Spatial tuning of translational optic flow responses in hawkmoths of varying body size

Rebecca Grittner,Emily Baird,Anna Stöckl

doi:10.1007/s00359-021-01530-1

Abstract

To safely navigate their environment, flying insects rely on visual cues, such as optic flow. Which cues insects can extract from their environment depends closely on the spatial and temporal response properties of their visual system. These in turn can vary between individuals that differ in body size. How optic flow-based flight control depends on the spatial structure of visual cues, and how this relationship scales with body size, has previously been investigated in insects with apposition compound eyes. Here, we characterised the visual flight control response limits and their relationship to body size in an insect with superposition compound eyes: the hummingbird hawkmoth Macroglossum stellatarum. We used the hawkmoths’ centring response in a flight tunnel as a readout for their reception of translational optic flow stimuli of different spatial frequencies. We show that their responses cut off at different spatial frequencies when translational optic flow was presented on either one, or both tunnel walls. Combined with differences in flight speed, this suggests that their flight control was primarily limited by their temporal rather than spatial resolution. We also observed strong individual differences in flight performance, but no correlation between the spatial response cutoffs and body or eye size.

Highlights

To safely navigate their environment, many flying animals rely on visual cues
Hawkmoth responses to translational optic flow compared to other insects On a general level, the hawkmoths’ responses to the lateral patterns in the tunnel were similar to those previously described in hawkmoths (Stöckl and Kelber 2019) and other insects (Kirchner and Srinivasan 1989; Baird et al 2010; Dyhr and Higgins 2010; Kern et al 2012; Chakravarthi et al 2018)
While the hawkmoths’ responses to resolvable translational optic flow patterns were similar across pattern wavelengths in the asymmetric configuration and for flight speed and lateral movement in the symmetric configuration, the centring response differed in strength depending on pattern wavelength (Fig. 3)

Summary

Introduction

To safely navigate their environment, many flying animals rely on visual cues. Insects in particular obtain information about their own position, their flight speed, their course and distance to nearby objects from wide-field image motion generated as they move through the air (Srinivasan et al 1999; Collett 2002; Egelhaaf et al 2014) called optic flow (Koenderink 1986). Whether insects can make use of the visual cues present in their environment depends on the characteristics of their eyes, and of their nervous system that subsequently processes the visual information (Baird et al 2020). The spatial sampling base of the eyes’ optics limits the absolute spatial resolution for motion detection (Borst and Egelhaaf 1989). The neural processing of the information sampled by the eyes, both in the spatial and temporal domain, sets a limit to the optic flow responses of the insects (Borst and Egelhaaf 1989). Optical and neural tuning define the species-specific spatial and temporal cutoffs of the optic flow-based flight responses

Methods

Discussion

Conclusion