Behavioral and Neural Analysis of Associative Learning in the Honeybee: a Taste from the Magic Well

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/6199991 Behavioral and neural analysis of associative learning in the honeybee: A taste from the magic well Article in Journal of Comparative Physiology A · September 2007 DOI: 10.1007/s00359-007-0235-9 · Source: PubMed CITATIONS READS 403 1,513 1 author: Martin Giurfa CNRS - Paul Sabatier University - Toulouse III 292 PUBLICATIONS 11,360 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Cognitive abilities in the honey bees. View project Ecos Plus: Pheromonal control of Linepithema humile View project All content following this page was uploaded by Martin Giurfa on 31 March 2014. The user has requested enhancement of the downloaded file. J Comp Physiol A DOI 10.1007/s00359-007-0235-9 REVIEW Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well Martin Giurfa Received: 17 February 2007 / Revised: 21 April 2007 / Accepted: 22 April 2007 © Springer-Verlag 2007 Abstract Equipped with a mini brain smaller than one Abbreviations cubic millimeter and containing only 950,000 neurons, hon- AL Antennal lobe eybees could be indeed considered as having rather limited CS Conditioned stimulus cognitive abilities. However, bees display a rich and inter- DMTS Delayed matching-to-sample esting behavioral repertoire, in which learning and memory DNMTS Delayed non matching-to-sample play a fundamental role in the framework of foraging activi- MB Mushroom body ties. We focus on the question of whether adaptive behavior mRNA Messenger ribonucleic acid in honeybees exceeds simple forms of learning and whether PER Proboscis extension reXex the neural mechanisms of complex learning can be unrav- RNAi Ribonucleic acid interference eled by studying the honeybee brain. Besides elemental SER Sting extension reXex forms of learning, in which bees learn speciWc and univocal US Unconditioned stimulus links between events in their environment, bees also master VUMmx1 Ventral unpaired median neuron of the diVerent forms of non-elemental learning, including catego- maxillary neuromere 1 rization, contextual learning and rule abstraction, both in the visual and in the olfactory domain. DiVerent protocols allow accessing the neural substrates of some of these learning Introduction forms and understanding how complex problem solving can be achieved by a relatively simple neural architecture. These French naturalist BuVon (1707–1788) became famous for the results underline the enormous richness of experience- 36 volumes of his Natural History, an entire life’s work dependent behavior in honeybees, its high Xexibility, and where he covered subjects as diverse as the origin of the solar the fact that it is possible to formalize and characterize in system, the fossilization processes, the classiWcation of Xora controlled laboratory protocols basic and higher-order cog- and fauna and the origin of Mankind. Following a peculiar nitive processing using an insect as a model. vision of animal intelligence, he expressed admiration for some creatures while he fervently rejected others. Among the Keywords Perception · Cognition · Learning · despised animals, an insect gathered his anger and devastating Memory · Honeybee criticisms. It was neither an irritating mosquito nor a creeping cockroach. It was the honeybee. BuVon was impressed by the reproductive capabilities of a honeybee queen which This paper is dedicated to the memory of Guillermo ‘Willy’ Zaccardi X (1972–2007), disciple and friend beyond time and distance, who will “produces thirty or forty thousands ies” (bees were indis- always be remembered with a smile. tinctly called bees and Xies in his works) thus constituting “the largest known multiplication in the animal kingdom”. M. Giurfa (&) This led him to conclude that “the most abject, vilest and Research Centre on Animal Cognition, smallest species are the most abundant ones” (BuVon 1749a, CNRS – University Paul Sabatier, 118 route de Narbonne, 31062 Toulouse cedex 9, France pp. 13–14). He went farther and argued that “it is forceful to e-mail: [email protected] conclude that bees, taken individually, have less genius than 123 J Comp Physiol A a dog, a monkey and the vast majority of living animals; tions that allow discerning the ‘simple’ from the ‘complex’. we shall also agree that they have less docility, less attach- I will focus on associative learning and introduce the dis- ment and less feelings, in a word, less qualities relative to tinction between elemental and non-elemental learning, our own ones” (BuVon 1749b, pp. 93–94). which may be useful as a boundary between simple and This animadversion contrasts with the admiration complex forms of learning. expressed by another famous