Vertical System Cells Research Articles

Non-uniform weighting of local motion inputs underlies dendritic computation in the fly visual system

The fly visual system offers a unique opportunity to explore computations performed by single neurons. Two previous studies characterized, in vivo, the receptive field (RF) of the vertical system (VS) cells of the blowfly (calliphora vicina), both intracellularly in the axon, and, independently using Ca2+ imaging, in hundreds of distal dendritic branchlets. We integrated this information into detailed passive cable and compartmental models of 3D reconstructed VS cells. Within a given VS cell type, the transfer resistance (TR) from different branchlets to the axon differs substantially, suggesting that they contribute unequally to the shaping of the axonal RF. Weighting the local RFs of all dendritic branchlets by their respective TR yielded a faithful reproduction of the axonal RF. The model also predicted that the various dendritic branchlets are electrically decoupled from each other, thus acting as independent local functional subunits. The study suggests that single neurons in the fly visual system filter dendritic noise and compute the weighted average of their inputs.

Efficient encoding of motion is mediated by gap junctions in the fly visual system.

Understanding the computational implications of specific synaptic connectivity patterns is a fundamental goal in neuroscience. In particular, the computational role of ubiquitous electrical synapses operating via gap junctions remains elusive. In the fly visual system, the cells in the vertical-system network, which play a key role in visual processing, primarily connect to each other via axonal gap junctions. This network therefore provides a unique opportunity to explore the functional role of gap junctions in sensory information processing. Our information theoretical analysis of a realistic VS network model shows that within 10 ms following the onset of the visual input, the presence of axonal gap junctions enables the VS system to efficiently encode the axis of rotation, θ, of the fly’s ego motion. This encoding efficiency, measured in bits, is near-optimal with respect to the physical limits of performance determined by the statistical structure of the visual input itself. The VS network is known to be connected to downstream pathways via a subset of triplets of the vertical system cells; we found that because of the axonal gap junctions, the efficiency of this subpopulation in encoding θ is superior to that of the whole vertical system network and is robust to a wide range of signal to noise ratios. We further demonstrate that this efficient encoding of motion by this subpopulation is necessary for the fly's visually guided behavior, such as banked turns in evasive maneuvers. Because gap junctions are formed among the axons of the vertical system cells, they only impact the system’s readout, while maintaining the dendritic input intact, suggesting that the computational principles implemented by neural circuitries may be much richer than previously appreciated based on point neuron models. Our study provides new insights as to how specific network connectivity leads to efficient encoding of sensory stimuli.

Near-optimal decoding of transient stimuli from coupled neuronal subpopulations.

Coupling between sensory neurons impacts their tuning properties and correlations in their responses. How such coupling affects sensory representations and ultimately behavior remains unclear. We investigated the role of neuronal coupling during visual processing using a realistic biophysical model of the vertical system (VS) cell network in the blow fly. These neurons are thought to encode the horizontal rotation axis during rapid free-flight maneuvers. Experimental findings suggest that neurons of the VS are strongly electrically coupled, and that several downstream neurons driving motor responses to ego-rotation receive inputs primarily from a small subset of VS cells. These downstream neurons must decode information about the axis of rotation from a partial readout of the VS population response. To investigate the role of coupling, we simulated the VS response to a variety of rotating visual scenes and computed optimal Bayesian estimates from the relevant subset of VS cells. Our analysis shows that coupling leads to near-optimal estimates from a subpopulation readout. In contrast, coupling between VS cells has no impact on the quality of encoding in the response of the full population. We conclude that coupling at one level of the fly visual system allows for near-optimal decoding from partial information at the subsequent, premotor level. Thus, electrical coupling may provide a general mechanism to achieve near-optimal information transfer from neuronal subpopulations across organisms and modalities.

Optomotor-blind in the Development of the Drosophila HS and VS Lobula Plate Tangential Cells

The horizontal system and vertical system cells of the dipteran optic lobes are well understood regarding their physiology and role in visually guided behavior. Little is known, however, about their development. Drosophila optomotor-blind (omb) is required for the development of the HS/VS cells which are lacking in the adult brain of the In(1)omb[H31] regulatory mutant. We have analyzed the omb regulatory region, required for HS/VS development, for enhancers active in the central nervous system. A 1-kb fragment, ombJb, was identified 114 kb downstream of the omb transcription start site, that could drive expression in much of the presumptive embryonic optic lobe anlage. Expression in these cells is lost in In(1)omb[H31] suggesting that they contain the HS/VS precursor cell(s). We used Laser ablation in the embryonic CNS in order to localize the position of the HS/VS precursor cell(s) in this tissue. An omb-Gal4 enhancer trap line, which showed activity in the optic lobe anlage in a pattern similar to ombJb enhancer, was used to drive GFP expression, thus allowing to focus the Laser beam to the relevant area. We identified a small region in the embryonic brain from which the HS/VS cells are likely to develop. Omb encodes a transcription factor of the T-box family. Since loss of omb disrupts HS/VS cell development, we assume that HS/VS ontogeny is controlled by Omb target genes. As a first step toward their identification, we characterized the Omb DNA-binding specificity.

