Responses of blowfly motion-sensitive neurons to reconstructed optic flow along outdoor flight paths

Abstract

The retinal image flow a blowfly experiences in its daily life on the wing is determined by both the structure of the environment and the animal's own movements. To understand the design of visual processing mechanisms, there is thus a need to analyse the performance of neurons under natural operating conditions. To this end, we recorded flight paths of flies outdoors and reconstructed what they had seen, by moving a panoramic camera along exactly the same paths. The reconstructed image sequences were later replayed on a fast, panoramic flight simulator to identified, motion sensitive neurons of the so-called horizontal system (HS) in the lobula plate of the blowfly, which are assumed to extract self-motion parameters from optic flow. We show that under real life conditions HS-cells not only encode information about self-rotation, but are also sensitive to translational optic flow and, thus, indirectly signal information about the depth structure of the environment. These properties do not require an elaboration of the known model of these neurons, because the natural optic flow sequences generate-at least qualitatively-the same depth-related response properties when used as input to a computational HS-cell model and to real neurons.

A `bright zone' in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity

“…Without information on these properties and their variation across the receptive fields of these neurons, the local responses of fly LPTCs will be difficult to predict for arbitrary moving patterns. With such data, however, increasingly accurate predictions of the responses to velocity can be made (Boeddeker et al, 2005;Dror et al, 2001;Lindemann et al, 2005;Shoemaker et al, 2005).…”

Blowfly flight characteristics are shaped by environmental features and controlled by optic flow information

“…It is characterized by periods where body orientation stays relatively constant and by brief saccadic turns where the animal reaches high rotation velocities (e.g. Boeddeker et al, 2005;Braun et al, 2010;Braun et al, 2012;Collett and Land, 1975;Geurten et al, 2010;Mronz and Lehmann, 2008;Ribak and Swallow, 2007;Schilstra and van Hateren, 1999;Tammero and Dickinson, 2002a;Wagner, 1985;Wagner, 1986;Zeil, 1983;Zeil, 1986). Body saccades are accompanied by head saccades.…”

Saccadic flight strategy facilitates collision avoidance: closed-loop performance of a cyberfly

“…In previous studies we could show that a population of output neurons in the blowfly visual motion pathway extracts information about all self-motion components from the complex optic flow patterns generated on the eyes while the blowfly is flying around in its environment (Boeddeker et al 2005;Karmeier et al 2006;Kern et al 2005;van Hateren et al 2005). In the latter accounts the blowfly's brain is concluded to use a saccadic gaze strategy to obtain information between saccades about the spatial layout of the environment.…”

“…This type of controller implements the classical hypothesis drawn from behavioural optomotor experiments on tethered flying or walking flies with the animal turning on the spot in response to a purely rotating environment [see, e.g., Götz 1975 (Drosophila); Warzecha and Egelhaaf 1996 (Lucilia)]. The second controller (saccadic controller) implements the saccadic flight mode observed in freely flying flies in laboratory Kern et al, in preparation) and outdoor environments (Boeddeker et al 2005). This type of controller generates short purely translational flight segments interleaved with sharp fast turns mimicking the body saccades observed in flies.…”

“…On the one hand, large parts of the blowfly visual system are involved in optic flow processing and, on the other hand, experimental analysis can be performed on blowflies by a broad spectrum of methods. Only recently it became possible, thanks to novel technologies, to investigate optic flow processing using visual stimuli which come very close to what flies have seen during their acrobatic flight manoeuvres (Boeddeker et al 2005;Karmeier et al 2006;Kern et al 2005;Lindemann et al 2003;van Hateren et al 2005).…”