Visuomotor transformation in the fly gaze stabilization system

For sensory signals to control an animal's behavior, they must first be transformed into a format appropriate for use by its motor systems. This fundamental problem is faced by all animals, including humans. Beyond simple reflexes, little is known about how such sensorimotor transformations take place. Here we describe how the outputs of a well-characterized population of fly visual interneurons, lobula plate tangential cells (LPTCs), are used by the animal's gaze-stabilizing neck motor system. The LPTCs respond to visual input arising from both self-rotations and translations of the fly. The neck motor system however is involved in gaze stabilization and thus mainly controls compensatory head rotations. We investigated how the neck motor system is able to selectively extract rotation information from the mixed responses of the LPTCs. We recorded extracellularly from fly neck motor neurons (NMNs) and mapped the directional preferences across their extended visual receptive fields. Our results suggest that-like the tangential cells-NMNs are tuned to panoramic retinal image shifts, or optic flow fields, which occur when the fly rotates about particular body axes. In many cases, tangential cells and motor neurons appear to be tuned to similar axes of rotation, resulting in a correlation between the coordinate systems the two neural populations employ. However, in contrast to the primarily monocular receptive fields of the tangential cells, most NMNs are sensitive to visual motion presented to either eye. This results in the NMNs being more selective for rotation than the LPTCs. Thus, the neck motor system increases its rotation selectivity by a comparatively simple mechanism: the integration of binocular visual motion information.     

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.     

Localized direction selective responses in the dendrites of visual interneurons of the fly

Background  

The various tasks of visual systems, including course control, collision avoidance and the detection of small objects, require at the neuronal level the dendritic integration and subsequent processing of many spatially distributed visual motion inputs. While much is known about the pooled output in these systems, as in the medial superior temporal cortex of monkeys or in the lobula plate of the insect visual system, the motion tuning of the elements that provide the input has yet received little attention. In order to visualize the motion tuning of these inputs we examined the dendritic activation patterns of neurons that are selective for the characteristic patterns of wide-field motion, the lobula-plate tangential cells (LPTCs) of the blowfly. These neurons are known to sample direction-selective motion information from large parts of the visual field and combine these signals into axonal and dendro-dendritic outputs.     

The optic lobe of Drosophila melanogaster

Summary We present a quantitative evaluation of Golgiimpregnated columnar neurons in the optic lobe of wildtype Drosophila melanogaster. This analysis reveals the overall connectivity pattern between the 10 neuropil layers of the medulla and demonstrates the existence of at least three major visual pathways. Pathway 1 connects medulla layer M10 to the lobula plate. Input layers of this pathway are M1 and M5. Pathway 2 connects M9 to shallow layers of the lobula, which in turn are tightly linked to the lobula plate. This pathway gets major input via M2. Pathways 1 and 2 receive input from retinula cells R1-6, either via the lamina monopolar cell L1 (terminating in M1 and M5) or via L2 and T1 (terminating in M2). Neurons of these pathways typically have small dendritic fields. We discuss evidence that pathways 1 and 2 may play a major role in motion detection. Pathway 3 connects M8 to deep layers of the lobula. In M8 information converges that is derived either from M3 (pathway 3a) or from M4 and M6 (pathway 3b), layers that get their major input from L3 and R8 or L4 and R7, respectively. Some neurons of pathway 3 have large dendritic fields. We suggest that they may be involved in the computation of form and colour. Possible analogies to the organization of pathways in the visual system of vertebrates are discussed.During the final editing of this work our friend A.P.M. Dittrich was tragically killed in an accident. Without him this and the previous work would never have been completed     

Spatio-Temporal Dynamics of Impulse Responses to Figure Motion in Optic Flow Neurons

White noise techniques have been used widely to investigate sensory systems in both vertebrates and invertebrates. White noise stimuli are powerful in their ability to rapidly generate data that help the experimenter decipher the spatio-temporal dynamics of neural and behavioral responses. One type of white noise stimuli, maximal length shift register sequences (m-sequences), have recently become particularly popular for extracting response kernels in insect motion vision. We here use such m-sequences to extract the impulse responses to figure motion in hoverfly lobula plate tangential cells (LPTCs). Figure motion is behaviorally important and many visually guided animals orient towards salient features in the surround. We show that LPTCs respond robustly to figure motion in the receptive field. The impulse response is scaled down in amplitude when the figure size is reduced, but its time course remains unaltered. However, a low contrast stimulus generates a slower response with a significantly longer time-to-peak and half-width. Impulse responses in females have a slower time-to-peak than males, but are otherwise similar. Finally we show that the shapes of the impulse response to a figure and a widefield stimulus are very similar, suggesting that the figure response could be coded by the same input as the widefield response.     

