Abstract

The insect mushroom bodies are higher-order brain centers and critical for odor learning. We investigated experience dependent plasticity of their intrinsic neurons, the Kenyon cells (KCs). Using calcium imaging, we recorded KC responses and investigated non-associative plasticity by applying repeated odor stimuli. Associative plasticity was examined by performing appetitive odor learning experiments. Olfactory, gustatory and tactile antennal stimuli evoked phasic calcium transients in sparse ensembles of responding KCs. Repeated stimulation with an odor led to a decrease in KCs' response strength. The pairing of an odor (conditioned stimulus, CS) with a sucrose reward (unconditioned stimulus) induced a prolongation of KC responses. After conditioning, KC responses to a rewarded odor (CS+) recovered from repetition-induced decrease, while the responses to a non-rewarded odor (CS−) decreased further. The spatio-temporal pattern of activated KCs changed for both odors when compared with the response before conditioning but the change was stronger for the CS−. These results demonstrate that KC responses are subject to non-associative plasticity during odor repetition and undergo associative plasticity after appetitive odor learning.

Highlights

  • Learning leads to the modification of neuronal excitability and synaptic strength between neurons

  • Visual inspection of the early and late Kenyon cells (KCs) responses during pretraining and training showed that odor–sucrose pairing evoked activity in some additional KCs, which were not activated by the odor alone, and odor-activated KCs increased their responses upon sucrose stimulation

  • We found that clawed KCs responded to antennal CS-related stimuli and US-related stimuli in a sparse way and with phasic response dynamics

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Summary

INTRODUCTION

Learning leads to the modification of neuronal excitability and synaptic strength between neurons. Learning-related changes have been found in different intrinsic and extrinsic MB neurons (Faber and Menzel, 2001; Grünewald, 1999b; Mauelshagen, 1993; Okada et al, 2007; Riemensperger et al, 2005; Wang et al, 2008; Yu et al, 2006) It is not known, whether KCs at their input site within the MB calyx are subject to learning-dependent plasticity. It induces a robust long-term memory in restrained bees (Bitterman et al, 1983), and during physiological measurements (Mauelshagen, 1993; Okada et al, 2007; Peele et al, 2006) It allows the characterization of excitatory vs inhibitory associative learning effects, as animals learn the forward pairing of the CS–US presentation as an excitatory association for the CS+ and the unrewarded CS presentation as an inhibitory association for the CS− (Hellstern et al, 1998; Rescorla, 1988). The results lead to the conclusion that both associative and non-associative processes underlie neural plasticity in the MB calyx

MATERIALS AND METHODS
A Pretraining odor training
C Correlation between pretraining and posttraining
DISCUSSION
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