Visual Associative Learning in Restrained Honey Bees with Intact Antennae

Susan E Fahrbach,Scott E Dobrin,Adrian G Dyer

doi:10.1371/journal.pone.0037666

Abstract

A restrained honey bee can be trained to extend its proboscis in response to the pairing of an odor with a sucrose reward, a form of olfactory associative learning referred to as the proboscis extension response (PER). Although the ability of flying honey bees to respond to visual cues is well-established, associative visual learning in restrained honey bees has been challenging to demonstrate. Those few groups that have documented vision-based PER have reported that removing the antennae prior to training is a prerequisite for learning. Here we report, for a simple visual learning task, the first successful performance by restrained honey bees with intact antennae. Honey bee foragers were trained on a differential visual association task by pairing the presentation of a blue light with a sucrose reward and leaving the presentation of a green light unrewarded. A negative correlation was found between age of foragers and their performance in the visual PER task. Using the adaptations to the traditional PER task outlined here, future studies can exploit pharmacological and physiological techniques to explore the neural circuit basis of visual learning in the honey bee.

Highlights

The proboscis extension response (PER) is an appetitive associative learning task commonly used to study olfactory learning and memory in harnessed insects
No difference was found between the groups of non-learners in their responses to the sucrose presentation on the rewarded trials, suggesting they all found the sucrose rewarding and remained capable of extending their proboscis throughout the training period
We report here the first example of successful visual PER conditioning in antennae-intact foragers on a differential learning paradigm

Summary

Introduction

The proboscis extension response (PER) is an appetitive associative learning (classical conditioning) task commonly used to study olfactory learning and memory in harnessed insects. Honey bees (and other insects, including fruit flies) reflexively extend their proboscis when a sweet solution (the unconditioned stimulus – US) is touched to an antenna. If this touch is paired with an odor (the conditioned stimulus – CS), a honey bee quickly learns the association and subsequently extends its proboscis to the odor alone [1,2]. The antennal lobes (ALs) and the mushroom bodies (MBs) have been identified as sites of convergence of the CS-US signals relevant for olfactory association learning in the insect brain [4]

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