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A Borst

Publications and source records attributed to A Borst.

At least 55 records · Page 3Linked to original sources

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 identification 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 microM) 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.

Acetylcholine↗

Calcium accumulation in visual interneurons of the fly: stimulus dependence and relationship to membrane potential.

1. The large motion-sensitive tangential neurons in the fly third visual neuropil spatially pool the postsynaptic signals of many local elements. The changes in membrane potential and calcium concentration induced in these cells by visual motion are analyzed in vivo by simultaneous optical and intracellular voltage recording techniques. 2. Visual motion in the preferred direction leads to depolarization of the cell and to calcium accumulation mainly in the axon terminal, the soma, and the dendritic tree. During motion in the null direction, the cell hyperpolarizes and virtually no changes in calcium concentration can be observed. 3. Dendritic calcium accumulation is first restricted to those dendritic branches that are close to the sites of direct synaptic input. In other parts of the dendrite the calcium concentration increases more slowly and usually reaches only lower levels. 4. Calcium starts accumulating at the onset of motion. However, the calcium concentration reaches its final steady-state level much later than the corresponding membrane potential changes. Even if these are completely transient at high temporal frequencies of pattern motion, the calcium signal stays high until the stimulus pattern stops moving. 5. The amplitude of the calcium signal depends on the temporal frequency of pattern motion in a similar way as do the corresponding membrane potential changes. However, there exist differences that can be attributed to the different time courses of both signals. 6. Depolarization of the dendritic tree by current injection through a microelectrode leads to similar changes in calcium accumulation as does activation by synaptic input, suggesting that calcium enters the cell via voltage-dependent channels. The possible function of calcium channels for dendritic integration of synaptic input is discussed.

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Processing of synaptic information depends on the structure of the dendritic tree.

The consequences of dendritic geometry for the processing of synaptic information was analysed in two types of motion-sensitive neurones in the visual system of the fly. These neurones differ conspicuously in the morphology of their dendrites but receive their input from the same type of local motion-sensitive elements. Intracellular recording and activating selected regions of the dendrite by visual motion showed that, in accordance with cable theory of nerve cells, the way in which postsynaptic signals interact is essentially determined by the structure of the dendritic tree.

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Dendritic processing of synaptic information by sensory interneurons.

One of the most distinguishing features of nerve cells is the vast morphological diversity of their input regions, that is, their dendrites. These range from bulbous structures, with only small protrusions, to large tree-like arborizations. The diversity of nerve cells is further augmented by a continuously increasing number of types of voltage-dependent conductances in dendrites that might alter the postsynaptic signals in a pronounced way. Moreover, intracellular factors such as Ca2+ link electrical activity with biochemical processes, and can induce short and long-term changes in responsiveness. This complexity of neurons in general, and the uniqueness of each cell type, sharply contrasts with the comparatively simple and uniform design principle of the integrate-and-fire units of so-called neuronal net models. This raises the question of which particular structural and physiological details of nerve cells really matter for the performance of neuronal circuits. An answer to this basic problem of computational neurobiology might be given only if the task of the neurons and circuits is known. This review illustrates how the problem can be approached particularly well in sensory interneurons. The functional significance of sensory interneurons can often be assessed more easily than that of central nerve cells because of their vicinity to the sensory surface.

Animals↗

Motion computation and visual orientation in flies.

1. Visual orientation greatly relies on the evaluation of the motion patterns received by the eyes when the animal moves around. 2. In a combination of behavioral, neurophysiological and pharmacological analysis and modelling, the mechanisms are established by which the visual system of the fly extracts three types of-basic retinal motion patterns. 3. Coherent retinal large-filed motion as is induced during deviations of the animal from its course, image expansion occurring when the animal approaches an obstacle, and relative motion which is induced when a nearby object is passed in front of its background. 4. Separate neuronal networks are specifically tuned to each of these motion patterns and make use of them in three different orientation tasks: in compensatory course stabilization, the control of landing behaviour and the fixation of objects.

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Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques.

