The synaptic organization of visual interneurons in the lobula complex of flies

Summary The synaptic organization of three classes of cobalt-filled and silver-intensified visual interneurons in the lobula complex of the blowfly Calliphora (Col A cells, horizontal cells and vertical cells) was studied electron microscopically. The Col A cells are regularly spaced, columnar, small field neurons of the lobula, which constitute a plexus of arborizations at the posterior surface of the neuropil and the axons of which terminate in the ventrolateral protocerebrum. They show postsynaptic specializations in the distal layer of their lobula-arborizations and additional presynaptic sites in a more proximal layer; their axon terminals are presynaptic to large descending neurons projecting into the thoracic ganglion. The horizontal and vertical cells are giant tangential neurons, the arborizations of which cover the anterior and posterior surface of the lobula plate, respectively, and which terminate in the perioesophageal region of the protocerebrum. Both classes of these giant neurons were found to be postsynaptic in the lobula plate and pre- and postsynaptic at their axon terminals and axon collaterals. The significance of these findings with respect to the functional properties of the neurons investigated is discussed.     

The centrifugal horizontal cells in the lobula plate of the blowfly, Phaenicia sericata

Intracellular recordings combined with iontophoretic injection of Procion Yellow M4RAN were used to study the anatomy and physiology of the centrifugal horizontal cells (CH-cells) in the lobula plate of the blowfly, Phaenicia sericata.Anatomy: The CH-cells comprise a set of two homolateral, giant visual interneurones (DCH, VCH) at the rostral surface of each lobula plate. Their extensive arborizations in the lobula plate possess bulbous swellings (boutons terminaux). The arborization of one cell (DCH) covers the dorsal, and the arborization of the other cell (VCH) the ventral half of the lobula plate. Their axons run jointly with those of the horizontal cells through the chiasma internum and the optic peduncle. Their protocerebral arborization possesses spines; they form a dense network together with the axonal arborization of the horizontal cells, a second type of giant homolateral cell most sensitive to horizontal motion. The protocerebral arborization of the CH-cells gives rise to a cell body fibre which traverses the protocerebrum dorsally to the oesophageal canal. The cell body lies on the contralateral side laterally and slightly dorsally to the oesophageal canal in the frontal cell body layer.Physiology: The CH-cells respond with graded potentials to rotatory movements of their surround. Cells in the right lobula plate respond with excitation (excitatory postsynaptic potentials, membrane depolarization) to clockwise motion (contralateral regressive, ipsilateral progressive), and with inhibition (inhibitory postsynaptic potentials, membrane hyperpolarization) to counterclockwise motion in either or both receptive fields; CH-cells respond to motion presented to the ipsilateral and/or contralateral eye. Cells of the left lobula plate respond correspondingly to the reverse directions of motion. Vertical pattern motion and stationary patterns are ineffective.The heterolateral H1-neurone elicits excitatory postsynaptic potentials in the DCH-cell; these postsynaptic potentials are tightly correlated 1:1 to the preceding H1-action potentíal. The delay between the peak of the action potential and the beginning of the DCH-postsynaptic potential is 1.15 msec, agreeing very well with the value reported previously for the blowfly, Calliphora (Hausen, 1976a). The synaptic input and output connections of the CH-cells are discussed.     

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.     

Golgi analysis of tangential neurons in the lobula plate of<Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

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 ofDrosophila lobula plate are relatively less explored. AsDrosophila permits a genetic analysis of neural functions, we have analysed the organization of lobula plate ofDrosophila 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 ofDrosophila which is reduced in the fronto-dorsal region as compared to larger flies     

