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Intracellular recording Electrophysiology. Recording electrodes were made of glass capillaries (GC100TF-10; Clark Electromedical Instruments, Pangbourne, UK) pulled on a Brown-Flaming P87 puller; when filled with 2 M KAc and 0.5 M KCl they had a resistance of about 20 M
Volume 17, Number 16, Issue of August 15, 1997 pp. 6023-6030
Copyright ©1997 Society for NeuroscienceDendritic Computation of Direction Selectivity and Gain Control in Visual Interneurons
Sandra Single, Juergen Haag, and Alexander Borst Friedrich-Miescher-Laboratory, Max-Planck-Society, D-72076 Tuebingen, Germany
ABSTRACT
The extraction of motion information from time varying retinal images is a fundamental task of visual systems. Accordingly, neurons that selectively respond to visual motion are found in almost all species investigated so far. Despite its general importance, the cellular mechanisms underlying direction selectivity are not yet understood in most systems. Blocking inhibitory input to fly visual interneurons by picrotoxinin (PTX), we demonstrate that their direction selectivity arises largely from interactions between postsynaptic signals elicited by excitatory and inhibitory input elements, which are themselves only weakly tuned to opposite directions of motion. Their joint activation by preferred as well as null direction motion leads to a mixed reversal potential at which the postsynaptic response settles for large field stimuli. Assuming the activation ratio of these opponent inputs to be a function of pattern velocity can explain how the postsynaptic membrane potential saturates with increasing pattern size at different levels for different pattern velocities ("gain control"). Accordingly, we find that after blocking the inhibitory input by PTX, gain control is abolished.
Key words: direction selectivity; motion detection; membrane parameters; compartmental model; synaptic conductance; neural computation; gain control; fly
INTRODUCTION
The fly has for long been a model system to study the processing and extraction of motion information from the time varying retinal images. In the third visual neuropile of the fly optic lobes a group of individually identifiable, motion-sensitive interneurons has been found. They are called lobula plate tangential cells (LPTCs) and are involved in visual course control (Hausen, 1984
). In the blowfly Calliphora erythrocephala this group comprises about 60 different cells. Via large dendritic arbors, these neurons spatially pool the signals of thousands of retinotopically arranged columnar elements (Borst and Egelhaaf, 1992
Fig. 1. a, Simulation of an LPTC receiving input from two arrays of EMDs tuned to opposite directions of motion and forming excitatory (+) and inhibitory () inputs onto the dendrite of the cell, respectively. A VS-cell was three-dimensionally reconstructed from cobalt-stained material and was simulated as having only passive membrane properties. b, Two different types of EMDs were modeled: those with a weak (Model 1) and those with a strong (Model 2.a and Model 2.b) direction selectivity. c, The responses (resp.) of the model LPTC were calculated for both types of EMDs under control conditions (left panel) and after inhibitory synapses were blocked (right panels, two different possible locations of blocking inhibition indicated by the shaded areas in the models in b). Under control conditions both models resulted in the same strong directionally selective motion response as well as in identical decreases of RIN on the order of 15%. When the inhibitory inputs were blocked, however, the different EMD models produced different fingerprints in the LPTC reactions, which allow discrimination between them experimentally.
[View Larger Version of this Image (48K GIF file)]
The computational structure of the fly motion detection system can be well described by a correlation type of elementary motion detector (EMD) (Borst and Egelhaaf, 1989
MATERIALS AND METHODS
Animal preparation Female blowflies (Calliphora erythrocephala) were briefly anesthesized with CO2 and mounted ventral side up with wax on a small preparation platform. The head capsule was opened from behind; the trachea and air sacs, which normally cover the lobula plate, were removed. To eliminate movements of the brain caused by peristaltic contractions of the esophagus, the proboscis of the animal was cut away, and the gut was pulled out. This allowed stable intracellular recordings of up to 45 min. The fly was then mounted in an upright position on a heavy recording table with the stimulus monitors in front of the animal. The fly brain was viewed from behind through a Zeiss dissection scope. For details of the dissection procedure, see Hausen (1982). Signals were amplified (SEC-10L; npi Electronics; operated in DCC mode at a switching frequency of 20 kHz) and fed to a 486 personal computer (PC) via an analog-to-digital (A/D) converter (DT 2801-A; Data Translation) at 2 kHz.