Subcellular mapping of dendritic activity in optic flow processing neurons

Dendritic integration is a fundamental element of neuronal information processing. So far, few studies have provided a detailed spatial picture of this process, describing the properties of local dendritic activity and its subcellular organization. Here, we used 2-photon calcium imaging in optic flow processing neurons of the fly Calliphora vicina to determine the preferred location and direction of local motion cues for small branchlets throughout the entire dendrite. We found a pronounced retinotopic mapping on both the subcellular and the cell population level. In addition, dendritic branchlets residing in different layers of the neuropil were tuned to distinct directions of motion. Summing the local receptive fields of all dendritic branchlets reproduced the characteristic properties of these neurons' axonal output receptive fields. Our results corroborate the notion that the dendritic morphology of vertical system cells allows them to selectively collect local motion inputs with particular directional preferences from a spatially organized input repertoire, thus forming filters that match global patterns of optic flow. Furthermore, we suggest that the facet arrangement across the fly's eye shapes the subcellular direction tuning to local motion stimuli. These data illustrate a highly structured circuit organization as an efficient way to hard-wire a complex sensory task.

Integration of binocular optic flow in cervical neck motor neurons of the fly

Global visual motion elicits an optomotor response of the eye that stabilizes the visual input on the retina. Here, we analyzed the neck motor system of the blowfly to understand binocular integration of visual motion information underlying a head optomotor response. We identified and characterized two cervical nerve motor neurons (called CNMN6 and CNMN7) tuned precisely to an optic flow corresponding to pitch movements of the head. By means of double recordings and dye coupling, we determined that these neurons are connected ipsilaterally to two vertical system cells (VS2 and VS3), and contralaterally to one horizontal system cell (HSS). In addition, CNMN7 turned out to be connected to the ipsilateral CNMN6 and to its contralateral counterpart. To analyze a potential function of this circuit, we performed behavioral experiments and found that the optomotor pitch response of the fly head was only observable when both eyes were intact. Thus, this neural circuit performs two visuomotor transformations: first, by integrating binocular visual information it enhances the tuning to the optic flow resulting from pitch movements of the head, and second it could assure an even head declination by coordinating the activity of the CNMN7 neurons on both sides.

Robust Coding of Ego-Motion in Descending Neurons of the Fly

In many species, motion-sensitive neurons responding to optic flow at higher processing stages are well characterized; however, less is known how this representation of ego-motion is further transformed into an appropriate motor response. Here, we analyzed in the blowfly Calliphora vicina the visuomotor transformation from motion-sensitive neurons in the lobula plate [V2 and vertical system (VS) cells] onto premotor descending neurons [descending neurons of the ocellar and vertical system (DNOVS) cells] feeding into the motor circuit of the fly thoracic ganglion. We found that each of these cells is tuned to rotation of the fly around a particular body axis. Comparing the responses of presynaptic and postsynaptic cells revealed that DNOVS cells have approximately the same tuning widths as V2 and VS cells. However, DNOVS signals cells are less corrupted by fluctuations arising from the spatial structure of the visual input than their presynaptic elements. This leads to a more robust representation of ego-motion at the level of descending neurons. Thus, when moving from lobula plate cells to descending neurons, the selectivity for a particular optic flow remains unaltered, but the robustness of the representation increases.

Response Properties of Motion-Sensitive Visual Interneurons in the Lobula Plate of Drosophila melanogaster

The crystalline-like structure of the optic lobes of the fruit fly Drosophila melanogaster has made them a model system for the study of neuronal cell-fate determination, axonal path finding, and target selection. For functional studies, however, the small size of the constituting visual interneurons has so far presented a formidable barrier. We have overcome this problem by establishing in vivo whole-cell recordings from genetically targeted visual interneurons of Drosophila. Here, we describe the response properties of six motion-sensitive large-field neurons in the lobula plate that form a network consisting of individually identifiable, directionally selective cells most sensitive to vertical image motion (VS cells). Individual VS cell responses to visual motion stimuli exhibit all the characteristics that are indicative of presynaptic input from elementary motion detectors of the correlation type. Different VS cells possess distinct receptive fields that are arranged sequentially along the eye's azimuth, corresponding to their characteristic cellular morphology and position within the retinotopically organized lobula plate. In addition, lateral connections between individual VS cells cause strongly overlapping receptive fields that are wider than expected from their dendritic input. Our results suggest that motion vision in different dipteran fly species is accomplished in similar circuitries and according to common algorithmic rules. The underlying neural mechanisms of population coding within the VS cell network and of elementary motion detection, respectively, can now be analyzed by the combination of electrophysiology and genetic intervention in Drosophila.

