Attention-like processes in insects: applications to pollinator biology and health

We live in a world flooded with visual stimuli. It is impossible to process all of these stimuli and we need to be able to selectively attend to a subset of them to perform tasks essential for survival. Attention is thus fundamentally important to sensory processing and much research has focussed on investigating attention in humans and other primates^1,2. Yet many other species across the animal kingdom also face similar challenges of ­­choosing specific targets over others to forage successfully and avoid predators. Attention-like capabilities could therefore have evolved multiple times in a diverse range of organisms.

Insects make especially interesting systems in which to study these processes. Given the vast evolutionary distance between insects and primates, neural mechanisms of attention (in primates) and attention-like processes (in insects) may have evolved to either convergent or unique solutions to selectively process visual stimuli. Comparing the two allows any common mechanisms to be identified, pointing towards fundamental computational solutions evolving in response to similar problems. However, points of difference are equally interesting, revealing alternative means of achieving attention-like processing and highlighting which mechanisms are unique to humans and other primates. Understanding attention-like processing in insects allows us to modulate it for our benefit, enhancing important insect-related sectors from pollination to pest control. Finally, these processes might be more tractable to direct neurobiological and genetic investigation in insects, thus opening up new avenues for the study of attention. There has been little research into attention-like capabilities in non-primates^3,4. In insects, it is only recently that work, has shown evidence of selective processing of visual tasks^5–14, suggesting attention-like processing. These are promising initial findings, but despite progress in the last couple of years, we still know little of the underlying processes and lack theoretical frameworks for investigating these processes in insects.

Research Program

This project will develop insects into model systems for the study of attention and test the hypothesis that the attention-like processes used by insects are analogous to attention in vertebrates. The framework of attention-like processes in insects will be used to investigate the effect of pesticides and floral chemicals on pollinator biology and the psychophysics of these processes will be modelled throughout to reveal any new algorithms for visual search and attention. I use attention-like to refer to selective processes in insects and look for whether these processes are attentional, i.e., they share the features of primate attention.

The project will use bumblebees and mantises, species with which I have extensive experience^6,7,13–19, to investigate visual attention-like processing in ecologically relevant settings. Bees are important pollinators and excellent models for studying both cognition and vision²⁰. Their ability to learn and remember rewarding targets makes them perfect for visual search experiments. They are ideal insect systems to study cognitive and top-down influences on attention. Mantises are specialized visual predators, and are the only insects known to have 3D vision^17,21. They have front-facing eyes with foveae, and clear behaviours that could be used to investigate spatial attention²². We have also established a novel paradigm to investigate mantis 3D vision^15,17,18. Mantises are therefore perfect systems for studying insect spatial attention, including in three dimensional space. Studying two insect systems would also begin to test how general the attentional framework is across insects.

This research represents an exciting possibility of integrating diverse attentional phenomena in tractable model systems to make predictions about natural behaviour. It aims to advance the understanding of various natural insect behaviours including pollination and predation. It would for example, shed light on how bees pollinate plants when present as monocultures (single targets) rather than as diverse communities (multiple targets and distractors) or on how flower nectar content (learned reward) and colour contrast (bottom-up saliency) interact to change bee sensory perception and cognition. Finally, it would also reveal the impact of pesticides on pollinator visual attention.

References

1.        Chun, M.M., and Wolfe, J.M. (2000). Visual Attention. In Blackwell Handbook of Perception, E. B. Goldstein, ed. (Massachussetts: Wiley-Blackwell), pp. 272–310.

2.        Johnson, A., and Proctor, R.W. (2004). Attention (Thousand Oaks, California: Sage Publications).

3.        Dukas, R., and Kamil, A.C. (2000). The cost of limited attention in blue jays. Behav. Ecol. 11, 502–506.

4.        Dukas, R., and Kamil, A.C. (2001). Limited attention: the constraint underlying search image. Behav. Ecol. 12, 192–199.

5.        Spaethe, J., Tautz, J., and Chittka, L. (2006). Do honeybees detect colour targets using serial or parallel visual search? J. Exp. Biol. 209, 987–993. Av

6.        Nityananda, V., and Pattrick, J.G. (2013). Bumblebee visual search for multiple learned target types. J. Exp. Biol. 216, 4154–60.

7.        Nityananda, V., Skorupski, P., and Chittka, L. (2014). Can bees see at a glance? J. Exp. Biol. 217, 1933–9.

8.        Sareen, P., Wolf, R., and Heisenberg, M. (2011). Attracting the attention of a fly. Proc. Natl. Acad. Sci. U. S. A. 108, 7230–7235.

9.        Wiederman, S.D., and O’Carroll, D.C. (2012). Selective attention in an insect visual neuron. Curr. Biol. 23, 1–6.

10.      Paulk, A.C., Stacey, J.A., Pearson, T.W.J., Taylor, G.J., Moore, R.J.D., Srinivasan, M. V., and van Swinderen, B. (2014). Selective attention in the honeybee optic lobes precedes behavioral choices. Proc. Natl. Acad. Sci. U. S. A. 111, 5006–5011.

11.     Van Swinderen, B., and Greenspan, R.J. (2003). Salience modulates 20-30 Hz brain activity in Drosophila. Nat. Neurosci. 6, 579–86.

12. De Bivort B. L., and van Swinderen, B. (2016) Evidence for selective attention in the insect brain. Curr. Opin. Insect Sci. 15, 9–15.

13.      Nityananda, V. (2016). Attention-like processes in insects. Proc. R. Soc. B Biol. Sci. 283, 20161986.

14.      Nityananda, V., and Chittka, L. (2015). Modality-specific attention in foraging bumblebees. R. Soc. Open Sci. 2, 150324. A

15.      Nityananda, V., Tarawneh, G., Henriksen, S., Umeton, D., Simmons, A., and Read, J.C.A. (2018). A Novel Form of Stereo Vision in the Praying Mantis. Curr. Biol. 28, 588–593.

16.      Nityananda, V., Tarawneh, G., Jones, L., Busby, N., Herbert, W., Davies, R., and Read, J.C.A.A. (2015). The contrast sensitivity function of the praying mantis Sphodromantis lineola. J. Comp. Physiol. A 201, 741–750.

17.      Nityananda, V., Tarawneh, G., Rosner, R., Nicolas, J., Crichton, S., and Read, J.C. (2016). Insect stereopsis demonstrated using a 3D insect cinema. Sci. Rep. 6, 18718.

18.      Nityananda, V., Bissianna, G., Tarawneh, G., and Read, J.C.A. (2016). Small or far away? Size and distance perception in the praying mantis. Philos. Trans. R. Soc. B 371, 20150262.

19.      Nityananda, V., Tarawneh, G., Errington, S., Serrano-Pedraza, I., and Read, J.C.A. (2016). The optomotor response of the praying mantis is driven predominantly by the central visual field. J. Comp. Physiol. A.

20.      Avarguès-Weber, A., Deisig, N., and Giurfa, M. (2011). Visual cognition in social insects. Annu. Rev. Entomol. 56, 423–43.

21.      Rossel, S. (1983). Binocular stereopsis in an insect. Nature 302, 821–822.

22.      Prete, F.R., and Mahaffey, R.J. (1993). Appetitive responses to computer-generated visual stimuli by the praying mantis Sphodromantis lineola (Burr.). Vis. Neurosci. 10, 669–679.