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The Journal of Neuroscience, April 15, 2002, 22(8):3227-3233
Dendro-Dendritic Interactions between Motion-Sensitive
Large-Field Neurons in the Fly
Juergen
Haag and
Alexander
Borst
Department of Environmental Science, Policy, and Management,
Division of Insect Biology, University of California, Berkeley,
Berkeley, California 94720
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ABSTRACT |
For visual course control, flies rely on a set of motion-sensitive
neurons called lobula plate tangential cells (LPTCs). Among these
cells, the so-called CH (centrifugal horizontal) cells shape by
their inhibitory action the receptive field properties of other LPTCs
called FD (figure detection) cells specialized for
figure-ground discrimination based on relative motion. Studying the
ipsilateral input circuitry of CH cells by means of dual-electrode and
combined electrical-optical recordings, we find that CH cells receive
graded input from HS (large-field horizontal system) cells via
dendro-dendritic electrical synapses. This particular wiring scheme
leads to a spatial blur of the motion image on the CH cell dendrite,
and, after inhibiting FD cells, to an enhancement of motion contrast. This could be crucial for enabling FD cells to discriminate object from
self motion.
Key words:
calcium; dendrite; electrophysiology; insect; motion
detection; vision
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INTRODUCTION |
Image segmentation into objects and
background is of prime importance for visual orientation and can rely
on several cues. Fast-flying animals, such as dipteran flies, have
shown to use motion cues for this task. When flying tethered in a well
defined environment, i.e., an arena consisting of a foreground figure and a background pattern, flies consistently exert torque toward the
figure whenever the figure moves relative to the background (Heisenberg
and Wolf, 1979 ; Reichardt and Poggio, 1979; Egelhaaf 1985a; Kimmerle
and Egelhaaf, 2000a). Analysis of the neural circuitry underlying this
motion-based figure-ground discrimination revealed a specific class of
neurons termed FD (figure detection) cells (Egelhaaf, 1985b),
which become selectively activated by motion of small objects in front
of an extended background. This response selectivity vanished after
laser ablation of the so-called vCH (ventral centrifugal
horizontal) cell (Warzecha et al., 1993), an inhibitory GABAergic
neuron (Meyer et al., 1986) with output synapses located within the
dendrite (Gauck et al., 1997).
FD and CH cells belong to a set of ~60 individually identifiable
motion-sensitive neurons called lobula plate tangential cells (LPTCs)
(Hausen et al., 1980; Hausen, 1982, 1984; Hengstenberg et al., 1982;
Borst and Haag, 1996; Haag and Borst, 2001). Among the LPTCs, HS
(large-field horizontal system) and VS (vertical system) cells are
thought to be the major output elements conveying information about
large-field horizontal and vertical image motion onto descending
neurons, which ultimately control motor neurons for locomotion or head
movements (Gronenberg and Strausfeld, 1990; Gilbert et al., 1995; Chan
et al., 1998). Whereas most LPTCs are thought to spatially integrate
the output signals of many thousands of columnar, local
motion-sensitive neurons on their large dendrite in the lobula
plate, the origin of motion sensitivity in CH cells remains
controversial. Based on the observations of anatomical structures
called "blebs" in their large lobula plate arborizations, CH cells
were first concluded to be solely presynaptic in the lobula plate and,
therefore, were christened "centrifugal horizontal" (Eckert and
Dvorak, 1983). CH cells were thought to inherit motion sensitivity from
HS cells via their ramifications in the protocerebrum. However, after
local motion stimulation, local calcium accumulation was observed in
the dendrites of CH cells (Egelhaaf et al., 1993). This fact is
incompatible with the assumption of CH cells being postsynaptic to the
axon terminal of HS cells only, in which all of the motion information
is spatially integrated, and any positional information is completely lost.