Stimulation. Stimuli were generated on a Tektronix 608 monitor by an image synthesizer (Picasso, Innisfree, Cambridge, MA) and consisted of a one-dimensional square wave grating of 28° spatial wavelength, 84% contrast, and 11.9 cd/m2 mean luminance displayed at a frame rate of 200 Hz. The angular width of the stimulus field was 62° in the horizontal and 74° in the vertical direction as seen by the fly. When activated, the grating was moving at 56°/sec.
Stimulus protocol and data processing. Each cell was continuously subject to the stimulus protocol shown in Figure 2a. For 2 sec, the pattern was at rest; then, the cell was stimulated for 2 sec by motion in its preferred direction and, for another 2 sec, by motion in its null direction. This sequence was repeated over and over again. For each stimulus condition (no motion, PD motion, and ND motion), five pulses of 2 nA of hyperpolarizing current were injected into the cell to determine the input resistance (RIN). The motion-induced change of input resistance, [RIN(motion) 4 M solution of PTX diluted in fly saline was injected into the hemolymph close to the lobula plate by means of a syringe. To allow for rapid diffusion, the neurolemma covering the lobula plate was punctuated before by means of a tungsten electrode. The responses were recorded for about 15-30 min. Because the time course of the PTX effect varied from recording to recording, averages were taken of those response sweeps for which the ND responses had reversed their sign and amounted to at least 50% of the PD response.
Fig. 2. a, Intracellular recording from a VS-cell of the fly lobula plate before (top panel) and 10 min after (bottom panel) PTX has been applied to the hemolymph (mean of 10 sweeps). The bars underneath the lower response trace indicate the 2 sec time interval while a grating was moving in the PD and ND of the cell, respectively. During motion as well as while the pattern was at rest, 2 nA pulses of hyperpolarizing current were injected into the cell to determine the input RIN. b, c, Motion response (b) and motion-induced change of input resistance ([RIN(motion)
[View Larger Version of this Image (39K GIF file)]
Extracellular recording Electrophysiology. Extracellular recordings were performed from the axonal arborizations of the H1-cell in the hemisphere contralateral to the stimulus side using a sharpened tungsten electrode. We decided to record from this spiking neuron, because experiments lasting several hours can easily be accomplished in extracellular recordings, and the general visual response characteristics of the H1-cell do not differ from those of VS- and CH-cells (Hausen, 1984
Stimulation. Stimuli consisted of a one-dimensional sine wave grating of 24° spatial wavelength, 29% (Fig. 3c,d) and 8% (Fig. 3e,f) contrast, and 21 cd/m2 mean luminance displayed at a frame rate of 200 Hz. The angular width of the stimulus field was 58° in the horizontal direction and 43° in the vertical direction as seen by the fly. Pattern size was varied in four or five steps of 10.7 or 8.6°, respectively, along the vertical axis of the stimulus monitor and presented at two different velocities for PD motion (72 or 360°/sec). 
Fig. 3. Gain control in model cell and real fly cell before and after blockade of inhibition. a, b, For the LPTC model, we used identical membrane parameters as in Figure 1. Inputs were driven by weak directional EMDs (Fig. 1b, Model 1). When stimulated by patterns of increasing size at two different velocities, the axonal membrane potential saturates at different levels (gain control). After blocking the inhibitory inputs, both velocities yield similar responses. c-f, Extracellular recordings of spiking LPTCs (H1-cells) before (c, e) and after (d, f) PTX application, using two different image velocities (v1 = 72 °/sec; v2 = 360 °/sec). c, In normal fly saline, the response increases with increasing stimulus size and saturates for each stimulus velocity at a different response level (gain control). d, After PTX application, the response increases significantly but now saturates at the same level for both velocities. Data represent the mean ± SEM of recordings from four different animals. e, f, Same experiment as in c, d, but using low-contrast gratings this time. A high-contrast stimulus with full pattern size was additionally used to determine a maximum spike frequency of each cell. All responses are expressed as percentage of this value. After PTX application, the cells respond at about the same level to both velocities. However, the responses to v2 now is slightly stronger than to v1 (compare with simulation results in a, b). Data represent the mean ± SEM of recordings from four different animals.
