Early visual experience and the receptive-field organization of optic flow processing interneurons in the fly motion pathway.

The distribution of local preferred directions and motion sensitivities within the receptive fields of so-called tangential neurons in the fly visual system was previously found to match optic flow fields as induced by certain self-motions. The complex receptive-field organization of the tangential neurons and the recent evidence showing that the orderly development of the fly's peripheral visual system depends on visual experience led us to investigate whether or not early visual input is required to establish the functional receptive-field properties of such tangential neurons. In electrophysiological investigations of two identified tangential neurons, it turned out that dark-hatched flies which were kept in complete darkness for 2 days develop basically the same receptive-field organization as flies which were raised under seasonal light/dark conditions and were free to move in their cages. We did not find any evidence that the development of the sophisticated receptive-field organization of tangential neurons depends on sensory experience. Instead, the input to the tangential neurons seems to be "hardwired" and the specificity of these cells to optic flow induced during self-motions of the animal may have evolved on a phylogenetical time scale.

Binocular contributions to optic flow processing in the fly visual system.

Integrating binocular motion information tunes wide-field direction-selective neurons in the fly optic lobe to respond preferentially to specific optic flow fields. This is shown by measuring the local preferred directions (LPDs) and local motion sensitivities (LMSs) at many positions within the receptive fields of three types of anatomically identifiable lobula plate tangential neurons: the three horizontal system (HS) neurons, the two centrifugal horizontal (CH) neurons, and three heterolateral connecting elements. The latter impart to two of the HS and to both CH neurons a sensitivity to motion from the contralateral visual field. Thus in two HS neurons and both CH neurons, the response field comprises part of the ipsi- and contralateral visual hemispheres. The distributions of LPDs within the binocular response fields of each neuron show marked similarities to the optic flow fields created by particular types of self-movements of the fly. Based on the characteristic distributions of local preferred directions and motion sensitivities within the response fields, the functional role of the respective neurons in the context of behaviorally relevant processing of visual wide-field motion is discussed.

Arrangement of optical axes and spatial resolution in the compound eye of the female blowfly Calliphora.

We determined the optical axes of ommatidia in the wild-type female blowfly Calliphora by inspecting the deep pseudopupil in large parts of the compound eye. The resulting map of optical axes allowed us to evaluate the spatial resolution in different parts of the eye in terms of interommatidial angles as well as the density of optical axes, and to estimate the orientation of ommatidial rows along the hexagonal eye lattice. The optical axes are not homogeneously distributed over the eye. In the frontal visual field the spatial resolution is about two times higher than in its lateral part and about three times higher as compared to the eye's dorsal pole region. The orientation of the ommatidial rows along the eye lattice is not the same for different regions of the eye but changes in a characteristic way. The inter-individual variability in the orientation of the ommatidial rows is estimated to be smaller than 8 degrees . The characteristic arrangement of the ommatidial lattice is discussed as an adaptation for efficient evaluation of optic flow as induced during self-motions of the animal.

Wide-field, motion-sensitive neurons and matched filters for optic flow fields.

The receptive field organization of a class of visual interneurons in the fly brain (vertical system, or VS neurons) shows a striking similarity to certain self-motion-induced optic flow fields. The present study compares the measured motion sensitivities of the VS neurons (Krapp et al. 1998) to a matched filter model for optic flow fields generated by rotation or translation. The model minimizes the variance of the filter output caused by noise and distance variability between different scenes. To that end, prior knowledge about distance and self-motion statistics is incorporated in the form of a "world model". We show that a special case of the matched filter model is able to predict the local motion sensitivities observed in some VS neurons. This suggests that their receptive field organization enables the VS neurons to maintain a consistent output when the same type of self-motion occurs in different situations.

Computation of object approach by a wide-field, motion-sensitive neuron.

The lobula giant motion detector (LGMD) in the locust visual system is a wide-field, motion-sensitive neuron that responds vigorously to objects approaching the animal on a collision course. We investigated the computation performed by LGMD when it responds to approaching objects by recording the activity of its postsynaptic target, the descending contralateral motion detector (DCMD). In each animal, peak DCMD activity occurred a fixed delay delta (15

Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly.

The third visual neuropil (lobula plate) of the blowfly Calliphora erythrocephala is a center for processing motion information. It contains, among others, 10 individually identifiable "vertical system" (VS) neurons responding to visual wide-field motions of arbitrary patterns. We demonstrate that each VS neuron is tuned to sense a particular aspect of optic flow that is generated during self-motion. Thus the VS neurons in the fly supply visual information for the control of head orientation, body posture, and flight steering. To reveal the functional organization of the receptive fields of the 10 VS neurons, we determined with a new method the distributions of local motion sensitivities and local preferred directions at 52 positions in the fly's visual field. Each neuron was identified by intracellular staining with Lucifer yellow and three-dimensional reconstructions from 10-micron serial sections. Thereby the receptive-field organization of each recorded neuron could be correlated with the location and extent of its dendritic arborization in the retinotopically organized neuropil of the lobula plate. The response fields of the VS neurons, i.e., the distributions of local preferred directions and local motion sensitivities, are not uniform but resemble rotatory optic flow fields that would be induced by the fly during rotations around various horizontal axes. Theoretical considerations and quantitative analyses of the data, which will be presented in a subsequent paper, show that VS neurons are highly specialized neural filters for optic flow processing and thus for the visual sensation of self-motions in the fly.

A fast stimulus procedure to determine local receptive field properties of motion-sensitive visual interneurons.

We present a method to determine, within a few seconds, the local preferred direction (LPD) and local motion sensitivity (LMS) in small patches of the receptive fields of wide-field motion-sensitive neurons. This allows us to map, even during intracellular recordings, the distribution of LPD and LMS over the huge receptive fields of neurons sensing self-motions of the animal. Comparisons of the response field of a given neuron with the optic flow fields caused by different movements in space, allows us to specify the particular motion of the animal sensed by that neuron.

Estimation of self-motion by optic flow processing in single visual interneurons.

Humans, animals and some mobile robots use visual motion cues for object detection and navigation in structured surroundings. Motion is commonly sensed by large arrays of small field movement detectors, each preferring motion in a particular direction. Self-motion generates distinct 'optic flow fields' in the eyes that depend on the type and direction of the momentary locomotion (rotation, translation). To investigate how the optic flow is processed at the neuronal level, we recorded intracellularly from identified interneurons in the third visual neuropile of the blowfly. The distribution of local motion tuning over their huge receptive fields was mapped in detail. The global structure of the resulting 'motion response fields' is remarkably similar to optic flow fields. Thus, the organization of the receptive fields of the so-called VS neurons strongly suggests that each of these neurons specifically extracts the rotatory component of the optic flow around a particular horizontal axis. Other neurons are probably adapted to extract translatory flow components. This study shows how complex visual discrimination can be achieved by task-oriented preprocessing in single neurons.