On the other hand, precise knowledge about the input circuitry of CH
cells and exactly where on the extended branches of the neurons
these cells make contact seems to be crucial for understanding the
essence of the neural mechanism underlying figure-ground
discrimination: one cell inhibiting another does not necessarily tune
the latter sensitive to small moving objects. To decide from which
neurons of the lobula plate CH cells receive their motion-sensitive
input and where this input converges onto their extended ramifications, i.e., lobula plate or protocerebrum, we, therefore, studied the connectivity between CH cells and other motion-sensitive neurons with
similar visual response properties, i.e., HS cells. Using dual
intracellular and combined optical-electrical recording techniques, we
show in the following that CH cells receive ipsilateral visual motion
information via electrical dendro-dendritic synapses from HS cells. As
will be discussed in detail, this particular wiring cannot only resolve
a number of puzzling facts about CH cells collected in the past but
seems also appropriate for the function of CH cells in the context of
figure-ground discrimination.
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MATERIALS AND METHODS |
Preparation and set up. Female blowflies
(Calliphora vicina) were briefly anesthetized with
CO2 and mounted ventral side up with wax on a
small preparation platform. The head capsule was opened from behind;
the trachea and airsacs that 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. The fly was then mounted on a heavy
recording table. Visual stimuli were produced by an arc lamp, the image
of which was projected onto a screen (10 × 8 cm) positioned 10.5 cm below the fly. The square wave grating had a spatial wavelength of
12°, a mean luminance of 17.7 cd/m2, and
a contrast of 92%. The fly brain was viewed from behind through a
microscope (Axiotech vario 100HD; Zeiss, Oberkochen, Germany).
Electrical recording. Electrodes were pulled on a
Brown-Flaming micropipette puller (P-97) using thin-wall glass
capillaries with an outer diameter of 1 mm (GC100TF-10; Clark
Electromedical Instruments, Pangbourne, UK). The tip of the electrode
was filled with 8.8 mM Calcium Green (Ca-Green-1
hexapotassium salt; Molecular Probes, Eugene, OR), 10 mM Alexa 568 (Alexa Fluor 568 hydrazide; Molecular Probes), or 8.8 mM Calcium Orange
(Ca-Orange tetrapotassium salt; Molecular Probes). The shaft of the
electrode was filled with a solution containing 2 M KAc plus 0.5 M
KCl. Electrodes had resistances of ~25 M . An SEL10 amplifier (NPI
Electronics, Tamm, Germany) was used in the bridge mode. For the
experiments with dual intracellular recordings a second SEL10 amplifier
was used. All recordings were made from the axons of the cells. For data analysis, the output signal of the amplifier was fed to a Pentium
III personal computer via an 12 bit analog-to-digital converter
(DAS-1602; ComputerBoards, Middleboro, MA) at a sampling rate of 5 kHz.
Optical recording. We used a Zeiss UD 20×, 0.57 numerical
aperture (NA) air objective or an Epiplan 40×, 0.75 NA water
immersion lens and a CCD camera (equipped with an EEV chip,
1024 × 512 pixel; PXL; PhotoMetrics Inc., Huntington Beach, CA)
connected to a Power Macintosh (Apple Computers, Cupertino, CA). The
first frame of each image series was taken as a reference and
subtracted from each following image. This resulted in a series of
difference images ( F), which were subsequently
divided by the reference frame (F/F).
For calcium imaging, we used Calcium Green (Molecular Probes) with the
Zeiss filter set #9 [bandpass (BP), 450-490 nm; dichroic mirror (DM),
510 nm; longpass (LP), 520 nm] and Calcium Orange (Molecular
Probes) with the Zeiss filter set #15 (BP, 546 nm; DM, 580 nm; LP, 590 nm). To visualize neurons with Alexa 568 (Molecular Probes), we used
the same filter set.
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RESULTS |
As mentioned in the introductory remarks, HS and CH cells share
many visual response properties: like CH cells, HS cells are excited by
horizontal front-to-back motion and respond to motion stimuli in a
graded way (Eckert and Dvorak, 1983). To investigate whether this
response similarity is based on direct connectivity, HS and CH cells
located in the same hemisphere were recorded simultaneously by means of
intracellular electrodes (Fig. 1). When
the pattern moved in the preferred (PD) and null direction (ND) of the
cells, both neurons exhibited similar response characteristics (Fig. 1a), including high-amplitude EPSPs during PD motion (Haag
and Borst, 2001). In Figure 1b, the HS EPSPs were used to
trigger the averaging of CH signals. Both averages revealed a
synchronous rise with almost no delay. To investigate whether these
EPSPs in the CH cell are elicited by HS EPSPs or arise in parallel, HS
cells were stimulated to produce large-amplitude action potentials (Hengstenberg, 1977; Haag et al., 1997) by release from hyperpolarizing current injection (Fig. 2c,
inset). Triggering CH cell signals by these HS cell rebound
spikes did not reveal any distinct signals in CH cells (Fig.
