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Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well

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Abstract

Equipped with a mini brain smaller than one cubic millimeter and containing only 950,000 neurons, honeybees could be indeed considered as having rather limited cognitive abilities. However, bees display a rich and interesting behavioral repertoire, in which learning and memory play a fundamental role in the framework of foraging activities. We focus on the question of whether adaptive behavior in honeybees exceeds simple forms of learning and whether the neural mechanisms of complex learning can be unraveled by studying the honeybee brain. Besides elemental forms of learning, in which bees learn specific and univocal links between events in their environment, bees also master different forms of non-elemental learning, including categorization, contextual learning and rule abstraction, both in the visual and in the olfactory domain. Different protocols allow accessing the neural substrates of some of these learning forms and understanding how complex problem solving can be achieved by a relatively simple neural architecture. These results underline the enormous richness of experience-dependent behavior in honeybees, its high flexibility, and the fact that it is possible to formalize and characterize in controlled laboratory protocols basic and higher-order cognitive processing using an insect as a model.

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Abbreviations

AL:

Antennal lobe

CS:

Conditioned stimulus

DMTS:

Delayed matching-to-sample

DNMTS:

Delayed non matching-to-sample

MB:

Mushroom body

mRNA:

Messenger ribonucleic acid

PER:

Proboscis extension reflex

RNAi:

Ribonucleic acid interference

SER:

Sting extension reflex

US:

Unconditioned stimulus

VUMmx1 :

Ventral unpaired median neuron of the maxillary neuromere 1

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Acknowledgments

I thank JM Devaud, JC Sandoz and R Menzel for helpful criticisms on previous versions of this manuscript. I also thank all the members of my research team at the University of Toulouse for providing a stimulating and productive environment. Thanks are also due to the CNRS, the University of Toulouse and the Institut Universitaire de France for much support.

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  1. Research Centre on Animal Cognition, CNRS – University Paul Sabatier, 118 route de Narbonne, 31062, Toulouse cedex 9, France

    Martin Giurfa

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Correspondence to Martin Giurfa.

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This paper is dedicated to the memory of Guillermo ‘Willy’ Zaccardi (1972–2007), disciple and friend beyond time and distance, who will always be remembered with a smile.

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Giurfa, M. Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193, 801–824 (2007). https://doi.org/10.1007/s00359-007-0235-9

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  • DOI: https://doi.org/10.1007/s00359-007-0235-9

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