Neural basis of forward flight control and landing in honeybees

Abstract

The impressive repertoire of honeybee visually guided behaviors, and their ability to learn has made them an important tool for elucidating the visual basis of behavior. Like other insects, bees perform optomotor course correction to optic flow, a response that is dependent on the spatial structure of the visual environment. However, bees can also distinguish the speed of image motion during forward flight and landing, as well as estimate flight distances (odometry), irrespective of the visual scene. The neural pathways underlying these abilities are unknown. Here we report on a cluster of descending neurons (DNIIIs) that are shown to have the directional tuning properties necessary for detecting image motion during forward flight and landing on vertical surfaces. They have stable firing rates during prolonged periods of stimulation and respond to a wide range of image speeds, making them suitable to detect image flow during flight behaviors. While their responses are not strictly speed tuned, the shape and amplitudes of their speed tuning functions are resistant to large changes in spatial frequency. These cells are prime candidates not only for the control of flight speed and landing, but also the basis of a neural ‘front end’ of the honeybee’s visual odometer.

A Model for Detection of Angular Velocity of Image Motion Based on the Temporal Tuning of the Drosophila

“…And the responses weakly depend on the spatial period of the grating. This coincides with the responses of the descending neurons according to Ibbotson's records [10,14]. And this is important for insects estimating flight speed or gauging distance of foraging journey in a clutter environment.…”

“…We simulated the OFF pathway of the Drosophila's visual neural circuits when the sinusoidal grating moving in preferred direction. The normalized responses of AVDM over different velocities and spatial periods in contrast of experimental results [14] can been seen from Fig. 4.…”

FoxP in bees: A comparative study on the developmental and adult expression pattern in three bee species considering isoforms and circuitry

“…The relatively dorsal site of our lobular injection site is compatible with the location of the layer 1–4 dendrites which are involved in motion detection in bumblebees (Paulk, Phillips‐Portillo, Dacks, Fellous, & Gronenberg, ). The tract also resembles the POT1 (posterior optic tract 1) which lies in close proximity to presynaptic endings of descending “optomotor neurons” that are able to detect rotational image flow (Ibbotson, Hung, Meffin, Boeddeker, & Srinivasan, ).…”

Visual control of landing maneuvers in houseflies on vertical and inverted surfaces

“…A recent study in bees revealed descending neurons in the ventral nerve cord monotonically increased their median firing rate with the angular velocity of a frontally presented rotating spiral stimulus, up to a specific angular velocity value beyond which the response saturated. However, the median response of the neurons was also a function of the number of arms in the rotating spiral (which correlates with spatial frequency) (Ibbotson et al, 2017). In flies, the lobula plate tangential cells integrate inputs from local motion detectors and respond to wide-field motion (for a detailed review see Borst et al, 2010).…”