Eigenanalysis of a neural network for optic flow processing

Flies gain information about self-motion during free flight by processing images of the environment moving across their retina. The visual course control center in the brain of the blowfly contains, among others, a population of ten neurons, the so-called vertical system (VS) cells that are mainly sensitive to downward motion. VS cells are assumed to encode information about rotational optic flow induced by self-motion (Krapp and Hengstenberg 1996 Nature 384 463–6). Recent evidence supports a connectivity scheme between the VS cells where neurons with neighboring receptive fields are connected to each other by electrical synapses at the axonal terminals, whereas the boundary neurons in the network are reciprocally coupled via inhibitory synapses (Haag and Borst 2004 Nat. Neurosci. 7 628–34; Farrow et al 2005 J. Neurosci. 25 3985–93; Cuntz et al 2007 Proc. Natl Acad. Sci. USA). Here, we investigate the functional properties of the VS network and its connectivity scheme by reducing a biophysically realistic network to a simplified model, where each cell is represented by a dendritic and axonal compartment only. Eigenanalysis of this model reveals that the whole population of VS cells projects the synaptic input provided from local motion detectors on to its behaviorally relevant components. The two major eigenvectors consist of a horizontal and a slanted line representing the distribution of vertical motion components across the fly's azimuth. They are, thus, ideally suited for reliably encoding translational and rotational whole-field optic flow induced by respective flight maneuvers. The dimensionality reduction compensates for the contrast and texture dependence of the local motion detectors of the correlation-type, which becomes particularly pronounced when confronted with natural images and their highly inhomogeneous contrast distribution.

Reciprocal inhibitory connections within a neural network for rotational optic-flow processing

Neurons in the visual system of the blowfly have large receptive fields that are selective for specific optic flow fields. Here, we studied the neural mechanisms underlying flow–field selectivity in proximal Vertical System (VS)-cells, a particular subset of tangential cells in the fly. These cells have local preferred directions that are distributed such as to match the flow field occurring during a rotation of the fly. However, the neural circuitry leading to this selectivity is not fully understood. Through dual intracellular recordings from proximal VS cells and other tangential cells, we characterized the specific wiring between VS cells themselves and between proximal VS cells and horizontal sensitive tangential cells. We discovered a spiking neuron (Vi) involved in this circuitry that has not been described before. This neuron turned out to be connected to proximal VS cells via gap junctions and, in addition, it was found to be inhibitory onto VS1.

Robust coding of flow-field parameters by axo-axonal gap junctions between fly visual interneurons

Complex flight maneuvers require a sophisticated system to exploit the optic flow resulting from moving images of the environment projected onto the retina. In the fly's visual course control center, the lobula plate, 10 so-called vertical system (VS) cells are thought to match, with their complex receptive fields, the optic flow resulting from rotation around different body axes. However, signals of single VS cells are unreliable indicators of such optic flow parameters in the context of their noisy, texture-dependent input from local motion measurements. Here we propose an alternative encoding scheme based on network simulations of biophysically realistic compartmental models of VS cells. The simulations incorporate recent data about the highly selective connectivity between VS cells consisting of an electrical axo-axonal coupling between adjacent cells and a reciprocal inhibition between the most distant cells. We find that this particular wiring performs a linear interpolation between the output signals of VS cells, leading to a robust representation of the axis of rotation even in the presence of textureless patches of the visual surround.

Integration of Lobula Plate Output Signals by DNOVS1, an Identified Premotor Descending Neuron

Many motion-sensitive tangential cells of the lobula plate in blowflies are well described with respect to their visual response properties and the connectivity among them. They have large and complex receptive fields with different preferred directions in different parts of their receptive fields matching the optic flow that occurs during various flight maneuvers. However, much less is known about how tangential cells connect to postsynaptic neurons descending to the motor circuits in the thoracic ganglion and how optic flow is represented in these downstream neurons. Here we describe the physiology and the connectivity of a prominent descending neuron called DNOVS1 (for descending neurons of the ocellar and vertical system). We find that DNOVS1 is electrically coupled to a subset of vertical system cells. The specific wiring leads to a preference of DNOVS1 for rotational flow fields around a particular body axis. In addition, DNOVS1 receives input from interneurons connected to the ocelli.