scientist, who devoted his life Associative learning is a capacity that is widespread to the study of honeybees. Karl von Frisch (1886–1982) among living animals and that allows extracting the logical became famous for the discovery of the honeybee dance, a structure of the world. It consists in establishing predictive ritualized behavior that allows a successful bee forager to relationships between contingent events in the environment inform other bees within the hive about the distance and so that uncertainty is reduced and adaptive behavior results direction of a proWtable food source (Frisch 1967). This was from individual experience with such events. Two major not the only contribution made by von Frisch. He left us an forms of associative learning are usually recognized: in amazingly rich and accurate body of evidence on honeybee classical conditioning (Pavlov 1927), animals learn to asso- behavior that spans studies on honeybee navigation, vision, ciate an originally neutral stimulus (conditioned stimulus, olfaction, taste and magnetic sensing among others (Frisch CS) with a biologically relevant stimulus (unconditioned 1967). Von Frisch liked to describe honeybees as a “magic stimulus, US); in operant conditioning (Skinner 1938), they well” for discoveries in biology because the more is drawn learn to associate their own behavior with a reinforcer. from it, the more is to draw. Surprisingly, this fascination Both forms of learning allow, therefore, predicting reliably ended at a particular point, in which, ironically, von Frisch reinforcement, either appetitive or aversive, and admit could eventually join some of BuVon’s ideas. He expressed diVerent levels of complexity. In their most simple version, his view on the plasticity underlying honeybee behavior in both rely on the establishment of elemental links connect- the following way: “The brain of a bee is the size of a grass ing two speciWc and unambiguous events in the animal’s seed and is not made for thinking. The actions of bees are world. What has been learned for a given tone in terms of mainly governed by instinct” (Frisch 1962, p. 78). Certainly, its outcome is valid for that tone but not necessarily for von Frisch expressed this view in relation to communication another stimulus like a light. The outcome of a given behavior but it is nevertheless striking that a tendency to dis- behavior, like pressing a lever, is valid for that behavior but miss the cognitive capacities of bees—and of insects in gen- not for a diVerent one like pulling a chain. These forms of eral—has been perpetuated throughout diVerent centuries. learning, which have been intensively studied by experi- Despite this prolonged skepticism, in the last three mental psychologists, are also particularly interesting for decades honeybees have become a useful model for the neuroscientists interested in the neural bases of learning study of learning and memory (Menzel and Erber 1978; because they allow tracing to the level of neural circuits and Menzel et al. 1993; Menzel 1985). More recently they have single neurons the basis of associations underlying learn- also acquired a new reputation in the framework of studies ing. Because these forms of learning rely on speciWc stimuli addressing higher-order cognitive capacities that for long (e.g. a given CS and a given US), it is possible to study time seemed to be the exclusive patrimony of some verte- where and how in the central nervous system such stimuli brates such as monkeys, pigeons or dolphins, which are are represented, where and how their neural pathways inter- reputed for their good learning abilities. In this review, I act in order to facilitate association and how experience will analyze the contributions made by research on honey- modiWes their respective neural representations. Both at the bee learning and memory that facilitated such an evolution. behavioral and neural level, these forms of learning have in I will present Wndings and open questions that show the common the univocal and unambiguous relationships extent to which honeybees have increased our current established between events in the world. Due to the fact understanding of cognitive processing both at the behav- that they can be characterized through speciWc links ioral and the cellular level. I hope, in this way, to underline between unique events, simple forms of associative learn- the power and potential of the honeybee in the framework ing are termed ‘elemental learning’ forms. Typical exam- of cognitive neurosciences. ples of elemental learning are absolute conditioning (A+), in which a single stimulus A is reinforced (+), and diVeren- tial conditioning (A+ vs. B¡), in which one stimulus, A, is Elemental and

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