Candidate glutamatergic neurons in the visual system of Drosophila

The visual system of Drosophila contains approximately 60,000 neurons that are organized in parallel, retinotopically arranged columns. A large number of these neurons have been characterized in great anatomical detail. However, studies providing direct evidence for synaptic signaling and the neurotransmitter used by individual neurons are relatively sparse. Here we present a first layout of neurons in the Drosophila visual system that likely release glutamate as their major neurotransmitter. We identified 33 different types of neurons of the lamina, medulla, lobula and lobula plate. Based on the previous Golgi-staining analysis, the identified neurons are further classified into 16 major subgroups representing lamina monopolar (L), transmedullary (Tm), transmedullary Y (TmY), Y, medulla intrinsic (Mi, Mt, Pm, Dm, Mi Am), bushy T (T), translobula plate (Tlp), lobula intrinsic (Lcn, Lt, Li), lobula plate tangential (LPTCs) and lobula plate intrinsic (LPi) cell types. In addition, we found 11 cell types that were not described by the previous Golgi analysis. This classification of candidate glutamatergic neurons fosters the future neurogenetic dissection of information processing in circuits of the fly visual system.     

Neural correlates of the optomotor response in the fly

Summary Studies of the optomotor response, the tendency to turn in response to a moving pattern, have yielded some understanding of the motion detection capabilities of the fly. We present data from extracellular microelectrode recordings from the optic lobes of the housefly, Musca domestica and the blowflies Eucalliphora lilaea and Calliphora phaenicia. Directionally selective and directionally nonselective motion sensitive units were observed in the region between the medulla and the lobula of all three species. Employing similar stimulus conditions to those used in the optomotor reaction studies, it was found that the response of the directionally selective units exhibited most of the characteristics of the optomotor response torque measurements. It is concluded that these units code the information prerequisite to the optomotor response and hence, that much data processing is achieved in the first few synaptic layers of the insect visual nervous system.     

Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions

We measured the orientation tuning of two neurons of the fly lobula plate (H1 and H2 cells) sensitive to horizontal image motion. Our results show that H1 and H2 cells are sensitive to vertical motion, too. Their response depended on the position of the vertically moving stimuli within their receptive field. Stimulation within the frontal receptive field produced an asymmetric response: upward motion left the H1/H2 spike frequency nearly unaltered while downward motion increased the spike frequency to about 40% of their maximum responses to horizontal motion. In the lateral parts of their receptive fields, no such asymmetry in the responses to vertical image motion was found. Since downward motion is known to be the preferred direction of neurons of the vertical system in the lobula plate, we analyzed possible interactions between vertical system cells and H1 and H2 cells. Depolarizing current injection into the most frontal vertical system cell (VS1) led to an increased spike frequency, hyperpolarizing current injection to a decreased spike frequency in both H1 and H2 cells. Apart from VS1, no other vertical system cell (VS2-8) had any detectable influence on either H1 or H2 cells. The connectivity of VS1 and H1/H2 is also shown to influence the response properties of both centrifugal horizontal cells in the contralateral lobula plate, which are known to be postsynaptic to the H1 and H2 cells. The vCH cell receives additional input from the contralateral VS2-3 cells via the spiking interneuron V1.     

On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly

A new class of large-field tangential neurones (Figure Detection (FD-) cells) has been found and analysed in the lobula plate, the posterior part of the third visual ganglion, of the fly by combined extra-and intracellular recording as well as Lucifer Yellow injection. The FD-cells are likely to play a prominent role in figure-ground discrimination. Together with the Horizontal Cells, the output elements of the neuronal network underlying the optomotor course control reaction, they seem to be appropriate to account for the characteristic yaw torque response to relative motion. The FD-cells might thus compensate for the deficits of the Horizontal Cells with respect to figureground discrimination (see Egelhaaf, 1985a).The FD-cells are directionally selective for either front-to-back (FD 1, FD 4) or back-to-front motion (FD 2, FD 3). Their excitatory receptive fields cover part of (FD 1, FD 2, FD 3) or the entire horizontal extent (FD 4) of the visual field of one eye. Their most important common property in the context of figureground discrimination is that they are more sensitive to relatively small objects than to spatially extended patterns. Their response to a small figure is much reduced by simultaneous large-field motion in front of the ipsi-as well as the contralateral eye. This large-field inhibition is either directionally selective or bidirectional, depending on the FD-cell under consideration. The main dendritic arborization of all FD-cells resides in the lobula plate. Their axonal projections lie in either the ipsi-or contralateral posterior optic foci and, thus, in the same area as the terminals of the Horizontal Cells. The FD-cells are, therefore, appropriate candidates for output elements of the optic lobes involved in figure-ground discrimination.     