The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica

Summary Three giant horizontal-motion-sensitive (HS) neurons arise in the lobula plate. Their axons terminate ipsilaterally in the medial deutocerebrum and suboesophageal ganglion. Both Golgi impregnations and cobalt fills demonstrate that endings of the two HS cells, representing the upper and middle third of the retina, differ in shape and location from that of the HS cell subtending the lower third of the eye. This dichotomy is reflected by the terminals of a pair of centrifugal horizontal cells (CH), one of which invades lobula plate neuropil subtending the upper two-thirds of the retina. The other overlaps the dendrites of the HS cell subtending the lower one-third of the retina.The HS cells are cobalt-coupled to a variety of complexly arborizing descending neurons. In Musca domestica, gap-junction-like apposition areas have been observed between HS axon collaterals and descending neuron dendrites. The three HS cells also share conventional chemical synapses with postsynaptic elements, which include the dendritic spines of descending neurons. Unlike the giant vertical-motion-sensitive neurons of the lobula plate, whose relationships with descending neurons appear to be relatively simple, the horizontal cells end on a large number of descending neurons where they comprise one of several different populations of terminals. These descending neurons terminate within various centres of the thoracic ganglia, including neuropil supplying leg, neck, and flight muscle.     

Intensity and motion responses of giant vertical neurons of the fly eye

There are nine “giant vertical” neurons in the lobula plate of the fly optic lobe. Intracellular recordings were obtained from the three most peripheral of these cells. These cells respond to a light flash with graded changes in the membrane potential. The response consists of an “on” transient, a sustained depolarization, an increase in membrane potential fluctuations, and an “off” transient. Signal averaging showed that only the “on” and “off” transients are correlated to the stimulus. A pattern of horizontally oriented stripes moving in the vertical direction evokes a response larger than the response to a stationary pattern. The response is most sensitive to vertical movement; motion in the downward direction evokes a net membrane potential depolarization, and upward motion results in a net hyperpolarization. We conclude that the giant vertical cells function primarily as vertical motion detectors and that the direction of the motion is encoded in the polarity of the shift in the membrane potential.     

Columnar cells necessary for motion responses of wide-field visual interneurons in <Emphasis Type="Italic">Drosophila</Emphasis>

Wide-field motion-sensitive neurons in the lobula plate (lobula plate tangential cells, LPTCs) of the fly have been studied for decades. However, it has never been conclusively shown which cells constitute their major presynaptic elements. LPTCs are supposed to be rendered directionally selective by integrating excitatory as well as inhibitory input from many local motion detectors. Based on their stratification in the different layers of the lobula plate, the columnar cells T4 and T5 are likely candidates to provide some of this input. To study their role in motion detection, we performed whole-cell recordings from LPTCs in Drosophila with T4 and T5 cells blocked using two different genetically encoded tools. In these flies, motion responses were abolished, while flicker responses largely remained. We thus demonstrate that T4 and T5 cells indeed represent those columnar cells that provide directionally selective motion information to LPTCs. Contrary to previous assumptions, flicker responses seem to be largely mediated by a third, independent pathway. This work thus represents a further step towards elucidating the complete motion detection circuitry of the fly.     

The vertical-horizontal neurone (VH) in the lobula plate of the blowfly,Phaenicia

Summary The anatomy and physiology of a motion-sensitive neurone, the vertical-horizontal (VH-) cell in the third visual neuropil (lobula plate) of the blowfly,Phaenicia was studied by intracellular recordings combined with dye injection. The cell possesses two dendritic fields in different layers of the lobula plate. The axon runs jointly with those of the vertical cells along the caudal surface of the lobula plate and terminates in the central protocerebrum lateral to the esophageal canal. The receptive field of the VH-cell is subdivided into two physiologically different parts which correspond to the two dendritic fields: if the input reaches the dendritic field residing in a more caudal layer (V-layer), the cell responds maximally to vertical pattern motion; whereas if the input reaches the dendritic field residing in a more rostral layer (H-layer), the cell responds maximally to horizontal pattern motion. The VH-neurone responds maximally to a contrast frequency of approximately / 1.8 Hz which coincides with the contrast frequency dependence of optomotor (following) responses. It is, therefore, considered to be a likely candidate mediating the pitch response (Blondeau and Heisenberg 1982) in flies.     

