Abstract
Navigating animals combine multiple perceptual faculties, learn during exploration, retrieve multi-facetted memory contents, and exhibit goal-directedness as an expression of their current needs and motivations. Navigation in insects has been linked to a variety of underlying strategies such as path integration, view familiarity, visual beaconing, and goal-directed orientation with respect to previously learned ground structures. Most works, however, study navigation either from a field perspective, analyzing purely behavioral observations, or combine computational models with neurophysiological evidence obtained from lab experiments. The honey bee (Apis mellifera) has long been a popular model in the search for neural correlates of complex behaviors and exhibits extraordinary navigational capabilities. However, the neural basis for bee navigation has not yet been explored under natural conditions. Here, we propose a novel methodology to record from the brain of a copter-mounted honey bee. This way, the animal experiences natural multimodal sensory inputs in a natural environment that is familiar to her. We have developed a miniaturized electrophysiology recording system which is able to record spikes in the presence of time-varying electric noise from the copter's motors and rotors, and devised an experimental procedure to record from mushroom body extrinsic neurons (MBENs). We analyze the resulting electrophysiological data combined with a reconstruction of the animal's visual perception and find that the neural activity of MBENs is linked to sharp turns, possibly related to the relative motion of visual features. This method is a significant technological step toward recording brain activity of navigating honey bees under natural conditions. By providing all system specifications in an online repository, we hope to close a methodological gap and stimulate further research informing future computational models of insect navigation.
Highlights
Where should we look for neuronal correlates of navigation? The central complex was found to house neurons essential for sun compass related navigation (Homberg et al, 2011)
We propose a novel methodology to record neuronal activity from mushroom body extrinsic neurons (MBENs) of honey bees on a quadcopter
We propose a novel methodology in the search for the neural correlates of navigation in bees
Summary
Visual guidance using view memories or structured landmark memories may play a role. It is still unknown whether and how those components are combined and at which level of computation they may be available to a navigating bee (Collett, 2019; Webb, 2019). The search for the neural correlates of navigation has made considerable progress through experiments in which the recorded animal was able to move freely in close-to-natural environments (O’Keefe and Nadel, 1979; Bingman and Able, 2002; Hafting et al, 2005; Rubin et al, 2014; Eliav et al, 2021)
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