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.

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.

Tri-axial, real-time logging of fly head movements.

We present a method to record and simultaneously display the three rotatory components of arbitrary head turns of an insect flying stationarily in a wind tunnel or walking on a treadmill. An elongated marker, placed on the fly's forehead, is video-recorded from ahead under deep red stroboscopic illumination, invisible to the insect. A fast on-board image processor of a PC video-adapter (True Vision, AT-Vista), programmed in its native code, extracts position and orientation of the marker in the video-image. The host PC transforms these data into calibrated head angles and displays stimulus and response components after 40 ms processing time at a rate of 50 frames per second. Head turns are measured relative to the fly's trunk even when the fly is rotated around its body axis provided that it is aligned with the video-axis. Technical tests, as well as recordings from live flies responding to various stimuli, illustrate the performance and accuracy of the procedure. This minimally invasive method of motion recording should be easily adaptable to other insects and to similar movements of small parts.

Independent spatial waves of biochemical differentiation along the surface of chicken brain as revealed by the sequential expression of acetylcholinesterase.

AChE-positive cells suddenly amass in a superficial layer of the neuroepithelium; this layer finally covers, in a sheat-like manner, the entire surface of the embryonic chicken brain. This feature is functionally not understood; however, it appears shortly after the neurons become postmitotic, and the lateral extensions of this layer can easily be traced using histochemistry on serial brain sections. The layer can therefore be exploited to delineate spatially the waves of onset of biochemical tissue differentiation. We have studied whole brains between stages 11 and 30 and provide the first complete spatial schemes of brain differentiation based on computer-reconstructed, two- and three-dimensional maps. The brain does not differentiate in one smooth coherent wave, but instead five separate primary AChE-activation zones are detected: the first originating at stage 11 ("rhombencephalic wave"), the second at the same time ("midbrain wave"), the third at stage 15 ("tectal wave"). A fourth zone develops later, at stage 18, from the bottom part of the telencephalon to the top. Retinal development also starts at stage 18. In a given area, it appears that AChE-development shortly precedes that of the formation of major fiber tracts. AChE might therefore represent a prerequisite for fiber growth and pathfinding.

A piezoelectric device to aid penetration of small nerve fibers with microelectrodes.

A small piezoelectric device for cell penetration is described. It retracts the micropipette slowly by electrostriction, and pushes it very fast (less than 5 microsecond) forward by short-circuiting the transducer. The design, operation circuit, and performance under test conditions are described. Penetration examples from small nerve fibers (less than 5 micrometer) show that membrane puncture occurs only with the fast forward push. Cells are not noticeably damaged, even if the device is repeatedly operated after cell penetration.

2-Deoxy-D-glucose maps movement-specific nervous activity in the second visual ganglion of Drosophila.

Adult Drosophila were fed with tritium labeled deoxyglucose prior to a 5-hour period of visual stimulation. A flickering disk of light and a moving grating were presented to the left and right eyes, respectively. Autoradiography revealed enhanced labeling solely in that part of the second optic ganglion (medulla) whose visual field was stimulated by movement.