Prior classical olfactory conditioning improves odour-cued flight orientation of honey bees in a wind tunnel

SUMMARYLocusts can learn associations between olfactory stimuli and food rewards, and use the acquired memories to choose between foods according to their nutrient requirements. They are a model system for both the study of olfactory coding and insect nutritional regulation. Previous studies have used operant paradigms for conditioning freely moving locusts, restricting the study of the neural mechanisms underlying the acquisition of olfactory memories, which requires restrained preparations for electrophysiological recordings. Here we present two complementary paradigms for the classical conditioning of olfactory memories in restrained desert locusts (Schistocerca gregaria). These paradigms allow precise experimental control over the parameters influencing learning. The first paradigm is based on classical (Pavlovian) appetitive conditioning. We show that opening of the maxillary palps can be used as a measure of memory acquisition. Maxillary palp opening in response to odour presentation is significantly higher in locusts trained with paired presentation of an odour and a food reward than in locusts trained either with unpaired presentation of food and odour or the odour alone. The memory formed by this conditioning paradigm lasts for at least 24h. In the second paradigm, we show that classical conditioning of an odour memory in restrained locusts influences their decisions in a subsequent operant task. When locusts that have been trained to associate an odour with a food reward are placed in a Y-maze, they choose the arm containing that odour significantly more often than naïve locusts. A single conditioning trial is sufficient to induce a significant bias for that odour for up to 4h. Multiple-and block-trial training induce a significant bias that lasts at least 24h. Thus, locusts are capable of forming appetitive olfactory memories in classical conditioning paradigms and can use these memories to modify their decisions. Supplementary material available online at

Section: Discussionmentioning

confidence: 99%

Associative olfactory learning in the desert locust, Schistocerca gregaria

Simões

Ott

Niven

2011

“…The use of freely moving animals is therefore necessary to evaluate the associations established during conditioning. In the case of PER conditioning, the positive (attractive) quality acquired by the odour after pairing with sucrose was clearly shown by experiments in which bees previously conditioned in a PER protocol demonstrated an increased orientation towards the odour, either when walking in a four-armed olfactometer (Sandoz et al, 2000) or when flying in a wind tunnel (Chaffiol et al, 2005). These and other experiments in bees (e.g.…”

Section: Introductionmentioning

confidence: 85%

Odour aversion after olfactory conditioning of the sting extension reflex in honeybees

Carcaud

Roussel

Giurfa

et al. 2009

SUMMARYIn Pavlovian conditioning, an originally neutral stimulus (conditioned stimulus or CS) gains control over an animal's reflex after its association with a biologically relevant stimulus (unconditioned stimulus or US). As a consequence, a conditioned response is emitted by the animal upon further CS presentations. In such a situation, the subject exhibits a reflex response, so that whether the CS thereby acquires a positive or a negative value for the animal is difficult to assess. In honeybees, Apis mellifera, an odour (CS) can be associated either with sucrose solution (US) in the appetitive conditioning of the proboscis extension reflex (PER), or with an electric shock (US) in the aversive conditioning of the sting extension reflex (SER). The term 'aversive' may not apply to the latter as bees do not suppress SER as a consequence of learning but, on the contrary, start emitting SER to the CS. To determine whether the CS acquires a positive or a negative value in these conditioning forms, we compared the orientation behaviour of freely walking honeybees in an olfactory-cued Y-maze after training them with an odour-sucrose association (PER conditioning) or an odour-shock association (SER conditioning). We show that the same odours can acquire either a positive value when associated to sucrose, or a negative value when associated to an electric shock, as bees respectively approach or avoid the CS in the Y-maze. Importantly, these results clearly establish the aversive nature of SER conditioning in honeybees.

“…Gerber et al, 1996;Sandoz et al, 2000;Chaffiol et al, 2005;Mc Cabe and Farina, 2009). However, none of these previous studies provided the precise control of experience and/or the bi-directional transfer in both contexts achieved in our work.…”

Section: Information Transfer Between Different Experimental Contextsmentioning

confidence: 99%

Learning context modulates aversive taste strength in honey bees

Sanchez

Serre

Avarguès‐Weber

et al. 2015

The capacity of honey bees (Apis mellifera) to detect bitter substances is controversial because they ingest without reluctance different kinds of bitter solutions in the laboratory, whereas free-flying bees avoid them in visual discrimination tasks. Here, we asked whether the gustatory perception of bees changes with the behavioral context so that tastes that are less effective as negative reinforcements in a given context become more effective in a different context. We trained bees to discriminate an odorant paired with 1 mol l −1 sucrose solution from another odorant paired with either distilled water, 3 mol l −1 NaCl or 60 mmol l −1 quinine. Training was either Pavlovian [olfactory conditioning of the proboscis extension reflex (PER) in harnessed bees], or mainly operant (olfactory conditioning of free-walking bees in a Y-maze). PER-trained and maze-trained bees were subsequently tested both in their original context and in the alternative context. Whereas PER-trained bees transferred their choice to the Y-maze situation, Y-maze-trained bees did not respond with a PER to odors when subsequently harnessed. In both conditioning protocols, NaCl and distilled water were the strongest and the weakest aversive reinforcement, respectively. A significant variation was found for quinine, which had an intermediate aversive effect in PER conditioning but a more powerful effect in the Y-maze, similar to that of NaCl. These results thus show that the aversive strength of quinine varies with the learning context, and reveal the plasticity of the bee's gustatory system. We discuss the experimental constraints of both learning contexts and focus on stress as a key modulator of taste in the honey bee. Further explorations of bee taste are proposed to understand the physiology of taste modulation in bees.