The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

Abstract

Traditional models of insect vision have assumed that insects are only capable of low-level analysis of local cues and are incapable of global, holistic perception. However, recent studies on honeybee (Apis mellifera) vision have refuted this view by showing that this insect also processes complex visual information by using spatial configurations or relational rules. In the light of these findings, we asked whether bees prioritize global configurations or local cues by setting these two levels of image analysis in competition. We trained individual freeflying honeybees to discriminate hierarchical visual stimuli within a Y-maze and tested bees with novel stimuli in which local and/or global cues were manipulated. We demonstrate that even when local information is accessible, bees prefer global information, thus relying mainly on the object's spatial configuration rather than on elemental, local information. This preference can be reversed if bees are pre-trained to discriminate isolated local cues. In this case, bees prefer the hierarchical stimuli with the local elements previously primed even if they build an incorrect global configuration. Pre-training with local cues induces a generic attentional bias towards any local elements as local information is prioritized in the test, even if the local cues used in the test are different from the pre-trained ones. Our results thus underline the plasticity of visual processing in insects and provide new insights for the comparative analysis of visual recognition in humans and animals.

Attention-like processes in insects

“…In these experiments, they do learn to make the selective discriminations required from both tasks [26]. Prior learning experience can also modify bees' natural preference for global information and lead to them selectively attending to local information over global features in a stimulus [71]. These examples seem to make a clear case for learning and memory influencing a bee's visual search behaviour during foraging tasks.…”

Recognition of human face images by the free flying wasp Vespula vulgaris

“…For example, bees may need to memorize complex flower patterns to avoid deceptive plant flowers (Stejskal, Streinzer, Dyer, Paulus, & Spaethe, 2015). Interestingly, it has also been demonstrated that honeybees have the capacity to rely on configural processing with prolonged visual experience (Avarguès-Weber, Portelli, et al, 2010;Stach, Benard, & Giurfa, 2004;Stach & Giurfa, 2005), thus offering a fascinating parallel with primate visual processing (Avarguès-Weber et al, 2015).…”

“…In parallel, the honeybee has emerged as a major model of visual cognitive processing in insects (Avarguès-Weber, Deisig, & Giurfa, 2011;Avarguès-Weber, Dyer, Combe, & Giurfa, 2012;Avarguès-Weber, Dyer, Ferrah, & Giurfa, 2015;Avarguès-Weber & Giurfa, 2013;Chittka & Niven, 2009;Howard, Avarguès-Weber, Garcia, & Dyer, 2017;Srinivasan, 2010). The honeybee can be trained to solve perceptually or cognitively difficult visual tasks in free-flying conditions by collecting sucrose associated with a target visual stimulus while an alternative stimulus offers a distasteful substance (quinine; Avarguès-Weber, de Brito Sanchez, et al, 2010).…”

“…The honeybee can be trained to solve perceptually or cognitively difficult visual tasks in free-flying conditions by collecting sucrose associated with a target visual stimulus while an alternative stimulus offers a distasteful substance (quinine; Avarguès-Weber, de Brito Sanchez, et al, 2010). Honeybees are very amenable to visual cognitive studies as individuals collect nutrition for the entire colony, returning to the hive to offload the food collected when satiated, thus retaining an intact motivation for the sucrose reward throughout the entire coarse of a day, enabling consequently long training and associated testing to understand the mechanisms underlying visual perception (Avarguès-Weber et al, 2015;Avarguès-Weber, Portelli, et al, 2010;Dyer & Griffiths, 2012;Gross et al, 2009;Stach & Giurfa, 2005). It has now been well established that individual bees can learn to recognize complex pictures, such as human faces (Dyer, Neumeyer, & Chittka, 2005;Dyer & Vuong, 2008).…”

The answer is blowing in the wind: free flying honeybees can integrate visual and mechano-sensory inputs for making complex foraging decisions

“…Bees have a trichromatic (UV-, blue-, green-sensitive) visual system, allowing fine colour (Avargues-Weber et al, 2010;Dyer et al, 2011;Peitsch et al, 1992) and spatial (Avargues-Weber et al, 2015;Giurfa et al, 1999) discrimination. Bees also possess a capacity to accurately sense olfactory cues (Giurfa and Sandoz, 2012), and a capacity to perceive tactile cues on flowers via mechano-receptive sensilla trichodea (Erber et al, 1998;Kevan and Lane, 1985).…”