[View Larger Version of this Image (34K GIF file)]
Simulations Denoting the spatial separation between the input lines of the motion detectors as
Stimulus protocol and data processing (different from intracellular recordings). PTX was diluted in fly saline to 3 × 10 , the pattern had a one-dimensional sinusoidal luminance modulation of wavelength
= 16
= 60 msec, and multipliers M. The output signals of the motion detectors were used as excitatory and inhibitory conductances (about 1-2 mS/cm2, the exact value depending on the stimulus condition) for a variable number of dendritic membrane areas of the cell, using the compartmental model software Nemosys (Eeckman et al., 1994
RESULTS
We investigated the degree of direction selectivity of the input elements of LPTCs by a combined experimental and modeling approach. Our experimental diagnostics consisted in intracellular recordings of the motion response of LPTCs as well as in measurements of their motion-induced change of input resistance (RIN), a measure of synaptic conductance changes. We also disturbed the system by blocking inhibitory input synapses with PTX. As will be shown by our simulation studies, both weak and strong directional EMDs can lead to identical reactions of the LPTCs. However, when inhibitory synapses are blocked, the two alternatives then lead to different predictions and, thus, allow to decide between them experimentally.
The simulation study comprised two arrays of EMDs tuned to opposite directions of motion, which make excitatory and inhibitory synapses on the dendrite of a realistic compartmental model of a fly LPTC, respectively (Fig. 1a). The model cell had only passive membrane properties, the precise values of which were determined in an independent set of experiments (Borst and Haag, 1996
We tested these model predictions in intracellular recordings from fly LPTCs. In normal fly saline, PD motion led to a graded depolarization, whereas ND motion hyperpolarized the LPTCs. After PTX application, the PD response increased, whereas the ND response reversed its sign (Fig. 2a,b). Such a strong decrease of direction selectivity caused by the GABA receptor blocker has been reported previously for extracellular measurements of spiking LPTCs such as the H1-cell (Schmid and Bülthoff, 1988
Weak directional tuning of EMDs results in a joint activation of excitatory and inhibitory input by either preferred or null direction motion. This has the interesting functional consequence that the membrane potential of the postsynaptic cell is expected to saturate with increasing pattern size moving in the preferred direction of the cells at a level between the excitatory and inhibitory reversal potentials. Because for correlation-type local motion detectors the activation ratio of the excitatory and inhibitory input elements is a function of pattern velocity (Reichardt, 1987 With increasing pattern size, ge and gi become large compared with gleak, and the membrane potential tends toward a saturation level. Assuming Ee =
(1) with c = gi/ge denoting the ratio of inhibitory and excitatory conductances being co-activated during PD motion. Obviously, without assuming additional mechanisms, gain control can only occur for weak directional EMDs. In correlation-type EMDs, the ratio c is expected to depend on the image velocity v in approximately the following way:
(2) with R denoting 2
(3) times the ratio of the sampling base of the EMD and the spatial pattern wavelength
denoting the phase response of the temporal filter of the EMD.
We simulated the spatial integration properties of the model cell with weak directional EMDs at two different image velocities, with and without inhibitory synaptic input. With both excitatory and inhibitory input being intact, the model cell indeed showed gain control; with increasing pattern size the membrane potential saturated at different levels for both velocities, with the smaller velocity yielding larger responses (Fig. 3a). When the inhibitory input was blocked, both image velocities resulted in similar responses, and the response to the higher velocity was now slightly stronger than to the smaller one (Fig. 3b).
To verify these predictions experimentally we recorded the activity of a spiking LPTC, the H1 neuron, with an extracellular electrode and measured the responses to gratings moving horizontally along the preferred direction at two different speeds. In normal fly saline, the responses became larger with increasing pattern size and saturated at different levels for the two image velocities (Fig. 3c). After PTX application the responses were increased overall. Importantly, the neurons now responded with about the same strength to both velocities (Fig. 3d). Thus, in accordance with the simulation results, gain control was abolished after the inhibitory input to the LPTCs has been blocked. However, this effect could have also been attributable to a spike frequency saturation caused by the increased responsiveness of the cell after PTX application. We therefore repeated the experiments at low stimulus contrasts (Fig. 3e,f), including additional measurements of the maximum firing rate of the cell in response to high-contrast stimuli. Again, after PTX application, the cells responded with about the same spike frequency to both velocities. However, because of the low contrast stimulation, keeping the cell away from output saturation, more details of the response became visible: (1) in comparison with the control conditions, the response increase was more linear than before PTX application; and (2) the higher velocity yielding a smaller response before now resulted in a slightly stronger response amplitude than did the lower velocity. Both response characteristics were in close agreement with the simulation results (Fig. 3, compare f with b).
