Motion cues improve the performance of harnessed bees in a colour learning task

Abstract

The proboscis extension conditioning (PER) is a successful behavioural paradigm for studying sensory and learning mechanisms in bees. Whilst mainly used with olfactory and tactile stimuli, more recently reliable PER conditioning has been achieved with visual stimuli such as colours and looming stripes. However, the results reported in different studies vary quite strongly, and it remains controversially discussed how to best condition visual PER. It is particularly striking that visual PER leads to more limited performance as compared to visual conditioning of free-flying bees. It could be that visual PER learning is affected by the lack of movement and that the presence of visual motion cues could compensate for it. We tested whether bees would show differences in learning performances when conditioned either with a colour and motion stimulus in combination or with colour alone. Colour acquisition was improved in the presence of the motion stimulus. The result is consistent with the idea that visual learning might be tightly linked to movement in bees, given that they use vision predominantly during flight. Our results further confirm recent findings that successful visual PER conditioning in bees is achievable without obligatorily removing the antennae.

Length of stimulus presentation and visual angle are critical for efficient visual PER conditioning in the restrained honey bee,Apis mellifera

“…In the present study, we showed that restrained workers of the Western honey bee Apis mellifera carnica with intact antennae were capable of learning and discriminating between two monochromatic lights by using the PER paradigm. Whereas early studies stated that visual PER conditioning is only successful when the bee's antennae were ablated, recent studies revealed different results (Balamurali et al, 2015;Dobrin and Fahrbach, 2012;Jernigan et al, 2014;Lichtenstein et al, 2015;Riveros and Gronenberg, 2012). The present study provides further evidence that antennal deprivation is not necessary for successful color learning in restrained honey bees.…”

“…More than 60 years ago, Kuwabara (1957) conducted the first study of visual PER conditioning to investigate color learning of restrained honey bees and concluded that visual PER conditioning is only successful when bees are deprived of their antennae. Several studies confirmed his observation (Hori et al, 2006;Mota et al, 2011;Niggebrugge et al, 2009); but recently, other studies have shown successful conditioning of a visual stimulus with a sucrose reward using the PER in intact honey bees (Balamurali et al, 2015;Dobrin and Fahrbach, 2012;Jernigan et al, 2014) and bumble bees (Lichtenstein et al, 2015;Riveros and Gronenberg, 2012). However, at least for the Western honey bee, the performance level reached in restrained individuals with intact antennae was significantly lower than that achieved with olfactory conditioning (Dobrin and Fahrbach, 2012) or conditioning was only successful in combination with olfactory (Mota et al, 2011) or motion cues (Balamurali et al, 2015).…”

“…The mode of stimulus presentation might also affect learning speed and performance. In most previous studies on PER color learning, stimuli were presented using LEDs or monochromatic filters, by globally illuminating the whole training setup from above (Hori et al, 2006;Mota et al, 2011), or presenting the color stimuli from below (Dobrin and Fahrbach, 2012;Jernigan et al, 2014;Riveros and Gronenberg, 2012) or from the front (Balamurali et al, 2015). In contrast, in our setup, every harnessed bee was held in a single small quadratic chamber and the color stimulus was presented directly from the top of the chamber.…”

Visual discrimination transfer and modulation by biogenic amines in honeybees

“…The methodology used here proved to be equally effective in conditioning antennae-deprived and intact harnessed bees to a visual differential task. After adapting (in different ways) previously published protocols for conditioning intact harnessed bees to visual stimuli (Dobrin and Fahrbach, 2012;Jernigan et al, 2014;Balamurali et al, 2015), we believe that some parameters were important to reach this goal in our laboratory: (i) complete darkness of the conditioning environment; (ii) large size and lateral presentation of the visual stimuli; and (iii) inclination of the bee body at 45 deg. Although these seemed to be important parameters for the success of our classical conditioning protocol, further controlled studies are necessary to understand how and to what extent they modulate appetitive visual learning in harnessed honeybees.…”

Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay

“…It has proven difficult, however, to achieve successful conditioning of color stimuli with rewards or punishment in harnessed honey bees. Differential conditioning with a reward-paired color stimulus and a non-rewarded color stimulus resulted in moderate learning rates when the antennae were ablated (Kuwabara, 1957; Hori et al, 2006, 2007; Niggebrugge et al, 2009), when the bee was able to turn her head easily (Dobrin and Fahrbach, 2012) or when the color stimulus was combined with movement (Balamurali et al, 2015). Colored light, however, has been used successfully as a context for olfactory learning in PER when presented as an occasion-setter (Mota et al, 2011) or in a reinstatement paradigm (Plath et al, 2012).…”