Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to Africanized honeybees

Cabe, Sofía I. Mc; Hartfelder, Klaus; Santana, Weyder Cristiano; Farina, Walter M.

doi:10.1007/s00359-007-0260-8

Cited by 52 publications

(51 citation statements)

References 46 publications

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“…Olfactory PER conditioning has become a versatile tool for the study of questions, not only in the field of comparative experimental psychology (e.g., Chandra and Smith 1998;Hellstern et al 1998;Deisig et al 2001Deisig et al , 2002Deisig et al , 2003, as originally planned by Takeda, but also in diversified fields such as olfactory perception (e.g., Vareschi 1971;Guerrieri et al 2005b;Reinhard et al 2010), neurobiology of olfaction and olfactory learning (e.g., Hammer 1993;Stopfer et al 1997;Faber et al 1999;Sandoz et al 2003;Rath et al 2011), molecular bases of memory (for review, see Menzel 1999;Schwärzel and Müller 2006), social bases of behavior in bees (e.g., Chaline et al 2005;Arenas and Farina 2008), and floral ecology (Wright et al 2002(Wright et al , 2005, to cite only a few examples. The basic premises of olfactory PER conditioning have also been adapted in other species, such as bumblebees (Laloi et al 1999;Riveros and Gronenberg 2009), stingless bees (McCabe et al 2007;Farina 2009, 2010), moths (Fan et al 1997;Fan and Hansson 2001;Daly et al 2004), and even ants, which do not have a proboscis but whose mouthpart movements can also be conditioned (Guerrieri and d'Ettorre 2010;Guerrieri et al 2011).…”

Section: Resultsmentioning

confidence: 99%

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

Giurfa

Sandoz²

2012

Learn. Mem.

346

334

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The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.Classical conditioning (Pavlov 1927) is a form of conditioning in which a subject learns to associate a neutral stimulus (the "conditioned stimulus," or CS), which does not originally elicit a behavioral response, with a stimulus of biological significance (the "unconditioned stimulus," or US), which elicits an innate, often reflexive, response. Through this association, the originally neutral stimulus acquires the capacity to elicit a conditioned response.Decades of research on animal learning and memory have established some invertebrates (e.g., the sea hare, Aplysia californica, the fruit fly, Drosophila melanogaster, the honeybee, Apis mellifera) as standard models for the study of classical conditioning (Giurfa 2007b;Menzel et al. 2007). This success can be attributed to the fact that these animals can learn nonassociative as well as Pavlovian and operant associations and possess relatively simple nervous systems that allow retracing of these phenomena to the cellular and molecular levels in different kinds of laboratory preparations. Among these invertebrates, the honeybee, Apis mellifera, has emerged as a robust and influential model for the study of

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Section: Resultsmentioning

confidence: 99%

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

Giurfa

Sandoz²

2012

Learn. Mem.

346

334

View full text Add to dashboard Cite

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“…The bees have to respond to one rewarded odor and discriminate it from another unrewarded odor. Melipona quadrifasciata is able to solve this differential task and is so far the only stingless bee for which olfactory proboscis extension reflex conditioning has been successful (McCabe et al 2007). Further studies in M. quadrifasciata show that food-odor information acquired in the nest influence performance in differential conditioning experiments.…”

Section: Introductionmentioning

confidence: 99%

Olfactory associative learning in two African stingless bee species (Meliponula ferruginea and M. bocandei, Meliponini)

et al. 2015

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Worldwide only a few of the more than 500 stingless bee species has been studied in any detail. Most studies on stingless bees have been conducted in the Neotropics, whereas a very few have been undertaken in Africa. Foraging success is dependent to a greater or lesser extent on olfactory cues or signals. A prerequisite to effective foraging via odors is that the bees are able to associate odors with a nectar reward and memorize this information. In the context of olfactory learning, only five species of stingless bees have been studied using classical conditioning of the proboscis extension reflex (PER). Foragers are capable of using previously experienced olfactory information when choosing food sources, but they rarely respond in differential PER assays. This study examines for the first time the olfactory learning abilities of African stingless bees. A differential conditioning assay was used to study learning and memory of Meliponula ferruginea and Meliponula bocandei. Our results clearly show that both stingless bee species associate odors with a reward. Learning performance of both stingless bee species was poor compared to Apis m. scutellata. This might reflect that the experimental procedure has been optimized for Apis mellifera. However, the PER paradigm seems to be suitable to study learning, memory, and olfactory perception in Meliponula. As in honeybees, this paradigm will open the way to answer ecological, psychological, and neurobiological questions in these species.

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“…Here, we evaluate the potential of the PER protocol to study visual learning in Africanized honey bees (AHB; feral bees near Apis mellifera scutellata) (Francoy et al, 2008), which were introduced to the Neotropics over 50 years ago (Smith et al, 1989;Spivak et al, 1991;Schneider et al, 2004;Roubik, 2009). They readily learn olfactory cues following the PER protocol (Abramson et al, 1997;McCabe et al, 2007;Couvillon et al, 2010), yet their performance appears to be poorer (Couvillon et al, 2010) and a previous attempt to condition AHBs to light was unsuccessful (Abramson et al, 1997). We relied on absolute and discriminant learning tasks that were evaluated using colored lights of three different wavelengths.…”

Section: Introductionmentioning

confidence: 99%

Color dependent learning in restrained Africanized honey bees

Jernigan

Roubik

Wcislo

et al. 2013

Journal of Experimental Biology

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Associative color learning has been demonstrated to be very poor using restrained European honey bees unless the antennae are amputated. Consequently, our understanding of proximate mechanisms in visual information processing is handicapped. Here we test learning performance of Africanized honey bees under restrained conditions with visual and olfactory stimulation using the proboscis extension response (PER) protocol. Restrained individuals were trained to learn an association between a color stimulus and a sugar-water reward. We evaluated performance for 'absolute' learning (learned association between a stimulus and a reward) and 'discriminant' learning (discrimination between two stimuli). Restrained Africanized honey bees (AHBs) readily learned the association of color stimulus for both blue and green LED stimuli in absolute and discriminatory learning tasks within seven presentations, but not with violet as the rewarded color. Additionally, 24-h memory improved considerably during the discrimination task, compared with absolute association (15-55%). We found that antennal amputation was unnecessary and reduced performance in AHBs. Thus color learning can now be studied using the PER protocol with intact AHBs. This finding opens the way towards investigating visual and multimodal learning with application of neural techniques commonly used in restrained honey bees.

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Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to Africanized honeybees

Cited by 52 publications

References 46 publications

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

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

Olfactory associative learning in two African stingless bee species (Meliponula ferruginea and M. bocandei, Meliponini)

Color dependent learning in restrained Africanized honey bees

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