DISCUSSION
By measuring the motion-induced change of input resistance before and after the application of PTX, we have provided evidence that the input elements to the fly LPTCs exhibit only weak directional tuning. Consequently, the strong direction selectivity observed in the visual responses of fly LPTCs comes about by the opponent action of input elements. As a functional consequence the membrane potential of LPTCs saturates with increasing pattern size at different levels for different pattern velocities (gain control).
There are two critical questions arising in this context. The first question is to what extent the motion-induced change of input resistance can be attributed to synaptic conductance changes as was done here, or whether they reflect second-order effects such as voltage-gated conductances after synaptic activation. First of all, measurements of the specific passive membrane parameters of fly LPTCs (Borst and Haag, 1996
Another important question pertains to the site of action of PTX. Because the drug was applied extracellularly to the lobula plate by either punctuating the neurolemma or direct pressure injection (see Materials and Methods), it could affect other GABAergic inhibitory synapses, too, besides the ones on the LPTC dendrites. When we added identical amounts of PTX to the hemolymph without punctuating the neurolemma, no effect on the visual response properties of the H1 neuron was observed, indicating a rather localized effect of the drug. As a further control, we also pressure injected PTX into the medulla instead of the lobula plate. Interestingly, besides some differences in the time course, these different procedures resulted in almost identical effects on the visual response properties of the H1-cell (data not shown). This can indicate either that, within the limits of our diagnostic tools, different sites of PTX action lead to similar results in the LPTC responses, or, alternatively, that PTX is rather free to diffuse within the optic lobes of the fly. Whatever the answer to these alternatives is, we know that (1) PTX-sensitive GABA receptors do exist on LPTC dendrites and thus will be blocked by PTX, and (2) as can be seen by our simulation results (Fig. 1b, Model 2.b), additional action on presynaptic targets anywhere upstream of the LPTC dendrite results in an increased activity of the remaining excitatory input to the LPTC and consequently to an increased change of input resistance during PD motion. However, we observed a clear reduction of motion-induced change of input resistance after PTX application. This is only compatible with a rather specific effect of PTX restricted to the LPTC input synapses.
In this context, it is also of interest to consider the situation if the input elements had, in contrast to our conclusions, a full directional tuning. What would be the consequence? To explain both the large motion-induced changes of input resistance and the small amplitudes of LPTC visual responses, one had to postulate very small driving forces for the underlying ionic currents. As outlined in Materials and Methods, the value for the inhibitory current would be 13 mV below, and the value for the excitatory current had to be only 24 mV above the resting potential of the cell. Both values are highly unlikely, given the usual internal and external concentrations of the participating ions. Furthermore, fully directional input elements would lead to one fixed reversal potential in the postsynaptic cell, irrespective of pattern velocity. To explain gain control, one, therefore, had to postulate additional mechanisms for gain control in LPTCs.
In summary, as a functional consequence of having both the subtraction of opponent inputs as well as the spatial integration of these inputs implemented within one stage on the dendrites of the cells, their response can still signal changes in image velocity even under conditions in which the cells are spatially saturated. Apart from dynamic aspects of this signaling (Haag and Borst, 1996
FOOTNOTES
Received April 15, 1997; revised May 22, 1997; accepted May 23, 1997.
We are grateful to T. Martin for excellent technical assistance, T. Brotz, V. Gauck, J. Gold, and F. Theunissen for helpful discussions and critically reading earlier versions of this manuscript, and K. G. Goetz (Max-Planck-Institute of Biological Cybernetics) for the generous loan of part of the equipment.
Correspondence should be addressed to Alexander Borst, Friedrich-Miescher-Laboratory, Max-Planck-Society, Spemannstrasse 37-39, D-72076 Tuebingen, Germany.
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ABSTRACT
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