Redefining Single-Trial Memories in the Honeybee

Villar, María Eugenia; Marchal, Paul Alfred; Viola, Haydeé; Giurfa, Martín

doi:10.1016/j.celrep.2020.01.086

Cited by 44 publications

(57 citation statements)

References 60 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In this way, besides evaluating how preexosure to pheromonal components affected their learning, we evaluated how it affected memory retention after conditioning. As a robust proxy of memory retention, we quantified the percentage of bees exhibiting specific memory, i.e., responding only to the CS+ and not to the CS− 22 , 23 . Preexposure to pheromone components of different valence induced opposite modulation of specific memory (Fig.…”

Section: Resultsmentioning

confidence: 99%

Pheromone components affect motivation and induce persistent modulation of associative learning and memory in honey bees

et al. 2020

Self Cite

View full text Add to dashboard Cite

Since their discovery in insects, pheromones are considered as ubiquitous and stereotyped chemical messengers acting in intraspecific animal communication. Here we studied the effect of pheromones in a different context as we investigated their capacity to induce persistent modulations of associative learning and memory. We used honey bees, Apis mellifera , and combined olfactory conditioning and pheromone preexposure with disruption of neural activity and two-photon imaging of olfactory brain circuits, to characterize the effect of pheromones on olfactory learning and memory. Geraniol, an attractive pheromone component, and 2-heptanone, an aversive pheromone, improved and impaired, respectively, olfactory learning and memory via a durable modulation of appetitive motivation, which left odor processing unaffected. Consistently, interfering with aminergic circuits mediating appetitive motivation rescued or diminished the cognitive effects induced by pheromone components. We thus show that these chemical messengers act as important modulators of motivational processes and influence thereby animal cognition.

show abstract

Section: Resultsmentioning

confidence: 99%

Pheromone components affect motivation and induce persistent modulation of associative learning and memory in honey bees

et al. 2020

Self Cite

View full text Add to dashboard Cite

show abstract

“…Fruitflies (Drosophila melanogaster) can form an association between an odour and a reward in one exposure, which may last up to 24 h (Krashes and Waddell 2008). Honeybees and ants can learn to associate a sucrose reward with a colour, odour, or direction after only one exposure, and retrieve this memory several days later (Menzel 1968;Grüter et al 2011;Piqueret et al 2019;Oberhauser et al 2019;Villar et al 2020). Ants have even been reported to return to memorised locations after multiple months in winter diapause (Salo and Rosengren 2001).…”

Section: Introductionmentioning

confidence: 99%

“…However, not all social insects perform equally well in odour-association tasks. While Apis mellifera honeybees can learn an odour-reward association in a single proboscis extension response trial (Menzel 1993;Henske et al 2015;Villar et al 2020), some stingless bee species, such as Meliponula bocandei, seem to form only weak associations under identical circumstances (Henske et al 2015). While L. niger ants reach a choice accuracy of 71% after one round of differential exposure to two odours associated with a reward and a punishment (Oberhauser et al 2019), Camponotus mus seem to require up to eight such visits to reach comparable accuracy (Dupuy et al 2006).…”

Section: Introductionmentioning

confidence: 99%

Very rapid multi-odour discrimination learning in the ant Lasius niger

Czaczkes

Kumar

2020

Insect. Soc.

View full text Add to dashboard Cite

Insects can be very good learners. For example, they can form associations between a cue and a reward after only one exposure. Discrimination learning, in which multiple cues are associated with different outcomes, is critical for responding correctly complex environments. However, the extent of such discrimination learning is not well explored. Studies concerning discrimination learning within one valence are also rare. Here we ask whether Lasius niger ants can form multiple concurrent associations to different reward levels, and how rapidly such associations can be learned. We allowed individual workers to sequentially feed on up to four different food qualities, each associated with a different odour cue. Using pairwise preference tests, we found that ants can successfully learn at least two, and likely three, odour/quality associations, requiring as little as one exposure to each combination in order for learning to take place. By testing preference between two non-extreme values (i.e. between 0.4 M and 0.8 M having been trained to the qualities 0.2, 0.4, 0.8 and 1.6) we exclude the possibility that ants are only memorising the best and worst values in a set. Such rapid learning of multiple associations, within one valence and one modality, is impressive, and makes Lasius niger a very tractable model for complex training paradigms.