Sharing Receptive Fields with Your Neighbors: Tuning the Vertical System Cells to Wide Field Motion

In the blowfly, the direction-selective response of the 60 lobula-plate tangential cells has been ascribed to the integration of local motion information across their extensive dendritic trees. Because the lobula plate is organized retinotopically, the receptive fields of the tangential cells ought to be determined by their dendritic architecture. However, this appears not always to be the case. One compelling example is the exceptionally wide receptive fields of the vertical system (VS) tangential cells. Using dual-intracellular recordings, Haag and Borst (2004) found VS cells to be mutually coupled in such a way that each VS cell is connected exclusively to its immediate neighbors. This coupling may form the basis of the broad receptive fields of VS cells. Here, we tested this hypothesis directly by photoablating individual VS cells. The receptive field width of VS cells indeed narrowed after the ablation of single VS cells, specifically depending on whether the receptive field of the ablated cell was more frontal or more posterior to the recorded cell. In particular, the responses changed as if the neuron lost access to visual information from the ablated neuron and those VS cells more distal than it from the recorded neuron. These experiments provide strong evidence that the lateral connections among VS cells are a crucial component in the mechanism underlying their complex receptive fields, augmenting the direct columnar input to their dendrites.

Golgi analysis of tangential neurons in the lobula plate of Drosophila melanogaster.

The lobula plate (LP), which is the third order optic neuropil of flies, houses wide-field neurons which are exquisitely sensitive to motion. Among Diptera, motion-sensitive neurons of larger flies have been studied at the anatomical and physiological levels. However, the neurons of Drosophila lobula plate are relatively less explored. As Drosophila permits a genetic analysis of neural functions, we have analysed the organization of lobula plate of Drosophila melanogaster. Neurons belonging to eight anatomical classes have been observed in the present study. Three neurons of the horizontal system (HS) have been visualized. The HS north (HSN) neuron, occupying the dorsal lobula plate is stunted in its geometry compared to that of larger flies. Associated with the HS neurons, thinner horizontal elements known as h-cells have also been visualized in the present study. Five of the six known neurons of the vertical system (VS) have been visualized. Three additional neurons in the proximal LP comparable in anatomy to VS system have been stained. We have termed them as additional VS (AVS)-like neurons. Three thinner tangential cells that are comparable to VS neurons, which are elements of twin vertical system (tvs); and two cells with wide dendritic fields comparable to CH neurons of Diptera have been also observed. Neurons comparable to VS cells but with 'tufted' dendrites have been stained. The HSN and VS1-VS2 neurons are dorsally stunted. This is possibly due to the shape of the compound eye of Drosophila which is reduced in the fronto-dorsal region as compared to larger flies.

Structure of the vertical and horizontal system neurons of the lobula plate in Drosophila.

The lobula plate in the optic lobe of the fly brain is a high-order processing center for visual information. Within the lobula plate lie a small number of giant neurons that are responsible for the detection of wide field visual motion. Although the structure and motion sensitivity of these cells have been extensively described in large flies, the system has not been described systematically in Drosophila. Here, we use the mosaic analysis with a repressible cell marker (MARCM) system to analyze a subset of these cells, the horizontal and vertical systems. Our results suggest that the Drosophila horizontal system is similar to those described in larger flies, with three neurons fanning their dendrites over the lobula plate. We found that there are six neurons in the Drosophila vertical system, a figure that compares with 9-11 neurons in large flies. Even so, the Drosophila vertical system closely resembles the systems of larger flies, with each neuron in Drosophila having an approximate counterpart in large flies. This anatomical similarity implies that the inputs to the vertical system are similarly organized in these various fly species, and that it is likely that the Drosophila neurons respond to motions similar to those sensed by their specific structural counterparts in large flies. Additionally, the similar appearance of vertical system cells in multiple cell clones demonstrates that they share a common developmental lineage. Access to these cells in Drosophila should allow for the use of genetic tools in future studies of horizontal and vertical system function.

A preparation of the blowfly ( Calliphora erythrocephala) brain for in vitro electrophysiological and pharmacological studies

We describe a method for the preparation and maintenance of the blowfly ( Calliphora erythrocephala) brain in a recording chamber under in vitro conditions in a semi-slice configuration. Large identified neurones in the posterior part of the 3rd optic lobe (lobula plate) can be penetrated easily with microelectrodes. The so-called vertical system (VS) cells which respond to vertical image motion in vivo could be encountered best because their axons are escorted individually by specific tracheae. Fluorescent stained cells show their natural shape as being in vivo. Electrophysiological properties of the cells investigated so far, i.e., resting potential (about −40 mV) and firing properties (single rebound spikes), are comparable to recordings in intact flies. Initial pharmacological experiments on VS cells in this preparation reveal that iontophoretical application of acetylcholine and carbamylcholine results in depolarization. VS cells also respond to bath-applied nicotine (1 μM) with a slow depolarization of their membrane potential in normal fly saline as well as in a Ca 2+-free saline, suggesting direct cholinergic input via nicotinic receptors. The suitability of the preparation for a wide range of electrophysiological and pharmacological studies is discussed.