On the Computations Analyzing Natural Optic Flow: Quantitative Model Analysis of the Blowfly Motion Vision Pathway

Abstract

For many animals, including humans, the optic flow generated on the eyes during locomotion is an important source of information about self-motion and the structure of the environment. The blowfly has been used frequently as a model system for experimental analysis of optic flow processing at the microcircuit level. Here, we describe a model of the computational mechanisms implemented by these circuits in the blowfly motion vision pathway. Although this model was originally proposed based on simple experimenter-designed stimuli, we show that it is also capable to quantitatively predict the responses to the complex dynamic stimuli a blowfly encounters in free flight. In particular, the model visual system exploits the active saccadic gaze and flight strategy of blowflies in a similar way, as does its neuronal counterpart. The model circuit extracts information about translation velocity in the intersaccadic intervals and thus, indirectly, about the three-dimensional layout of the environment. By stepwise dissection of the model circuit, we determine which of its components are essential for these remarkable features. When accounting for the responses to complex natural stimuli, the model is much more robust against parameter changes than when explaining the neuronal responses to simple experimenter-defined stimuli. In contrast to conclusions drawn from experiments with simple stimuli, optimization of the parameter set for different segments of natural optic flow stimuli do not indicate pronounced adaptational changes of these parameters during long-lasting stimulation.

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

“…In the present study these responses to translational optic flow are more pronounced, presumably because the speed of flying flies is much higher than that of walking flies. When HSE-Cells are confronted with the optic flow reconstructed from free flight manoeuvres the time course of the response is not proportional to the time course of the fly's rotational velocity, which casts doubt on the common view that the HSE-cell acts primarily as a rotation detector (Kern et al 2005b;Lindemann et al 2003bLindemann et al , 2005van Hateren et al 2005). These studies also show that HSE responses can provide information about translation and thus, implicitly, about the spatial relation of the animal to its surroundings during the intervals between saccades.…”

“…We simulated HS-cell responses with a computational model of the fly's visual motion pathway, that was originally developed to explain the responses to simple experimenter-designed stimuli (Borst et al 1995(Borst et al , 2003Egelhaaf and Borst 1989;Kern et al 2001a) and that was recently also shown to explain responses to optic flow generated under free-flight conditions in the laboratory (Lindemann et al 2005). The model is organized as follows ( Input images are sampled by Gaussian low-pass filters (r=2°) and fed into the model's photoreceptors, spaced equally at 2°along elevation and azimuth.…”

“…A simple equivalent circuit of a one-compartment passive membrane patch spatially pools the outputs of EMDs, where the positive and negative outputs of the EMDs control excitatory and inhibitory conductances, respectively. This processing layer is thought to correspond to the dendritic tree of the HSE-Cell (for details and parameters see Lindemann et al 2005). The model visual field covers À50°£ / £ 120°in azimuth and À50°£ h £ 50°in elevation for the right HSE.…”

“…Our results corroborate the point that differences in the appearance of natural scenes have little effect on the responses of fly motion sensitive neurons, but they also show that the dynamical properties of the behaviourally generated optic flow strongly influence the neuronal responses. This aspect has been stressed by several recent studies, which analysed the performance of identified neurons in the visual system of the fly by confronting them with image sequences as they are experienced during walking and flight in indoor environments with a 3-D structure Kern et al 2000Kern et al , 2001bKern et al , 2005bKimmerle and Egelhaaf 2000a, b;Lindemann et al 2003bLindemann et al , 2005van Hateren et al 2005;Egelhaaf 1996, 1997). During walking, the response of the HSE-Cell does reflect the animal's turning direction nearly independently of the texture and spatial layout of the environment, but is also affected by translational flow when the animal walks close to objects (Kern et al 2001a, b).…”

“…Three identified TCs of the horizontal system (HS) in each hemisphere of the blowfly brain respond in a directionally selective manner to horizontal visual motion, as it occurs for instance during rotations about the vertical (yaw) axis (Hausen 1982a, b). When optic flow as experienced in free flight is replayed to HScells the neuronal signals provide information on translational self-motion between saccades and thus, implicitly, on the spatial relation of the animal to its environment (Kern et al 2005b;Lindemann et al 2005;van Hateren et al 2005). This evidence indicates that, in contrast to previous conclusions (e.g.…”