Fast learning but coarse discrimination of colours in restrained honeybees.

addresses: Department of Neurobiology, Institute of Biology, Free University of Berlin, 14195 Berlin, Germany.types: Journal Article; Research Support, Non-U.S. Gov't© 2009 Company of Biologists. Post print version deposited in accordance with SHERPA RoMEO guidelines. The definitive version is available at: http://jeb.biologists.org/content/212/9/1344Colours are quickly learnt by free-moving bees in operant conditioning settings. In the present study, we report a method using the classical conditioning of the proboscis extension response (PER) in restrained honeybees (Apis mellifera), which allows bees to learn colours after just a few training trials. We further analysed how visual learning and discrimination is influenced by the quality of a stimulus by systematically varying the chromatic and achromatic properties of the stimuli. Using differential conditioning, we found that faster colour discrimination learning was correlated with reduced colour similarity between stimuli. In experiments with both absolute and differential conditioning, restrained bees showed poor colour discrimination and broad generalisation. This result is in strong contrast to the well-demonstrated ability of bees to finely discriminate colours under free-flight conditions and raises further questions about the temporal and perceptual processes underlying the ability of bees to discriminate and learn colours in different behavioural contexts

Visual Associative Learning in Restrained Honey Bees with Intact Antennae

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

Mechanisms, functions and ecology of colour vision in the honeybee.

notes: PMCID: PMC4035557types: Journal Article© The Author(s) 2014.This is an open access article that is freely available in ORE or from Springerlink.com. Please cite the published version available at: http://link.springer.com/article/10.1007%2Fs00359-014-0915-1Research in the honeybee has laid the foundations for our understanding of insect colour vision. The trichromatic colour vision of honeybees shares fundamental properties with primate and human colour perception, such as colour constancy, colour opponency, segregation of colour and brightness coding. Laborious efforts to reconstruct the colour vision pathway in the honeybee have provided detailed descriptions of neural connectivity and the properties of photoreceptors and interneurons in the optic lobes of the bee brain. The modelling of colour perception advanced with the establishment of colour discrimination models that were based on experimental data, the Colour-Opponent Coding and Receptor Noise-Limited models, which are important tools for the quantitative assessment of bee colour vision and colour-guided behaviours. Major insights into the visual ecology of bees have been gained combining behavioural experiments and quantitative modelling, and asking how bee vision has influenced the evolution of flower colours and patterns. Recently research has focussed on the discrimination and categorisation of coloured patterns, colourful scenes and various other groupings of coloured stimuli, highlighting the bees' behavioural flexibility. The identification of perceptual mechanisms remains of fundamental importance for the interpretation of their learning strategies and performance in diverse experimental tasks.Biotechnology and Biological Sciences Research Council (BBSRC

Toxic but Drank: Gustatory Aversive Compounds Induce Post-ingestional Malaise in Harnessed Honeybees

BACKGROUND: Deterrent substances produced by plants are relevant due to their potential toxicity. The fact that most of these substances have an unpalatable taste for humans and other mammals contrasts with the fact that honeybees do not reject them in the range of concentrations in which these compounds are present in flower nectars. Here we asked whether honeybees detect and ingest deterrent substances and whether these substances are really toxic to them. RESULTS: We show that pairing aversive substances with an odor retards learning of this odor when it is subsequently paired with sucrose. Harnessed honeybees in the laboratory ingest without reluctance a considerable volume (20 µl) of various aversive substances, even if some of them induce significant post-ingestional mortality. These substances do not seem, therefore, to be unpalatable to harnessed bees but induce a malaise-like state that in some cases results in death. Consistently with this finding, bees learning that one odor is associated with sugar, and experiencing in a subsequent phase that the sugar was paired with 20 µl of an aversive substance (devaluation phase), respond less than control bees to the odor and the sugar. Such stimulus devaluation can be accounted for by the malaise-like state induced by the aversive substances. CONCLUSION: Our results indicate that substances that taste bitter to humans as well as concentrated saline solutions base their aversive effect on the physiological consequences that their ingestion generates in harnessed bees rather than on an unpalatable taste. This conclusion is only valid for harnessed bees in the laboratory as freely-moving bees might react differently to aversive compounds could actively reject aversive substances. Our results open a new possibility to study conditioned taste aversion based on post-ingestional malaise and thus broaden the spectrum of aversive learning protocols available in honeybees

Insect Bio-inspired Neural Network Provides New Evidence on How Simple Feature Detectors Can Enable Complex Visual Generalization and Stimulus Location Invariance in the Miniature Brain of Honeybees

This work was supported by a Human Frontier Science Program Grant RGP0022/2014 to LC and Queen Mary University of London Scholarship to MR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Colour-dependent target detection by bees

No description supplie

Involvement of alpha-bungarotoxin-sensitive nicotinic brain receptors in long-term memory formation in the honeybee (Apis mellifera)

International audienc

Aversive reinforcement improves visual discrimination learning in free-flying honeybees

Background: Learning and perception of visual stimuli by free-flying honeybees has been shown to vary dramatically depending on the way insects are trained. Fine color discrimination is achieved when both a target and a distractor are present during training (differential conditioning), whilst if the same target is learnt in isolation (absolute conditioning), discrimination is coarse and limited to perceptually dissimilar alternatives. Another way to potentially enhance discrimination is to increase the penalty associated with the distractor. Here we studied whether coupling the distractor with a highly concentrated quinine solution improves color discrimination of both similar and dissimilar colors by free-flying honeybees. As we assumed that quinine acts as an aversive stimulus, we analyzed whether aversion, if any, is based on an aversive sensory input at the gustatory level or on a post-ingestional malaise following quinine feeding. Methodology/Principal Findings: We show that the presence of a highly concentrated quinine solution (60 mM) acts as an aversive reinforcer promoting rejection of the target associated with it, and improving discrimination of perceptually similar stimuli but not of dissimilar stimuli. Free-flying bees did not use remote cues to detect the presence of quinine solution; the aversive effect exerted by this substance was mediated via a gustatory input, i.e. via a distasteful sensory experience, rather than via a post-ingestional malaise. Conclusion: The present study supports the hypothesis that aversion conditioning is important for understanding how and what animals perceive and learn