Abstract
Honey bees are reputed for their remarkable visual learning and navigation capabilities. These capacities can be studied in virtual reality (VR) environments, which allow studying performances of tethered animals in stationary flight or walk under full control of the sensory environment. Here, we used a 2D VR setup in which a tethered bee walking stationary under restrictive closed-loop conditions learned to discriminate vertical rectangles differing in color and reinforcing outcome. Closed-loop conditions restricted stimulus control to lateral displacements. Consistently with prior VR analyses, bees learned to discriminate the trained stimuli. Ex vivo analyses on the brains of learners and non-learners showed that successful learning led to a downregulation of three immediate early genes in the main regions of the visual circuit, the optic lobes (OLs) and the calyces of the mushroom bodies (MBs). While Egr1 was downregulated in the OLs, Hr38 and kakusei were coincidently downregulated in the calyces of the MBs. Our work thus reveals that color discrimination learning induced a neural signature distributed along the sequential pathway of color processing that is consistent with an inhibitory trace. This trace may relate to the motor patterns required to solve the discrimination task, which are different from those underlying pathfinding in 3D VR scenarios allowing for navigation and exploratory learning and which lead to IEG upregulation.
Highlights
Learning relies on changes in neural activity and/or connectivity in the nervous system, which underlie the acquisition of new, durable information based on individual experience
We found that color learning in the 3D VR environment was associated with an upregulation of early growth response gene-1 (Egr1) in the calyces of the mushroom bodies (Geng et al, 2022), a main structure of the insect brain repeatedly associated with the storage and retrieval of olfactory memories (Heisenberg, 2003; Menzel, 2012)
Honey bee foragers from a hive located in our apiary were captured at an artificial feeder to which they were previously trained
Summary
Learning relies on changes in neural activity and/or connectivity in the nervous system, which underlie the acquisition of new, durable information based on individual experience. Pavlovian conditioning protocol that offers the possibility of acquiring consistent behavioral data coupled with the simultaneous use of invasive methods to record neural activity (Menzel, 1999, 2012; Giurfa, 2007; Giurfa and Sandoz, 2012) In this protocol, termed the olfactory conditioning of the proboscis extension reflex (PER), harnessed bees learn to associate an odorant with a reward of sucrose solution (Bitterman et al, 1983; Giurfa and Sandoz, 2012). Bees learn and memorize simple (Buatois et al, 2017, 2018) and higher-order (Buatois et al, 2020) visual discriminations, which offers the potential for mechanistic analyses of visually oriented performances (Zwaka et al, 2018; Rusch et al, 2021)
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