference Between Appetitive and Aversive Memoriesmentioning

confidence: 71%

“…Studies in honey bees have addressed memory after training in which the same odor is associated with simultaneous appetitive and aversive consequences (15,16). The result that bees did not evidence appetitive memory toward the learned odor is interpreted as a consequence of an interaction between opposite reinforcements.…”

mentioning

confidence: 99%

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Klappenbach

Nally

Locatelli

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The authors concluded that this was a post-ingestive response, as nicotine failed to stimulate the caterpillars' gustatory receptors, and taste-mediated aversive responses would have been faster in this species (Glendinning, 1996). In honeybees, in addition to gustatory responses to toxins, a post-ingestive mechanism involving serotonin has been identified as playing a role in conditioned food aversions (Wright et al, 2010). It is therefore possible that honeybees may have used post-ingestive mechanisms to detect the nectar nicotine in our study.…”

Section: Feeding Response To Nectar Nicotinementioning

confidence: 77%

“…Accumulating evidence, however, suggests that honeybees are indeed able to detect secondary metabolites Singaravelan et al, 2005;Wright et al, 2010), and their taste perception is likely to be more complex than assumed from the number of gustatory receptors (de Brito Sanchez et al, 2007 Wright et al (2010) have recently shown that gustatory receptors on the proboscis do respond to such substances. Honeybees are less likely to drink sucrose-quinine solutions presented to the proboscis as the toxin concentration increases (Wright et al, 2010).…”

Section: Feeding Response To Nectar Nicotinementioning

confidence: 99%

Honeybees and nectar nicotine: Deterrence and reduced survival versus potential health benefits

Köhler

Pirk

Nicolson

2012

Journal of Insect Physiology

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Secondary metabolites produced by plants for herbivore defence are often found in floral nectar, but their effect on the foraging behaviour and physiological performance of pollinators is largely unknown. Nicotine is highly toxic to most herbivores, and nicotine-based insecticides may contribute to current pollinator declines. We examined the effects of nectar nicotine on honeybee foraging choices and worker longevity. Free-flying honeybee (Apis mellifera scutellata) workers from six colonies were given a choice between multiple nicotine concentrations (0-1000 µM) in artificial nectar (0.15-0.63 M sucrose). The dose-dependent deterrent effect of nicotine was stronger in lower sugar concentrations, but even the highest nicotine concentrations did not completely repel honeybees, i.e. bees did not stop feeding on these diets. Nicotine in nectar acts as a partial repellent, which may keep pollinators moving between plants and enhance crosspollination. In the second part of the study, newly emerged workers from 12 colonies were caged and fed one of four nicotine concentrations (0-300 µM) in 0.63 M sucrose for 21 days. Moderate (≤30 µM) nicotine concentrations had no significant detrimental effect, but high nicotine concentrations reduced the survival of caged workers and their nectar storage in the honey comb.In contrast, worker groups that survived poorly on sugar-only diets demonstrated increased survival on all nicotine diets. In the absence of alternative nectar sources, honeybees tolerate naturally occurring nectar nicotine concentrations; and low concentrations can even be beneficial to honeybees. However, high nicotine concentrations may have a detrimental effect on colony fitness.

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“…This assay of food consumption described by Tiedeken et al 7 revealed that bees can detect bitter compounds in solutions. However, this assay was unable to distinguish taste from post-ingestive processes such as malaise that could also affect feeding behavior over this time interval [8][9][10] .…”

Section: Introductionmentioning

confidence: 99%

A Novel Behavioral Assay to Investigate Gustatory Responses of Individual, Freely-moving Bumble Bees (<em>Bombus terrestris</em>)

Kessler

Simpson

et al. 2016

JoVE

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Generalist pollinators like the buff-tailed bumble bee, Bombus terrestris, encounter both nutrients and toxins in the floral nectar they collect from flowering plants. Only a few studies have described the gustatory responses of bees toward toxins in food, and these experiments have mainly used the proboscis extension response on restrained honey bees. Here, a new behavioral assay is presented for measuring the feeding responses of freely-moving, individual worker bumble bees to nutrients and toxins. This assay measures the amount of solution ingested by each bumble bee and identifies how tastants in food influence the microstructure of the feeding behavior.The solutions are presented in a microcapillary tube to individual bumble bees that have been previously starved for 2-4 hr. The behavior is captured on digital video. The fine structure of the feeding behavior is analyzed by continuously scoring the position of the proboscis (mouthparts) from video recordings using event logging software. The position of the proboscis is defined by three different behavioral categories: (1) proboscis is extended and in contact with the solution, (2) proboscis is extended but not in contact with the solution and (3) proboscis is stowed under the head. Furthermore the speed of the proboscis retracting away from the solution is also estimated.In the present assay the volume of solution consumed, the number of feeding bouts, the duration of the feeding bouts and the speed of the proboscis retraction after the first contact is used to evaluate the phagostimulatory or the deterrent activity of the compounds tested.This new taste assay will allow researchers to measure how compounds found in nectar influence the feeding behavior of bees and will also be useful to pollination biologists, toxicologists and neuroethologists studying the bumble bee's taste system.

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Parallel Reinforcement Pathways for Conditioned Food Aversions in the Honeybee

Cited by 171 publications

References 41 publications

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Honeybees and nectar nicotine: Deterrence and reduced survival versus potential health benefits

A Novel Behavioral Assay to Investigate Gustatory Responses of Individual, Freely-moving Bumble Bees (<em>Bombus terrestris</em>)

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