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.     

The horizontal cells in the lobula plate of the blowfly,Phaenicia sericata

SummarySummary Combining intracellular recording and dye injection techniques, the horizontal cells of the blowfly,Phaenicia (= Lucilia) sericata, were studied.Anatomy In each lobula plate, one finds a set of three cells, termed NH-, EH- and SH-cell. EH occurs in two distinct anatomical forms, EH1 and EH2, differing in their respective branching patterns of the axon at the frontal surface of the lobula plate. Each cell's dendrite covers approximately a third of the surface of the lobula plate corresponding to a third of the visual field of the ipsilateral eye. These dendrites possess postsynaptic spines. The axons of all three cells pass along the frontal surface of the lobula plate within the inner chiasma; they cross the optic peduncle and enter the central protocerebrum where they form a second arborization, the axonal arborization consisting of dorsally extending collaterals. The axons terminate in the posterior slope of the ventrolateral protocerebrum. The axonal arborization as well as the axonal terminals possess telodendritic knobs. Ultrastructural investigations show that the lobula plate-dendrite possesses exclusively postsynaptic chemical synapses, and that the axonal arborisation and the axonal terminals possess pre- as well as postsynaptic chemical synapses. The very endings of the axons are exclusively presynaptic.Physiology The horizontal cells respond to stimulation within the ipsi- and/or contralateral receptive field. Regressive motion within the contralateral receptive field induces EPSPs and action potentials of small amplitude (10–35 mV); progressive motion is ineffective. Within the ipsilateral receptive field, regressive motion hyperpolarizes the cell membrane whereas progressive motion induces a strong depolarizing membrane potential-shift with superimposed fast potential changes of noisy appearance. Thus, the horizontal cells respond to rotational movement of the surround around the high axis of the animal: clockwise rotation excites the horizontal cells of the right lobula plate and counterclockwise motion those of the left lobula plate, respectively. However, this compound potential behaviour can only be recorded in the lobula plate-axon and main dendrites, whereas the horizontal cells respond tocontralateral regressive motion with action potentialsonly in their axonal terminals in the posterior slope; no graded potentials can be recorded in this cell region if stimulation occurs within theipsilateral receptive field. It is discussed that the previously described graded potentials for the axonal terminals (Hausen 1976b) can only be measured if the cells are already damaged. The probable cause of this change in response behaviour from action potentials to a compound potential behaviour (consisting of graded potentials and action potentials though of small amplitude) is discussed.This research was supported by the Deutsche Forschungsgemeinschaft through grants Ec56/1a + b and a Heisenberg stipend EC 56/3, funds from the SFB 114, and a grant from the National Science Foundation (NSF BMS 74-21712) awarded to the author and L.G. Bishop. I am indebted to Dr. A. Whittle and particularly to Prof. K. Meller for their invaluable help in ultrathin sectioning and to Mrs. B. Decker who introduced me to the technique of cutting serial semithin sections. Prof. K. Hamdorf helped with many stimulating discussions. I am most grateful to Dr. W. Broughton for kindly correcting the English style.     

Deoxyglucose mapping of nervous activity induced inDrosophila brain by visual movement

Summary The pattern of visually induced local metabolic activity in the optic lobes of two structural mutants ofDrosophila melanogaster is compared with the corresponding wildtype pattern which has been reported in Part I of this work (Buchner et al. 1984b). Individualoptomotor-blind ^H31 (omb) flies lacking normal giant HS-neurons were tested behaviourally, and those with strongly reduced responses to visual movement were processed for 3H-deoxyglucose autoradiography. The distribution of metabolic activity in the optic lobes ofomb apparently does not differ substantially from that found in wildtype. In the mutantlobula plate-less ^N684 (lop) the small rudiment of the lobula plate which lacks many small-field input neurons does not show any stimulus-specific labelling. The data provide further support for the hypothesis that small-field input neurons to the lobula plate are the cellular substrate of the direction-specific labelling inDrosophila (see Buchner et al. 1984b).Abbreviations DG deoxyglucose - omb optomotor blind^H31 - lop lobula plate-less^N684 - WT wildtype     

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.     

