The Critical Role of Head Movements for Spatial Representation During Bumblebees Learning Flight

Abstract

Bumblebees perform complex flight maneuvers around the barely visible entrance of their nest upon their first departures. During these flights bees learn visual information about the surroundings, possibly including its spatial layout. They rely on this information to return home. Depth information can be derived from the apparent motion of the scenery on the bees' retina. This motion is shaped by the animal's flight and orientation: Bees employ a saccadic flight and gaze strategy, where rapid turns of the head (saccades) alternate with flight segments of apparently constant gaze direction (intersaccades). When during intersaccades the gaze direction is kept relatively constant, the apparent motion contains information about the distance of the animal to environmental objects, and thus, in an egocentric reference frame. Alternatively, when the gaze direction rotates around a fixed point in space, the animal perceives the depth structure relative to this pivot point, i.e., in an allocentric reference frame. If the pivot point is at the nest-hole, the information is nest-centric. Here, we investigate in which reference frames bumblebees perceive depth information during their learning flights. By precisely tracking the head orientation, we found that half of the time, the head appears to pivot actively. However, only few of the corresponding pivot points are close to the nest entrance. Our results indicate that bumblebees perceive visual information in several reference frames when they learn about the surroundings of a behaviorally relevant location.

Optic flow based spatial vision in insects

“…This saccadic flight and gaze strategy is characterized by a sequence of often extremely fast rotations, the saccades, and by intervals in which the animals primarily translate with a largely constant gaze direction, leading to an OF on the eyes in which the translational component dominates (Fig. 2 A) (Land 1999 ; van Hateren and Schilstra 1999 ; Dickinson 2005 ; Zeil et al 2008 ; Egelhaaf et al 2012 ; Boeddeker et al 2015 ; Kress et al 2015 ; Muijres et al 2015 ; Doussot et al 2020 ). The relative duration of the intersaccades, i.e., the time during which the direction of gaze changes only slightly, accounts for more than 80% of the total flight time.…”

The potential underlying mechanisms during learning flights

“… 2018 ; Doussot et al. 2021 ) and in greenhouses (Robert et al. 2018 ), as well as outdoors (Zeil 1993 ; de Ibarra et al.…”

The influence of stimulus history on directional coding in the monarch butterfly brain

“…During locomotion, animals face a highly dynamic sensory world. For example, an insect often shows erratic flight maneuvers, which makes the sensory perception of a visual scene highly challenging (Collett and Land 1975 ; Egelhaaf et al 2012 ; Zeil 2012 ; Boeddeker et al 2015 ; Doussot et al 2021 ) mainly due to the following two spatio-temporal dynamics: the angular velocity, and the direction (trajectory). Irrespective of the dynamic nature of a visual cue, the insect’s neural system must reliably process directional information at any moment in time (Haberkern et al 2022 ).…”