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Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons

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Abstract

Odors elicit spatio-temporal patterns of activity in the olfactory bulb of vertebrates and the antennal lobe of insects. There have been several reports of changes in these patterns following olfactory learning. These studies pose a conundrum: how can an animal learn to efficiently respond to a particular odor with an adequate response, if its primary representation already changes during this process? In this study, we offer a possible solution for this problem. We measured odor-evoked calcium responses in a subpopulation of uniglomerular AL output neurons in honeybees. We show that their responses to odors are remarkably resistant to plasticity following a variety of appetitive olfactory learning paradigms. There was no significant difference in the changes of odor-evoked activity between single and multiple trial forward or backward conditioning, differential conditioning, or unrewarded successive odor stimulation. In a behavioral learning experiment we show that these neurons are necessary for conditioned odor responses. We conclude that these uniglomerular projection neurons are necessary for reliable odor coding and are not modified by learning in this paradigm. The role that other projection neurons play in olfactory learning remains to be investigated.

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Abbreviations

AL:

Antennal lobe

CR:

Conditioned response

CS−:

Non-rewarded stimulus

CS+:

Rewarded (conditioned) stimulus

ITI:

Inter-trial interval

l-ACT:

Lateral antenno-cerebralis tract

LP:

Lateral protocerebrum

m-ACT:

Medial antenno-cerebralis tract

MB:

Mushroom body

ml-ACT:

Mediolateral antenno-cerebralis tract

OB:

Olfactory bulb

OSN:

Olfactory sensory neuron

PN:

Projection neuron

RM ANOVA:

Repeated measures analysis of variance

SEG:

Subesophageal ganglion

T1–T4:

Tracts 1–4 in the antennal lobe

US:

Unconditioned stimulus

PER:

Proboscis extension reflex

VUMmx1:

Ventral unpaired neuron # 1 of the maxillary neuromere

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Acknowledgments

Support from Volkswagenstiftung, Human Frontier Science Program, Deutscher Akademischer Austauschdienst and Deutsche Forschungsgemeinschaft SFB 515 is acknowledged. Thanks also to Uli Müller for intellectual exchange during the entire project, to Paul Szyszka for valuable discussion and to Silke Sachse, Daniela Pelz and the referees for comments on the manuscript.

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  1. C. G. Galizia

    Present address: Universität Konstanz, 78457, Konstanz, Germany

Authors and Affiliations

  1. Institute of Neurobiology, Freie Universität Berlin, 14195, Berlin, Germany

    P. Peele, M. Ditzen, R. Menzel & C. G. Galizia

  2. Department of Entomology, University of California, Riverside, CA, 92521, USA

    C. G. Galizia

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  1. P. Peele
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  2. M. Ditzen
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Peele, P., Ditzen, M., Menzel, R. et al. Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons. J Comp Physiol A 192, 1083–1103 (2006). https://doi.org/10.1007/s00359-006-0152-3

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