Visual system of the stalk-eyed fly,Cyrtodiopsis quinqueguttata (Diopsidae,Diptera): an anatomical investigation of unusual eyes

Diopsid flies have eye stalks up to a centimeter in length, displacing the retina laterally from the rest of the head. This bizarre condition, called hypercephaly, is rare, but has evolved independently among several insect orders and is most common in flies (Diptera). Earlier studies of geometrical optics and behavior have led to various hypotheses about possible adaptive advantages of eye stalks, such as enhanced stereoscopic vision while other hypothesis suggest that eye stalks are an outcome of sexual selection. Here, we focus on how these curious distortions of head/eye morphology are accompanied by changes in the neural organization of the visual system of Cyrtodiopsis quinqueguttata. Histological examinations reveal that the optic lobes, lamina (La), medulla (Me), lobula (Lo), and lobula plate (LP) are contained entirely within the fly's eye bulbs, which are located at the distal ends of the eye stalks. We report that the organization of the peripheral visual system (La and Me) is similar to that of other Diptera (e.g., Musca and Drosophila), but deeper visual areas (Lo and LP) have been more strongly modified. For example, in both the lobula and lobula plate, fewer but larger giant collector neurons are found. The most pronounced difference is the reduction in the number of wide-field vertical cells of the lobula plate, where there are only four relatively large fibers, as opposed to 11 in Musca. The “fewer but larger” neural organization may enhance the conduction velocities of these cells, but may result in a loss of spatial resolution. At the base of the eye bulb, axon bundles collect and form a long optic nerve that extends the length of the eye stalk. We suggest that this organization of the diopsid visual system provides evidence for the costs of possessing long eye stalks. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 449–468, 1998     

Sexual dimorphism in the visual system of flies: The divided brain of male Bibionidae (Diptera)

Summary The mapping of the compound eyes onto the visual neuropils and the cell types in the lamina and the lobula complex of Bibionidae (Diptera) were studied by means of extracellular cobalt injections and Golgi impregnations. Dorsal and ventral eyes in males map into separate dorsal-and ventral neuropils up to the level of the lobula complex. The dorsal-eye lamina is unilayered, while the ventral-eye lamina in males and the lamina in females are multilayered: layers A and C are invaded by en-passant terminals of long visual fibres, layer B by the terminals of short visual fibres. Long visual fibres have a short and a long terminal in the ventral medulla with terminal specialisations in three distinct layers. Only one type of receptor ending exists in the dorsal medulla, the terminal branches of which are restricted to one layer only. Arrays of contralateral neurones are found in the medial part of the dorsal lobula, which receives input from the zone of binocular vision of the ipsilateral dorsal eye, and in the posterior dorsal lobula and lobula plate. The dorsal lobula plate contains large tangential neurones, the dendritic arborisations of which are revealed by cobalt injection into the thoracic ganglia. The divided brain of male bibionids offers the opportunity to investigate separately the nervous systems involved in sex-specific visually guided flight behaviour and in general visually guided flight control.     

Connections between wide-field monocular and binocular movement detectors in the brain of a hawk moth