Optic flow representation in the optic lobes of Diptera: modeling the role of T5 directional tuning properties

An evolutionarily conserved system of small retinotopic neurons in dipteran insects, called bushy T-cells, provides information about directional motion to large collator neurons in the lobula plate. Physiological and anatomical features of these cells provide the basis for a model that is used to investigate requirements for generating optic flow selectivity in collators while allowing for evolutionary variations. This account focuses on the role of physiological tuning properties of T5 neurons. Various flow fields are defined as inputs to retinotopic arrays of T5 cells, the responses of which are mapped onto collators using innervation matrices that promote selectivity for flow type and position. Properties known or inferred from physiological and anatomical studies of neurons contributing to motion detection are incorporated into the model: broad tuning to local motion direction and the representation of each visual sampling unit by a quartet of small-field T5-like neurons with orthogonal preferred directions. The model predicts hitherto untested response properties of optic flow selective collators, and predicts that selectivity for a given flow field can be highly sensitive to perturbations in physiological properties of the motion detectors.     

Neural action fields for optic flow based navigation: a simulation study of the fly lobula plate network

Optic flow based navigation is a fundamental way of visual course control described in many different species including man. In the fly, an essential part of optic flow analysis is performed in the lobula plate, a retinotopic map of motion in the environment. There, the so-called lobula plate tangential cells possess large receptive fields with different preferred directions in different parts of the visual field. Previous studies demonstrated an extensive connectivity between different tangential cells, providing, in principle, the structural basis for their large and complex receptive fields. We present a network simulation of the tangential cells, comprising most of the neurons studied so far (22 on each hemisphere) with all the known connectivity between them. On their dendrite, model neurons receive input from a retinotopic array of Reichardt-type motion detectors. Model neurons exhibit receptive fields much like their natural counterparts, demonstrating that the connectivity between the lobula plate tangential cells indeed can account for their complex receptive field structure. We describe the tuning of a model neuron to particular types of ego-motion (rotation as well as translation around/along a given body axis) by its 'action field'. As we show for model neurons of the vertical system (VS-cells), each of them displays a different type of action field, i.e., responds maximally when the fly is rotating around a particular body axis. However, the tuning width of the rotational action fields is relatively broad, comparable to the one with dendritic input only. The additional intra-lobula-plate connectivity mainly reduces their translational action field amplitude, i.e., their sensitivity to translational movements along any body axis of the fly.     

Directionally selective cells in the locust medulla

Summary Intracellular recordings of a distinctive class of directionally selective cell from the medulla of the locust,Locusta migratoria, optic lobe are described. Dye marking shows that these cells arborize in the distal part of the medulla, and project through the lobula complex. The cells are excited by upward movement and have receptive fields of about 20° in diameter. They are sensitive to a wide range of angular velocities from 0.02°/s to over 200°/s. The cells are sensitive to stationary flicker and have different latencies to dimming and brightening. Evidence is presented which suggests that directional computation depends, at least in part, on an inhibitory interaction between flicker sensitive channels.     