1. Visual interneurons tuned to the motion of small objects are found in many animal species and are assumed to be the neuronal basis of figure-ground discrimination by relative motion. A well-examined example is the FD1-cell in the third visual neuropil of blowflies. This cell type responds best to motion of small objects. Motion of extended patterns elicits only small responses. As a neuronal mechanism that leads to such a response characteristic, it was proposed that the FD1-cell is inhibited by the two presumably GABAergic and, thus, inhibitory CH-cells, the VCH- and the DCH-cell. The CH-cells respond best to exactly that type of motion by which the activity of the FD1-cell is reduced. The hypothesis that the CH-cells inhibit the FD1-cell and, thus, mediate its selectivity to small moving objects was tested by ablating the CH-cells either pharmacologically or by photoinactivation. 2. After application of the gamma-aminobutyric acid (GABA) antagonist picrotoxinin, the FD1-cell responds more strongly to large-field than to small-field motion, i.e., it has lost its small-field selectivity. This suggests that the tuning of the FD1-cell to small moving objects relies on a GABAergic mechanism and, thus, most likely on the CH-cells. 3. The role of each CH-cell for small-field tuning was determined by inactivating them individually. They were injected with a fluorescent dye and then ablated by laser illumination. Only photoinactivation of the VCH-cell eliminated the specific selectivity of the FD1-cell for small-field motion. Ablation of the DCH-cell did not significantly change the response characteristic of the FD1-cell. This reveals the important role of the VCH-cells in mediating the characteristic sensitivity of the FD1-cell to motion of small objects. 4. The FD1-cell is most sensitive to motion of small objects in the ventral part of the ipsilateral visual field, whereas motion in the dorsal part influences the cell only weakly. This specific feature fits well to the sensitivity of the VCH-cell to ipsilateral motion that is most pronounced in the ventral part of the visual field. The spatial sensitivity distribution of the FD1-cell matches also the characteristics of figure-ground discrimination and fixation behavior.

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Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques.

1. The FD1-cell in the visual system of the fly is an identified visual interneuron that is specifically tuned to motion of small objects. In the companion paper it was shown that this response property is mediated by one of the two CH-cells, the VCH-cell, that inhibits the FD1-cell by GABAergic synapses. Here the input organization of the two CH-cells is analyzed by both electrophysiological and optical recording techniques. 2. Both CH-cells are excited by front-to-back motion in the ipsilateral and by back-to-front motion in the contralateral visual field. They respond maximally to binocular rotatory motion about the vertical axis of the animal. The latter response is only slightly less than the sum of the corresponding monocular response components. The relative contribution of the ipsi-and contralateral eye to the binocular response varies considerably between flies. In extreme cases it is dominated by either the ipsi- or the contralateral eye. The two CH-cells are not equally sensitive along the vertical axis of the eye. The DCH-cell has its sensitivity maximum in the dorsal part, the VCH-cell in the ventral part of the visual field. 3. The CH-cells have two arborizations, a large one in the posterior part of the third visual neuropil, the lobula plate, and a smaller one in the ipsilateral ventrolateral brain. With the calcium-sensitive dye fura-2 as an activity marker, it is analyzed which of these branches of the CH-cells receive the ipsi- and contralateral motion input, respectively. During motion in the preferred direction within the ipsilateral visual field, calcium accumulates only in the CH-cells' main arborization in the lobula plate but not in their branches in the ventrolateral brain, indicating that the arborization in the lobula plate is postsynaptic to the ipsilateral input. In contrast, contralateral motion in the preferred direction leads to calcium accumulation in both arborizations, suggesting that both are postsynaptic to contralateral input elements. During preferred direction motion in the upper or lower part of the ipsilateral visual field, calcium accumulates in only dorsal or ventral branches of the CH-cells' arborization in the lobula plate, respectively, revealing that their ipsilateral motion input is organized retinotopically. Because this arborization, most likely, is also the main output terminal of the CH-cells, it is both pre- and postsynaptic. This specific neuronal design is discussed with respect to its consequences for the mechanism of tuning the FD1-cell to motion of small objects.

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Photo-ablation of single neurons in the fly visual system reveals neural circuit for the detection of small moving objects.

