An intrinsic oscillator underlies visual navigation in ants

Abstract

AbstractControlling behavior implies a constant balance between exploration – to gather information – and exploitation – to use this information to reach one’s goal. However, how this tradeoff is achieved in navigating animals is unclear. Here we recorded the paths of two phylogenetically distant visually navigating ant species (Myrmecia croslandi and Iridomyrmex purpureus) using a trackball-treadmill directly in their habitat. We show that both species continuously produce regular lateral oscillations with bursts of forward movement when facing the general direction of travel, providing a remarkable tradeoff between visual exploration across directions and movement areas. This dynamical signature is conserved across navigational contexts but requires certain visual cues to be fully expressed. Rotational feedback regulates the extent of turns, but is not required to produce them, indicating that oscillations are generated intrinsically. Learnt visual information modulates the oscillation’s amplitudes to fit the task at hand in a continuous manner: an unfamiliar panorama enhances the amplitude of oscillations in both naïve and experienced ants, favoring visual exploration; while a learnt familiar panorama reduces them, favoring exploitation through. The observed dynamical signature readily emerges from a simple neural-circuit model of the insect’s conserved pre-motor area known as the lateral accessory lobe, endorsing oscillations as a core, ancestral way of moving in insects. We discuss the importance and evolution of self-generated behaviors and how such an oscillator has been exapted to various modalities, behaviors and way of moving.