Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task

Abstract

Bees use visual memories to find the spatial location of previously learnt food sites. Characteristic learning flights help acquiring these memories at newly discovered foraging locations where landmarks—salient objects in the vicinity of the goal location—can play an important role in guiding the animal's homing behavior. Although behavioral experiments have shown that bees can use a variety of visual cues to distinguish objects as landmarks, the question of how landmark features are encoded by the visual system is still open. Recently, it could be shown that motion cues are sufficient to allow bees localizing their goal using landmarks that can hardly be discriminated from the background texture. Here, we tested the hypothesis that motion sensitive neurons in the bee's visual pathway provide information about such landmarks during a learning flight and might, thus, play a role for goal localization. We tracked learning flights of free-flying bumblebees (Bombus terrestris) in an arena with distinct visual landmarks, reconstructed the visual input during these flights, and replayed ego-perspective movies to tethered bumblebees while recording the activity of direction-selective wide-field neurons in their optic lobe. By comparing neuronal responses during a typical learning flight and targeted modifications of landmark properties in this movie we demonstrate that these objects are indeed represented in the bee's visual motion pathway. We find that object-induced responses vary little with object texture, which is in agreement with behavioral evidence. These neurons thus convey information about landmark properties that are useful for view-based homing.

Differential Tuning to Visual Motion Allows Robust Encoding of Optic Flow in the Dragonfly

“…Encoding both fast and slow motion places extensive demands on the neuronal networks underlying self-motion detection. Neurons that respond robustly to patterns of wide-field motion have been studied in several insect groups, including Dipteran flies (Hausen, 1982;Hausen and Egelhaaf, 1989), moths (Wicklein and Varju, 1999;Theobald et al, 2010;Stöckl et al, 2016), and bees (DeVoe et al, 1982;Ibbotson, 1991;Mertes et al, 2014). Typified by lobula plate tangential cells (LPTCs) of Dipteran flies, these neurons take input from local elementary motion detection (EMD) elements located in the medulla (Borst et al, 2010) and use local correlation of spatially separated inputs with asymmetric delay mechanisms, consistent with influential computational motion models (Hassenstein and Reichardt, 1956; Barlow and Levick, 1965;Gruntman et al, 2018).…”

Bumblebee Homing: The Fine Structure of Head Turning Movements

“…One important reason for using bumblebees as a model animal is the possibility to house them indoors, which allows experiments throughout the year [ 29 ]. Furthermore, bumblebees are more robust in comparison with honeybees, which makes them suitable for several neurobiological approaches like calcium imaging [ 30 ] or single cell intracellular recording [ 31 – 34 ]. Additionally, bumblebees show very similar learning abilities like honeybees, e.g.…”

Motion as a source of environmental information: a fresh view on biological motion computation by insect brains

“…Note that step-like, i.e., saccadic direction changes are more pronounced for the head than for the body. Bottom diagram: Angular yaw velocity of body (black line) and head (red line) of the same flight (Boeddeker et al, submitted; Data from Mertes et al, 2014 ). (B) Translational and rotational prototypical movements of honeybees during local landmark navigation.…”

“…Recently, it could even been shown that the intersaccadic responses of bee LWCs to visual stimuli as experienced during navigation flights in the vicinity of a goal strongly depend on the spatial layout of the environment. The spatial landmark constellation that guides the bees to their goal leads to a characteristic time-dependent response profile in LWCs during the intersaccadic intervals of navigation flights (Mertes et al, 2014 ).…”