Retinotopic organization of small-field-target-detecting neurons in the insect visual system

BACKGROUND: Despite having tiny brains and relatively low-resolution compound eyes, many fly species frequently engage in precisely controlled aerobatic pursuits of conspecifics. Recent investigations into high-order processing in the fly visual system have revealed a class of neurons, coined small-target-motion detectors (STMDs), capable of responding robustly to target motion against the motion of background clutter. Despite limited spatial acuity in the insect eye, these neurons display exquisite sensitivity to small targets. RESULTS: We recorded intracellularly from morphologically identified columnar neurons in the lobula complex of the hoverfly Eristalis tenax. We show that these columnar neurons with exquisitely small receptive fields, like their large-field counterparts recently described from both male and female flies, have an extreme selectivity for the motion of small targets. In doing so, we provide the first physiological characterization of small-field neurons in female flies. These retinotopically organized columnar neurons include both direction-selective and nondirection-selective classes covering a large area of visual space. CONCLUSIONS: The retinotopic arrangement of lobula columnar neurons sensitive to the motion of small targets makes a strong case for these neurons as important precursors in the local processing of target motion. Furthermore, the continued response of STMDs with such small receptive fields to the motion of small targets in the presence of moving background clutter places further constraints on the potential mechanisms underlying their small-target tuning.     

Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons

How is binocular motion information integrated in the bilateral network of wide-field motion-sensitive neurons, called lobula plate tangential cells (LPTCs), in the visual system of flies? It is possible to construct an accurate model of this network because a complete picture of synaptic interactions has been experimentally identified. We investigated the cooperative behavior of the network of horizontal LPTCs underlying the integration of binocular motion information and the information representation in the bilateral LPTC network through numerical simulations on the network model. First, we qualitatively reproduced rotational motion-sensitive response of the H2 cell previously reported in vivo experiments and ascertained that it could be accounted for by the cooperative behavior of the bilateral network mainly via interhemispheric electrical coupling. We demonstrated that the response properties of single H1 and Hu cells, unlike H2 cells, are not influenced by motion stimuli in the contralateral visual hemi-field, but that the correlations between these cell activities are enhanced by the rotational motion stimulus. We next examined the whole population activity by performing principal component analysis (PCA) on the population activities of simulated LPTCs. We showed that the two orthogonal patterns of correlated population activities given by the first two principal components represent the rotational and translational motions, respectively, and similar to the H2 cell, rotational motion produces a stronger response in the network than does translational motion. Furthermore, we found that these population-coding properties are strongly influenced by the interhemispheric electrical coupling. Finally, to test the generality of our conclusions, we used a more simplified model and verified that the numerical results are not specific to the network model we constructed.     

The three-dimensional optomotor torque system ofDrosophila melanogaster

Summary The well known optomotor yaw torque response in flies is part of a 3-dimensional system. Optomotor responses around the longitudinal and transversal body axes (roll and pitch) with strinkingly similar properties to the optomotor yaw response are described here forDrosophila melanogaster. Stimulated by visual motion from a striped drum rotating around an axis aligned with the measuring axis, a fly responds with torque of the same polarity as that of the rotation of the pattern. In this stimulus situation the optomotor responses for yaw, pitch and roll torque have about the same amplitudes and dynamic properties (Fig. 2). Pronounced negative responses are measured with periodic gratings of low pattern wavelengths due to geometrical interference (Fig. 3). The responses depend upon the contrast frequency rather than the angular velocity of the pattern (Fig. 4). Like the optomotor yaw response, roll and pitch responses can be elicited by small field motion in most parts of the visual field; only for motion below and behind the fly roll and pitch responses have low sensitivity.The mutantoptomotor-blind ^H31 (omb ^H31) in which the giant neurones of the lobula plate are missing or severely reduced, is impaired in all 3 optomotor torque responses (Fig. 5) whereas other visual responses like the optomotor lift/thrust response and the landing response (elicited by horizontal front-to-back motion) are not affected (Heisenberg et al. 1978).We propose that the lobula plate giant neurons mediate optomotor torque responses and that the VS-cells in particular are involved in roll and pitch but not in lift/thrust control. This hypothesis accommodates various electrophysiological and anatomical observations about these neurons in large flies.Abbreviation EMD elementary movement detector     

Vertical motion detectors and their synaptic relations in the third optic lobe of the fly

The synaptic relations of the giant vertical cells in the lobula plate of the fly were investigated using electron microscopical procedures and Lucifer yellow dye backfill and injection techniques. Histological features of the giant vertical cells are described. The giant vertical cells are exclusively postsynaptic in the lobula plate. They function to integrate input from dense arrays of chemical synapses and have a wide spatial input from the lobula plate. The giant vertical cells are postsynaptic to perpendicularly occurring cells. There are two classes of cells presynaptic to the vertical cells, one of which contains large dense-core vesicles. The giant vertical cells are not the only cells postsynaptic to these two classes of perpendicualr cells. A second group of smaller tangential cells, the twin vertical cells, were also found postsynaptic to many of the same cells that synapsed with the giant vertical cells. The twin vertical cells and the giant vertical cells are therefore integrating some of the same information in the lobula plate.     

