Krapp, Holger G., Bärbel Hengstenberg, and Roland Hengstenberg. Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J. Neurophysiol. 79: 1902–1917, 1998. 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-μm 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.

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.

Krapp, Holger G., Roland Hengstenberg, and Martin Egelhaaf. Binocular contributions to optic flow processing in the fly visual system. J Neurophysiol 85: 724 -734, 2001. 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.