Seeing near and seeing far; behavioural evidence for dual mechanisms of pattern vision in the honeybee (Apis mellifera)

Abstract

SUMMARYVisual perception is a primary modality for interacting with complex environments. Recent work has shown that the brain and visual system of the honeybee is able, in some cases, to learn complex spatial relationships, while in other cases, bee vision is relatively rudimentary and based upon simple elemental-type visual processing. In the present study, we test the ability of honeybees to learn 4-bar asymmetric patterns in a Y-maze with aversive-appetitive differential conditioning. In Experiment 1, a group of bees were trained at a small visual angle of 50deg by constraining individuals to the decision chamber within the Ymaze. Bees learned this task, and were able to solve the task even in the presence of background noise. However, these bees failed to solve the task when the stimuli were presented at a novel visual angle of 100deg. In Experiment 2, a separate group of bees were trained to sets of 4-bar asymmetric patterns that excluded retinotopic matching and, in this case, bees learned the configural rule describing stimuli at a visual angle of approximately 50deg, and this allowed the bees to solve the task when the stimuli were presented at a novel vision angle of 100deg. This shows that the bee brain contains multiple mechanisms for pattern recognition, and what a bee sees is very dependent upon the specific experience that it receives. These multiple mechanisms would allow bees to interact with complex environments to solve tasks like recognising landmarks at variable distances or quickly discriminating between rewarding/non-rewarding flowers at reasonable constant visual angles. Supplementary material available online at

The mysterious cognitive abilities of bees: why models of visual processing need to consider experience and individual differences in animal performance

“…Thus, there appears to be no mystery about the cognitive ability in bees. Data from several experiments show that highly trained and experienced bees exhibit behaviour that is consistent the definition of cognition (Avarguès-Weber et al, 2011b;Chittka et al, 2003;Dacke and Srinivasan, 2008;Dyer and Griffiths, 2011;Dyer and Vuong, 2008;Gross et al, 2009;Ings and Chittka, 2008;Zhang and Srinivasan, 1994).…”

“…In this case bees had learned a relationship rule that enabled extrapolation to a visual task that was well beyond the range of variation encountered in the training phase of the experiment. Comparing these two different results from the same study with stimuli of similar configuration suggests that in some cases bees do use a relatively simple retinotopic or elemental-type recognition system, while in other cases their vision is much more complex and consistent with rule-based cognitive visual processing (Dyer and Griffiths, 2011). Importantly, in both tested experimental conditions, individual honeybees were able to learn configured spatial stimuli at a small visual angle that was predicted not to be possible according to simple elemental models (Horridge, 2009a;Horridge, 2009b).…”

“…Behavioural experiments suggest that pattern vision in bees may be mediated by separate mechanisms that include retinotopic matching and/or configural-based rule learning, depending upon the context and level of individual experience of a bee Efler and Ronacher, 2000;Giger and Srinivasan, 1995). Recent work that has evaluated bee spatial vision using a combination of appetitive and aversive differential conditioning for an extended training period clearly shows that bees can learn a task stated to be impossible according to simple elemental models of bee vision (Dyer and Griffiths, 2011). This new behavioural work thus shows that models of insect vision based upon simple mechanistic explanations need to be revised to consider how individual differences, experience effects and indeed cognitive influences can significantly affect the results and interpretation of behavioural experiments.…”

“…Does this mean that bees do not use simple mechanisms? A recent study did a comparative evaluation of how honeybees solved a visual task at a novel visual angle depending upon the conditioning of individual bees (Dyer and Griffiths, 2011). When one group of bees was provided with differential conditioning to the same stimulus pair at A. G. Dyer Bees in Group 1 were trained to a 0deg view and could not subsequently recognise a 30deg view; bees in Group 2 were trained to a 60deg view and could not subsequently recognise a 30deg view.…”

“…Importantly, in both tested experimental conditions, individual honeybees were able to learn configured spatial stimuli at a small visual angle that was predicted not to be possible according to simple elemental models (Horridge, 2009a;Horridge, 2009b). The reason for this new development in our understanding of insect spatial vision is the use of the appetitive-aversive differential conditioning protocol (Avarguès-Weber et al, 2010a) combined with a modified Y-maze that constrained an individual bee to making a decision at a distance (Dyer and Griffiths, 2011), which underlines the importance of careful experimental control to understand mechanisms of spatial vision.…”