Coping with Space Neophobia in Drosophila melanogaster: The Asymmetric Dynamics of Crossing a Doorway to the Untrodden

TL;DR

This study investigates how Drosophila melanogaster adapt their behavior over days to overcome space neophobia when crossing a doorway to an unexplored area, revealing potential cognitive processes involved.

Contribution

It introduces an ethologically relevant experimental setup to study space neophobia in flies and compares their behavior to mice, suggesting possible cognitive mechanisms and deep homology.

Findings

Flies initially treat the doorway as a barrier, requiring repeated approaches.

Over days, flies learn to avoid returning, spending more time in the new area.

Behavioral dynamics in flies resemble those observed in mouse models of anxiety.

Abstract

Insects exhibit remarkable cognitive skills in the field and several cognitive abilities have been demonstrated in Drosophila in the laboratory. By devising an ethologically relevant experimental setup that also allows comparison of behavior across remote taxonomic groups we sought to reduce the gap between the field and the laboratory, and reveal as yet undiscovered ethological phenomena within a wider phylogenetic perspective. We tracked individual flies that eclosed in a small (45mm) arena containing a piece of fruit, connected to a larger (130mm) arena by a wide (5mm) doorway. Using this setup we show that the widely open doorway initially functions as a barrier: the likelihood of entering the large arena increases gradually, requiring repeated approaches to the doorway, and even after entering the flies immediately return. Gradually the flies acquire the option to avoid returning, spending more relative time and performing relatively longer excursions in the large arena. The entire process may take up three successive days. This behavior constitutes coping with space neophobia, the avoidance of untrodden space. It appears to be the same as the neophobic doorway-crossing reported in mouse models of anxiety. In both mice and flies the moment-to-moment developmental dynamics of transition between trodden and untrodden terrain appear to be the same, and in mice it is taken to imply memory and, therefore, cognition. Recent claims have been made for a deep homology between the arthropod central complex and the vertebrate basal ganglia, two structures involved in navigation. The shared dynamics of space occupancy in flies and mice might indicate the existence of cognitive exploration also in the flies or else a convergent structure exhibiting the same developmental dynamics.