Many animals use relative motion to segregate objects from their background. Nerve cells tuned to this visual cue have been found in various animal groups, such as insects, amphibians, birds and mammals. Well examined examples are the figure detection (FD) cells in the visual system of the blowfly. The mechanism that tunes a particular FD-cell, the FD1-cell, to small-field motion is analyzed by injecting individual visual interneurons with a fluorescent dye and ablating them by illumination with a laser beam. In this way, it is shown that the FD1-cell acquires its specific spatial tuning by inhibitory input from an identified GABAergic cell, the ventral centrifugal horizontal (VCH)-cell which is most sensitive to coherent large-field motion in front of both eyes. For the first time, the detection of small objects by evaluation of their motion parallax, thus, can be attributed to synaptic interactions between identified neurons.

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Dendritic integration of motion information in visual interneurons of the blowfly.

Dendritic integration plays a key role in the way information is processed by nerve cells. The large motion-sensitive interneurons of the fly appear to be most appropriate for an investigation of this process. These cells are known to receive input from numerous local motion-sensitive elements and to control visually-guided optomotor responses (e.g., Trends Neurosci., 11 (1988) 351-358; Stavenga and Hardie, Facets of Vision, Springer, 1989). The retinotopic input organization of these cells allows for in vivo stimulation of selected parts of their dendritic tree with their natural excitatory and inhibitory synaptic input signals. By displaying motion in either the cells' preferred or null direction in different regions of the receptive field we found: (i) Responses to combinations of excitatory and inhibitory motion stimuli can be described as the sum of the two response components. (ii) Responses to combination of excitatory stimuli show saturation effects. The deviation from linear superposition depends on the distance and relative position of the activated synaptic sites on the dendrite and makes the responses almost insensitive to the number of activated input channels. (iii) The saturation level depends on different stimulus parameters, e.g. the velocity of the moving pattern. The cell still encodes velocity under conditions of spatial saturation. The results can be understood on the basis of passive dendritic integration of the signals of retinotopically organized local motion-detecting elements with opposite polarity.

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In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation.

The computation of motion plays a central role in visual orientation. The fly has been successfully used as a model system for analyzing the mechanisms underlying motion detection. Thereby, much attention has been paid to a neuronal circuit of individually identifiable neurons in the third visual ganglion that extracts different types of retinal motion patterns and converts these patterns into specific components of visual orientation behavior. The extended dendritic trees of these large cells are the sites of convergence of numerous spatially distributed local motion-sensitive elements. As is revealed by in vivo microfluorometric imaging, these cells accumulate calcium during activation by visual motion stimulation. The spatiotemporal pattern of calcium distribution shows the following characteristics: (i) calcium accumulation is first spatially restricted to those dendritic branches that are depolarized by the retinotopic input, (ii) during ongoing motion stimulation calcium may also accumulate throughout the cell and, in particular, in regions that do not receive direct synaptic input. These experiments successfully monitor the intracellular distribution of activity-dependent ions in visual interneurons of living animals stimulated by their natural synaptic input.

Animals↗

Are there separate ON and OFF channels in fly motion vision?

Visual information is processed in a series of subsequent steps. The performance of each of these steps depends not only on the computations it performs itself but also on the representation of the visual surround on which it operates. Here we investigate the consequences of signal preprocessing for the performance of the motion-detection system of the fly. In particular, we analyze whether the retinal input signals are rectified and segregate into separate ON and OFF channels, which then feed independent parallel motion-detection pathways. We recorded the activity of an identified directionally selective interneuron (H1-cell) in response to apparent motion stimuli, i.e. sequential brightness changes at two neighboring locations in the visual field, as well as to brightness changes at only a single location. For apparent motion stimuli, the motion-dependent response component was determined by subtracting from the overall response to the individual stimulus components when presented alone. The following conclusions could be derived: (1) Apparent motion consisting of a sequence of increased or decreased brightness at two locations in the visual field have the same optimum interstimulus time interval (Fig. 3). (2) Sequences of brightness steps of like polarity (either increments or decrements) elicit positive and negative motion-dependent response components when mimicking motion in the cell's preferred and null direction, respectively. The motion-dependent response components are inverted in sign when the brightness steps of a stimulus sequence have a different polarity (Fig. 7). (3) The responses to the beginning and the end of a brightness pulse depend on the pulse duration. For pulse durations of less than 2 s, both events interact with each other (Fig. 9). All of these results do not provide any indication that the fly processes motion information in independent ON and OFF motion detectors. Brightness changes of both signs are rather represented at the input of the same movement detectors, and interactions between signals resulting from both brightness increments and decrements take their sign into account. This type of preprocessing of the retinal input is argued to render a motion-detection system particularly robust against noise.

