Mushroom Body Extrinsic Neurons in Walking Bumblebees Correlate With Behavioral States but Not With Spatial Parameters During Exploratory Behavior.

Nanxiang Jin,Randolf Menzel,Benjamin H Paffhausen,Aron Duer

doi:10.3389/fnbeh.2020.590999

Nanxiang Jin, Randolf Menzel + Show 2 more

Open Access

https://doi.org/10.3389/fnbeh.2020.590999

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Abstract

Central place foraging insects like honeybees and bumblebees learn to navigate efficiently between nest and feeding site. Essential components of this behavior can be moved to the laboratory. A major component of navigational learning is the active exploration of the test arena. These conditions have been used here to search for neural correlates of exploratory walking in the central arena (ground), and thigmotactic walking in the periphery (slope). We chose mushroom body extrinsic neurons (MBENs) because of their learning-related plasticity and their multi-modal sensitivities that may code relevant parameters in a brain state-dependent way. Our aim was to test whether MBENs code space-related components or are more involved in state-dependent processes characterizing exploration and thigmotaxis. MBENs did not respond selectively to body directions or locations. Their spiking activity differently correlated with walking speed depending on the animals’ locations: on the ground, reflecting exploration, or on the slope, reflecting thigmotaxis. This effect depended on walking speed in different ways for different animals. We then asked whether these effects depended on spatial parameters or on the two states, exploration and thigmotaxis. Significant epochs of stable changes in spiking did not correlate with restricted locations in the arena, body direction, or walking transitions between ground and slope. We thus conclude that the walking speed dependencies are caused by the two states, exploration and thigmotaxis, rather than by spatial parameters.

Highlights

Animals exposed to a novel environment perform typical searching movements during which they explore the environment
Notice that the spatial components between ground and slope are correlated with the shift between the two behavioral states, exploration on the ground and escape on the slope
The search for neural correlates of active exploration in small animals like the bumble bee imposes inevitable compromises with respect to the kind of movement, the size of the test arena, the motivation of the animal and the confinement imposed on the animal by the border of the arena

Summary

Introduction

Animals exposed to a novel environment perform typical searching movements during which they explore the environment. The central complex has been related to the sun compass (Homberg, 2004; Collett, 2019; Currier and Nagel, 2020), and the mushroom body (MB) to multiple forms of learning about object identities (Menzel, 2014). In most of these studies the animals were not able to actively explore the environment, rather they were restricted to experimental conditions that allowed researchers to combine neural recordings with tests of innate control mechanisms and Pavlovian forms of associative learning (Menzel et al, 2007). Essential to separate neural correlates of spatial coding from state-dependent behavioral states that cause the animal to switch between exploration and thigmotaxis

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