Summary Recordings were made in the brain of Sphinx ligustri of pairs of directionally selective movement detectors, and the spike trains analysed with a computer for possible synaptic connections between two classes of movement detector. (1) Neurones with large binocular fields which arise in the medial protocerebrum and project to the medulla or lobula of one optic lobe, or to the ventral nerve cord. (2) Movement detectors which project from the lobula complex of one optic lobe to the opposite medial protocerebrum. The majority of the second group had back-to-front preferred directions over the ipsilateral eye, and of these many were weakly sensitive to stimuli to the opposite eye. The ipsilateral receptive field covered most of the eye.Optic lobe output cells with the appropriate preferred direction provide a powerful excitatory input to the binocular movement detectors centrifugal to the medulla. Each centrifugal movement detector probably receives excitatory inputs from no more than two optic lobe output cells with back-to-front preferred direction. The same set of optic lobe output neurones probably feeds several cells projecting to the medulla and lobula of both optic lobes, and, possibly, to the ventral nerve cord.Evidence was obtained that the optic lobe output cells themselves receive few excitatory inputs, and that therefore the receptive fields of their input cells are large.Two moving stimuli were presented in different areas of the receptive field. Movement through the null direction in one area inhibited the response to movement in the preferred direction in another area. This suppression was stronger in optic lobe output cells with front-to-back preferred direction than in units with back-to-front preferred direction. Thus the optic lobe output cells, or wide-field units feeding them, receive inhibitory inputs from wide-field units with the opposite preferred direction.Similar tests in which moving stimuli were presented to both eyes gave results indicating that the binocular centrifugal movement detectors may receive inhibitory inputs from movement detectors with back-to-front preferred direction. The possible functional significance of these inhibitory inputs is discussed.I am very greatful to F. A. Miles for helpful discussion and criticism. Financial support came from the U. K. Science Research Council.     

A pair of descending neurons with dendrites in the optic lobes projecting directly to thoracic ganglia of dipterous insects

Summary The lobula descending neuron (LDN) of dipterous insects is a unique nerve cell (one on each side of the brain) that projects directly from the lobula complex of the optic lobes to neuropil in thoracic ganglia. In the supraoesophageal ganglia the LDN has two prominent groups of branches of which at least one is dendritic in nature. Postsynaptic branches are distributed in the lobula and some branches, the synaptic relations of which are not yet known, extend to the lobula plate. A second group of branches is found among dendrites of the descending neurons proper, in the lateral midbrain.The arborizations of LDN in the lobula (and lobula plate) map onto a retinotopic neuropil region subserving a posterior strip of the visual field of the compound eye. The arborizations in the lobula complex are extremely variable in size. The numbers of dendritic spines they possess vary greatly between left and right optic lobes of one animal, and between individual animals.     

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     

Two classes of visual motion sensitive interneurons differ in direction and velocity dependency of in vivo calcium dynamics

Neurons exploit both membrane biophysics and biochemical pathways of the cytoplasm for dendritic integration of synaptic input. Here we quantify the tuning discrepancy of electrical and chemical response properties in two kinds of neurons using in vivo visual stimulation. Dendritic calcium concentration changes and membrane potential of visual interneurons of the fly were measured in response to visual motion stimuli. Two classes of tangential cells of the lobula plate were compared, HS-cells and CH-cells. Both neuronal classes are known to receive retinotopic input with similar properties, yet they differ in morphology, physiology, and computational context. Velocity tuning and directional selectivity of the electrical and calcium responses were investigated. In both cell classes, motion-induced calcium accumulation did not follow the early transient of the membrane potential. Rather, the amplitude of the calcium signal seemed to be related to the late component of the depolarization, where it was close to a steady state. Electrical and calcium responses differed with respect to their velocity tuning in CH-cells, but not in HS-cells. Furthermore, velocity tuning of the calcium response, but not of the electrical response differed between neuronal classes. While null-direction motion caused hyperpolarization in both classes, this led to a calcium decrement in CH-cells, but had no effect on the calcium signal in HS-cells, not even when calcium levels had been raised by a preceding excitatory motion stimulus. Finally, the voltage-[Ca2+]i-relationship for motion-induced, transient potential changes was steeper and less rectifying in CH-cells than in HS-cells. These results represent an example of dendritic information processing in vivo, where two neuronal classes respond to identical stimuli with a similar electrical response, but differing calcium response. This highlights the capacity of neurons to segregate two response components.     

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.