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The role of GABA in detecting visual motion.

The basic computations underlying the extraction of motion from the visual environment have been characterized in great detail. A non-linear interaction, such as a multiplication, between neighbouring visual elements was shown to be the core of biological motion detectors in different species ranging from insects to man. GABA (gamma-aminobutyric acid)-ergic inhibitory synapses suppressing the responses to motion in one direction but not in the other are widely accepted to be the cellular basis for this non-linear interaction. Based on model predictions we can show in combined pharmacological and electrophysiological experiments that in the fly motion detection system GABAergic synapses do not play this role but rather are involved in another important step of motion computation. This makes a reconsideration of the role of inhibition in other motion detection systems necessary.

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Neuronal architecture of the antennal lobe in Drosophila melanogaster.

Computer reconstruction of the antennal lobe of Drosophila melanogaster has revealed a total of 35 glomeruli, of which 30 are located in the periphery of the lobe and 5 in its center. Several prominent glomeruli are recognizable by their location, size, and shape; others are identifiable only by their positions relative to prominent glomeruli. No obvious sexual dimorphism of the glomerular architecture was observed. Golgi impregnations revealed: (1) Five of the glomeruli are exclusive targets for ipsilateral antennal input, whereas all others receive afferents from both antennae. Unilateral amputation of the third antennal segment led to a loss of about 1000 fibers in the antennal commissure. Hence, about 5/6 of the approximately 1200 antennal afferents per side have a process that extends into the contralateral lobe. (2) Afferents from maxillary palps (most likely from basiconic sensilla) project into both ipsi- and contralateral antennal lobes, yet their target glomeruli are apparently not the same as those of antennal basiconic sensilla. (3) Afferents in the antennal lobe may also stem from pharyngeal sensilla. (4) The most prominent types of interneurons with arborizations in the antennal lobe are: (i) local interneurons ramifying in the entire lobe, (ii) unilateral relay interneurons that extend from single glomeruli into the calyx and the lateral protocerebrum (LPR), (iii) unilateral interneurons that connect several glomeruli with the LPR only, (iv) bilateral interneurons that link a small number of glomeruli in both antennal lobes with the calyx and LPR, (v) giant bilateral interneurons characterized by extensive ramifications in both antennal lobes and the posterior brain and a cell body situated in the midline of the suboesophageal ganglion, and (vi) a unilateral interneuron with extensive arborization in one antennal lobe and the posterior brain and a process that extends into the thorax. These structural results are discussed in the context of the available functional and behavioral data.

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Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process.

Direction selectivity of motion-sensitive neurons is generally thought to result from the nonlinear interaction between the signals derived from adjacent image points. Modeling of motion-sensitive networks, however, reveals that such elements may still respond to motion in a rather poor directionally selective way. Direction selectivity can be significantly enhanced if the nonlinear interaction is followed by another processing stage in which the signals of elements with opposite preferred directions are subtracted from each other. Our electrophysiological experiments in the fly visual system suggest that here direction selectivity is acquired in such a two-stage process.

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Principles of visual motion detection.

Motion information is required for the solution of many complex tasks of the visual system such as depth perception by motion parallax and figure/ground discrimination by relative motion. However, motion information is not explicitly encoded at the level of the retinal input. Instead, it has to be computed from the time-dependent brightness patterns of the retinal image as sensed by the two-dimensional array of photoreceptors. Different models have been proposed which describe the neural computations underlying motion detection in various ways. To what extent do biological motion detectors approximate any of these models? As will be argued here, there is increasing evidence from the different disciplines studying biological motion vision, that, throughout the animal kingdom ranging from invertebrates to vertebrates including man, the mechanisms underlying motion detection can be attributed to only a few, essentially equivalent computational principles. Motion detection may, therefore, be one of the first examples in computational neurosciences where common principles can be found not only at the cellular level (e.g., dendritic integration, spike propagation, synaptic transmission) but also at the level of computations performed by small neural networks.

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