show abstract

“…ANOVA procedures are applicable in the case of binary response variables despite their lack of normality if comparisons imply equal cell frequencies and at least 40 degrees of freedom of the error term (d 'Agostino, 1971;Lunney, 1970;Matsumoto, Menzel, Sandoz, and Giurfa, 2012), conditions that were met by our experiments. As this analysis confounds different bee categories (bees responding to the CS and not to the Nod, bees responding to both odorants, bees responding to none, and bees responding only to the Nod) and may hide important features of memory retention (Pamir, Chakroborty, Stollhoff, Gehring, Antemann, Morgenstern, Felsenberg, Eisenhardt, Menzel, and Nawrot, 2011;Pamir, Szyszka, Scheiner, and Nawrot, 2014;Villar et al, 2020), we focused on a more robust proxy of memory retention, which is the bees that showed CS-specific memory (i.e. that responded to the CS and not to the Nod) (Matsumoto et al, 2012;Villar et al, 2020).…”

Section: Statisticsmentioning

confidence: 99%

“…After successful learning, the odorant acquires the capacity to elicit PER per se. Olfactory PER conditioning leads to robust long-term memories that are stabilized in time (Menzel, 1999;2001;Muller, 2012), even after a single trial conditioning (Villar, Marchal, Viola, and Giurfa, 2020), thanks to the process of protein synthesis.…”

Section: Introductionmentioning

confidence: 99%

Degradation of an appetitive olfactory memory via devaluation of sugar reward is mediated by 5-HT signaling in the honey bee

Lai

Despouy

Sandoz

et al. 2020

Neurobiology of Learning and Memory

Self Cite

View full text Add to dashboard Cite

Conditioned taste aversion (CTA) learning induces the devaluation of a preferred food through its pairing with a stimulus inducing internal illness. In invertebrates, it is still unclear how this aversive learning impairs the memories of stimuli that had been associated with the appetitive food prior to its devaluation. Here we studied this phenomenon in the honey bee and characterized its neural underpinnings. We first trained bees to associate an odorant (conditioned stimulus, CS) with appetitive fructose solution (unconditioned stimulus, US) using a Pavlovian olfactory conditioning. We then subjected the bees that learned the association to a CTA training during which the antennal taste of fructose solution was contingent or not to the ingestion of quinine solution, which induces malaise a few hours after ingestion. Only the group experiencing contingent fructose stimulation and quinine-based malaise exhibited a decrease in responses to the fructose and a concomitant decrease in odor-specific retention in tests performed 23 h after the original odor conditioning. Furthermore, injection of dopamine-and serotonin-receptor antagonists after CTA learning revealed that this longterm decrease was mediated by serotonergic signaling as its blockade rescued both the responses to fructose and the odor-specific memory 23 h after conditioning. The impairment of a prior CS memory by subsequent CTA conditioning confirms that bees retrieve a devaluated US representation when presented with the CS. Our findings further highlight the importance of serotonergic signaling in aversive learning in the bee and uncover mechanisms underlying aversive memories induced by internal illness in invertebrates.

show abstract

Redefining Single-Trial Memories in the Honeybee

Cited by 44 publications

References 60 publications

Pheromone components affect motivation and induce persistent modulation of associative learning and memory in honey bees

Pheromone components affect motivation and induce persistent modulation of associative learning and memory in honey bees

Very rapid multi-odour discrimination learning in the ant Lasius niger

Degradation of an appetitive olfactory memory via devaluation of sugar reward is mediated by 5-HT signaling in the honey bee

Contact Info

Product

Resources

About