Cold-induced anesthesia impairs path integration memory in dung beetles

Ayse Yilmaz,Yakir Gagnon,Marcus Byrne,Emily Baird,Marie Dacke

doi:10.1016/j.cub.2021.10.067

Ayse Yilmaz, Yakir Gagnon + Show 3 more

Open Access

https://doi.org/10.1016/j.cub.2021.10.067

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Abstract

Path integration is a general mechanism used by many animals to maintain an updated record of their position in relation to a set reference point.1-11 To do this, they continually integrate direction and distance information into a memorized home vector. What remains unclear is how this vector is stored, maintained, and utilized for successful navigation. A recent computational model based on the neuronal circuitry of the insect central complex suggests that home vector memories are encoded across a set of putative memory neurons and maintained through ongoing recurrent neural activity.12 To better understand the nature of the home vector memory and experimentally assess underlying mechanisms for maintaining it, we performed a series of experiments on the path integrating dung beetle Scarabaeus galenus.13 We found that, while the directional component of the home vector was maintained for up to 1 h, the distance component of the vector memory decreased gradually over time. Using cold-induced anesthesia, we disrupted the neural activity of beetles that had stored a home vector of known length and direction. This treatment diminished both components of the home vector memory, but by different amounts-the homing beetles lost their distance memory before their directional memory. Together, these findings present new insights into the functional properties of home vector memories and provide the first empirical evidence that a biological process that can be disrupted by cold-induced anesthesia is essential to support homing by path integration.

Highlights

0.33 m from their point of release. This clearly confirmed that beetles could maintain and follow the direction and distance components of their home vector even after being caught at the feeder, immobilized, isolated in the dark, and transported to a new location (Figures 1Ai and 1Bi; Table 1)
In contrast to the stability of the angular component of the vector, the cold anesthetized beetles initiated their search behavior already at a radial distance of 0.43 ± 0.33 m (n = 14) from their point of release. This is significantly shorter than the 1.01 ± 0.56 m (n = 13, mean ± SD) recorded for the beetles immobilized for 10 min at ambient temperatures (p = 0.003, t test) (Figure 2C) and clearly shows that cold-induced anesthesia had a stronger effect on the distance component of the vector memory than on the angular component
Our findings provide the first empirical data showing that a biological mechanism that can be disrupted by coldinduced anesthesia is required for maintaining home vector memories

Summary

Introduction

Beetles trained to forage over distances of 1.25 or 2.55 m were immobilized in the dark for up to 120 min at ambient temperature or on ice. Vector length defines the radial distance traveled from the point of release in the test area until the turning point, i.e., where the beetle expects to find its burrow. This was done by placing immobilized beetles (with an expected home vector of 2.55 m) on ice for 10 or 60 min (body temperature lowered to 10.3C ± 1.8C and 1.5C ± 0.7C [mean ± SD, n = 10], respectively) (Figure S2A).

Results

Conclusion