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

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.

2020 ◽  
Vol 223 (22) ◽  
pp. jeb230250
Author(s):  
Denise Nery ◽  
Emilia Moreno ◽  
Andrés Arenas

ABSTRACTSearching for reward motivates and drives behaviour. In honey bees Apis mellifera, specialized pollen foragers are attracted to and learn odours with pollen. However, the role of pollen as a reward remains poorly understood. Unlike nectar, pollen is not ingested during collection. We hypothesized that pollen (but not nectar) foragers could learn pollen by sole antennal or tarsal stimulation. Then, we tested how pairing of pollen (either hand- or bee-collected) and a neutral odour during a pre-conditioning affects performance of both pollen and nectar foragers during the classical conditioning of the proboscis extension response. Secondly, we tested whether nectar and pollen foragers perceive the simultaneous presentation of pollen (on the tarsi) and sugar (on the antennae) as a better reinforcement than sucrose alone. Finally, we searched for differences in learning of the pollen and nectar foragers when they were prevented from ingesting the reward during the conditioning. Differences in pollen-reinforced learning correlate with division of labour between pollen and nectar foragers. Results show that pollen foragers performed better than nectar foragers during the conditioning phase after being pre-conditioned with pollen. Pollen foragers also performed better than nectar foragers in both the acquisition and extinction phases of the conditioning, when reinforced with the dual reward. Consistently, pollen foragers showed improved abilities to learn cues reinforced without sugar ingestion. We discussed that differences in how pollen and nectar foragers respond to a cue associated with pollen greatly contribute to the physiological mechanism that underlies foraging specialization in the honeybee.


Author(s):  
Kiri Li N. Stauch ◽  
Harrington Wells ◽  
Charles I. Abramson

Previous research looking at expectancy in animals has used various experimental designs focusing on appetitive and avoidance behaviors. In this study, honey bees (Apis mellifera) were tested ina series of three proboscis extension response (PER) experiments to determine to what degree honey bees’ form a cognitive-representation of an unconditioned stimulus (US). Tthe first experiment, bees were presented with either a 2 sec. sucrose US or 2 sec. honey US appetitive reward and the proboscis-extension duration was measured under each scenario. The PER duration was longer for the honey US even though each US was presented for just 2 sec. Honey bees in the second experiment were tested during extinction trials on a conditioned stimulus (CS) of cinnamon or lavender that was paired with either the sucrose US or honey US in the acquisition trials. The proportion of bees showing the PER response to the CS was recorded for each extinction trial for each US scenario, as was the duration of the proboscis extension for each bee. Neither measure differed between the honey US and sucrose US scenarios, In experiment three, bees were presented with a cinnamon or lavender CS paired with either honey US or sucrose US in a set of acquisition trials, but here the US was not given until after the proboscis was retracted. The PER duration after the CS, and again subsequent after the US, were recorded. While the PER duration after the US was longer for honey, the PER duration after the CS did not differ between honey US and sucrose US.


2002 ◽  
Vol 205 (10) ◽  
pp. 1429-1437 ◽  
Author(s):  
Yukihisa Matsumoto ◽  
Makoto Mizunami

SUMMARY Temporal determinants of olfactory long-term memory retention in the cricket Gryllus bimaculatus were studied. Elementary appetitive and aversive conditioning procedures, as well as a differential conditioning procedure, were applied. In appetitive conditioning, peppermint odour was paired with a water reward. In aversive conditioning, vanilla odour was paired with saline solution. In differential conditioning, an appetitive conditioning trial was followed by an aversive conditioning trial. The odour preference of crickets was tested before and 2 h, 1 day and 4 days after training by allowing the crickets to choose between peppermint or vanilla sources. Differential conditioning or appetitive conditioning alone led to long-lasting memory retention with no significant decay from 2 h to 4 days after training,but retention after aversive conditioning was absent 1 day after training. Studies using differential conditioning have shown (i) that four trials are sufficient to cause a saturated level of acquisition, (ii) that conditioning is successful when the conditioned stimulus is presented immediately or 5 s before the onset of presentation of the unconditioned stimulus, (iii) that the optimal interval between trials is 2-5 min, and (iv) that anaesthetic treatment with CO2 given immediately after training results in memory disruption but that anaesthetic-resistant memory develops fully 20 min after training. This study demonstrates that a differential conditioning procedure is particularly effective for the formation of long-term memory.


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.


1993 ◽  
Vol 69 (2) ◽  
pp. 609-625 ◽  
Author(s):  
J. Mauelshagen

1. Sensitization and classical odor conditioning of the proboscis extension reflex were functionally analyzed by repeated intracellular recordings from a single identified neuron (PE1-neuron) in the central bee brain. This neuron belongs to the class of "extrinsic cells" arising from the pedunculus of the mushroom bodies and has extensive arborizations in the median and lateral protocerebrum. The recordings were performed on isolated bee heads. 2. Two different series of physiological experiments were carried out with the use of a similar temporal succession of stimuli as in previous behavioral experiments. In the first series, one group of animals was used for a single conditioning trial [conditioned stimulus (CS), carnation; unconditioned stimulus (US), sucrose solution to the antennae and proboscis), a second group was used for sensitization (sensitizing stimulus, sucrose solution to the antennae and/or proboscis), and the third group served as control (no sucrose stimulation). In the second series, a differential conditioning paradigm (paired odor CS+, carnation; unpaired odor CS-, orange blossom) was applied to test the associative nature of the conditioning effect. 3. The PE1-neuron showed a characteristic burstlike odor response before the training procedures. The treatments resulted in different spike-frequency modulations of this response, which were specific for the nonassociative and associative stimulus paradigms applied. During differential conditioning, there are dynamic up and down modulations of spike frequencies and of the DC potentials underlying the responses to the CS+. Overall, only transient changes in the minute range were observed. 4. The results of the sensitization procedures suggest two qualitatively different US pathways. The comparison between sensitization and one-trial conditioning shows differential effects of nonassociative and associative stimulus paradigms on the response behavior of the PE1-neuron. The results of the differential conditioning procedure reveal that the effect observed for the one-trial conditioning paradigm is of an associative nature and that there might be modulations, which are specific for single and multiple trial conditioning procedures. It is hypothesized that the PE1-neuron is a possible element involved in the short-term acquisition, rather than in the long-term storage, of an associative olfactory memory in the honeybee.


2021 ◽  
Vol 9 ◽  
Author(s):  
Fabian A. Ruedenauer ◽  
Niklas W. Biewer ◽  
Carmen A. Nebauer ◽  
Maximilian Scheiner ◽  
Johannes Spaethe ◽  
...  

The nutritional composition of food is often complex as resources contain a plethora of different chemical compounds, some of them more, some less meaningful to consumers. Plant pollen, a major food source for bees, is of particular importance as it comprises nearly all macro- and micronutrients required by bees for successful development and reproduction. However, perceiving and evaluating all nutrients may be tedious and impair quick foraging decisions. It is therefore likely that nutrient perception is restricted to specific nutrients or nutrient groups. To better understand the role of taste in pollen quality assessment by bees we investigated nutrient perception in the Western honey bee, Apis mellifera. We tested if the bees were able to perceive concentration differences in amino acids, fatty acids, and sterols, three highly important nutrient groups in pollen, via antennal reception. By means of proboscis extension response (PER) experiments with chemotactile stimulation, we could show that honey bees can distinguish between pollen differing in amino and fatty acid concentration, but not in sterol concentration. Bees were also not able to perceive sterols when presented alone. Our finding suggests that assessment of pollen protein and lipid content is prioritized over sterol content.


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