Encoding of Naturalistic Optic Flow by a Population of Blowfly Motion-Sensitive Neurons

Abstract

To analyze the coding properties of neuronal populations sensory stimuli have usually been used that were much simpler than those encountered in real life. It has been possible only recently to stimulate visual interneurons of the blowfly with naturalistic visual stimuli reconstructed from eye movements measured during free flight. Therefore we now investigate with naturalistic optic flow the coding properties of a small neuronal population of identified visual interneurons in the blowfly, the so-called VS and HS neurons. These neurons are motion sensitive and directionally selective and are assumed to extract information about the animal's self-motion from optic flow. We could show that neuronal responses of VS and HS neurons are mainly shaped by the characteristic dynamical properties of the fly's saccadic flight and gaze strategy. Individual neurons encode information about both the rotational and the translational components of the animal's self-motion. Thus the information carried by individual neurons is ambiguous. The ambiguities can be reduced by considering neuronal population activity. The joint responses of different subpopulations of VS and HS neurons can provide unambiguous information about the three rotational and the three translational components of the animal's self-motion and also, indirectly, about the three-dimensional layout of the environment. I N T R O D U C T I O NEven single aspects of the world, such as the orientation of contours or the frequency of a tone, induce an activity pattern spread over multiple neurons. A given environmental situation, such as the movements of an animal in its environment, is reflected in this neuronal population activity rather than in the responses of single neurons. Population coding of sensory information has been analyzed in many studies (e.g., Averbeck and Lee 2004;Deadwyler and Hampson 1997;Nirenberg and Latham 1998;Pouget et al. 2000). The sensory input an animal encounters in real life, however, may have much more complex properties than the experimenter-defined stimuli usually used in these studies (for review see Reinagel 2001).We analyze the coding properties of a population of motionsensitive visual interneurons in the blowfly with naturalistic stimuli generated actively by the animal during nearly unrestrained behavior. This neuronal population consists of two classes of neurons, the 10 VS (vertical system) neurons (Hengstenberg 1982;Hengstenberg et al. 1982;Krapp et al. 1998) and the three HS (horizontal system) neurons (Hausen 1982a,b) whose response properties and function in visually guided behavior have been characterized in great detail (for reviews see Borst and Haag 2002;Egelhaaf et al. 2002Egelhaaf et al. , 2004. HS neurons are excited primarily by front-to-back motion and their receptive fields jointly cover one visual hemisphere. The latter is also true for VS neurons, which are most sensitive to downward motion within a vertical stripe of the visual field (Fig. 1A). Based on their receptive field properties (Krapp et al. 1998(Krap...

Encoding of Yaw in the Presence of Distractor Motion: Studies in a Fly Motion Sensitive Neuron

“…Previous work suggests that optic flow from natural flight Boeddeker et al, 2005;van Hateren et al, 2005;Karmeier et al, 2006) and higher-order motion stimulus (Quenzer and Zanker, 1991;Lee and Nordström, 2012) contain motion components that can evoke neural response. A strong enough motion along a nonoptimal axis can also induce neural excitation (Karmeier et al, 2003).…”

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.…”

“…Being an output neuron of the system and sensitive to horizontal movement (Hausen 1984), HSE is probably one of the most important neurons involved in controlling horizontal turns. Nonetheless, several additional neurons are likely to be involved in visual flight control, especially if all degrees of freedom of locomotion are taken into account (Karmeier et al 2006). (3) The forward velocity generated by the cyberfly was held constant, although recent observations suggest that blowflies modify their forward velocity depending on the environmental properties (Kern et al, in preparation).…”

“…In particular, we analysed the significance of sideward drift after saccadic turns that is one of the most distinguishing features of blowfly flight behaviour. The sideward components of head and body movements were concluded to be encoded in the responses of HSE neuron (Karmeier et al 2006;Kern et al 2005Kern et al , 2006. Sideward movements could be useful in the context of obstacle avoidance, if the blowfly is oriented perpendicular to an obstacle.…”

“…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).…”