Optic lobe projections of marginal ommatidia in Calliphora erythrocephala specialized for detecting polarized light

Summary The structure of ommatidia at the dorsal eye margin of the fly, Calliphora erythrocephala is specialized for the detection of the e-vector of polarized light. Marginal zone ommatidia are distinguished by R7/R8 receptor cells with large-diameter, short, untwisted rhabdomeres and long axons to the medulla. The arrangement of the R7 microvillar directions along the marginal zone is fan-shaped. Ommatidia lining the dorsal and frontal edge of the eye lack primary screening pigments and have foreshortened crystalline cones. The marginal ommatidia from each eye view a strip that is 5 °–20 ° contralateral to the fly's longitudinal axis and that coincides with the outer boundaries of the binocular overlap.Cobalt injection into the retina demonstrates that photoreceptor axons arising from marginal ommatidia define a special area of marginal neuropil in the second visual neuropil, the medulla. Small-field neurons arising from the marginal medulla area define, in turn, a special area of marginal neuropil in the two deepest visual neuropils, the lobula and the lobula plate. From these arise local assemblies of columnar neurons that relay the marginal zones of one optic lobe to equivalent areas of the opposite lobe and to midbrain regions from which arise descending neurons destined for the the thoracic ganglia.Optically, the marginal zone of the retina represents the lateral edge of a larger area of ommatidia involved in dorsofrontal binocular overlap. This binocularity area is also represented by special arrangements of columnar neurons, which map the binocularity area of one eye into the lobula beneath the opposite eye. Another type of binocularity neuron terminates in the midbrain.These neuronal arrangements suggest two novel features of the insect optic lobes and brain: (1) Marginal neurons that directly connect the left and right optic lobes imply that each lobe receives a common input from areas of the left and right eye, specialized for detecting the pattern of polarized light. (2) Information about the e-vector pattern of sky-light polarization may be integrated with binocular and monocular pathways at the level of descending neurons leading to thoracic motor neuropil.     

Optic flow representation in the optic lobes of Diptera: modeling innervation matrices onto collators and their evolutionary implications

A network model of optic flow processing, based on physiological and anatomical features of motion-processing neurons, is used to investigate the role of small-field motion detectors emulating T5 cells in producing optic flow selective properties in wide-field collator neurons. The imposition of different connectivities can mimic variations observed in comparative studies of lobula plate architecture across the Diptera. The results identify two features that are crucial for optic flow selectivity: the broadness of the spatial patterns of synaptic connections from motion detectors to collators, and the relative contributions of excitatory and inhibitory synaptic outputs. If these two aspects of the innervation matrix are balanced appropriately, the network's sensitivity to perturbations in physiological properties of the small-field motion detectors is dramatically reduced, suggesting that sensory systems can evolve robust mechanisms that do not rely upon precise control of network parameters. These results also suggest that alternative lobula plate architectures observed in insects are consistent in allowing optic flow selective properties in wide-field neurons. The implications for the evolution of optic flow selective neurons are discussed.     

A synergetic theory of environmentally-specified and learned patterns of movement coordination

By combining neuropharmacology and electrophysiology, we tried to determine whether the main neuronal mechanism responsible for direction-selective motion detection in the fly is based on an excitatory or an inhibitory synaptic interaction. By blocking inhibitory interactions with picrotoxinin, an antagonist of the inhibitory neurotransmitter GABA, we could abolish most of the directional selectivity of a large-field movement-sensitive neuron (H1-cell) in the lobula plate of the blowfly Calliphora erythrocephala. These modifications are similar to changes observed in the optomotor response of the fruitfly Drosophila melanogaster after application of picrotoxinin (Bülthoff and Bülthoff 1987a, b). Assuming a simplified logical model, these results are compatible with inhibitory synaptic interactions at the level of the elementary movement detectors. The picrotoxinin-induced changes in direction selectivity are not due to modifications of the peripheral visual processing in the retina and lamina. This was shown by simultaneous recordings of the electroretinogram and the H1-cell. The latencies between drug injections into various parts of the brain and their first effects on the H1-cell suggest that the inhibitory mechanism for motion detection is located in the medulla rather than in the lobula plate.