1c). We conclude that CH and HS cells receive a common input
causing the large EPSPs in parallel. Thus, either the cells are not
connected with each other or the connection does not allow fast signals
to travel across. To decide between these alternatives, we injected
current of either polarity into one of the cells and measured the
membrane voltage in the other. Figure 1d shows that HS cells
and CH cells followed with their membrane potential when current was
injected into the partner cell. The current-voltage relationship of
the HS-CH cell coupling as shown in Figure 1e was fairly
linear after a slight outward rectification that was observed
previously for the intrinsic current-voltage relationship of HS cells
(Borst and Haag, 1996). The amplitude of membrane potential change in
the follower cell was ~10-15% of the membrane potential change
recorded in the cell in which the current was directly injected. In
summary, HS and CH cells are coupled to each other in a symmetrical
way, with current of either polarity influencing the other cell.
However, the coupling between both cells does not allow fast signals to
cross between them, paralleling the previous finding that the
frequency-dependent amplification is seen solely in HS cells but not in
CH cells (Haag and Borst, 1996). Because the fine dendritic branchlets
in CH cells do not allow for electrical recording, we cannot decide at
present whether the coupling itself is slow or whether fast signals as
measured in the axon are strongly attenuated because of the
low-pass filtering by the dendrite of the cell.
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Figure 1.
Dual intracellular recordings from HS and CH
cells. a, Responses to visual motion in front of both
eyes along the PD and ND of the cells. b,
Simultaneously occurring large-amplitude EPSPs in HS and CH cells.
c, Rebound action potentials elicited in an HSE cell are
not transmitted to the dCH cell. d, Response of a dCH
cell to current injection into the ipsilateral HSE cell and vice versa.
e, Current-voltage relationship between an HSN and a
dCH cell. Current was injected into the HSN cell, and voltage response
was measured in the dCH cell.
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Figure 2.
Strength of connectivity between various pairs of
HS and CH cells. a, Location of HS and CH cell dendrites
within the lobula plate (modified from Borst and Haag, 1996).
b, Current of either +10 nA (black bars)
or  10 nA (gray bars) amplitude was injected
into HS cells, and membrane voltage was measured in the dCH cell.
c, Current was injected into the dCH cell, and membrane
voltage was measured in HS cells. Data represent the mean ± SEM
of four (HSN), five (HSE), and one (HSS) experiment.
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There exist three HS and two CH cells per lobula plate, which cover
different regions (Fig. 2a). Using again dual-electrode intracellular recording, we investigated the coupling between all
combinations of HS and CH cells. The results (Fig.
2b,c) are qualitatively identical to the
experiment described above: for all pairs, we found a bidirectional
coupling with hyperpolarizing current having larger effects than
depolarizing current. However, the absolute coupling strength depended
on the exact pair that was investigated. The influence on the dorsal
centrifugal horizontal (dCH) cell was strongest when current was
injected into the horizontal system north (HSN) cells and decreased
over HSE (horizontal system equatorial) to HSS (horizontal system
south) cells (Fig. 2b). The same held true when
current was injected into the dCH cell and the influence onto the HS
cells was considered (Fig. 2c). The opposite gradation was
observed for the coupling of vCH cells and HS cells: here the coupling
fell off from HSS over HSE to HSN cells (data not shown).
Importantly, the coupling strength between all cell pairs investigated
seemed to follow the amount of overlap between the dendrites of the
respective cells (Fig. 2a), suggesting that HS and CH cells
are connected via their dendrites.
To test this hypothesis, we used optical recording techniques (Borst
and Egelhaaf, 1992; Single and Borst, 1998). As was shown previously,
the calcium signal in HS and CH cells follows the membrane potential in
a rather linear way (Haag and Borst, 2000), thus making calcium a
feasible indicator of activity within these cells. To see whether
calcium imaging can be used to visualize connectivity, we filled one
cell with a calcium indicator and subsequently recorded from the other
cell electrically. Figure 3 shows the
results of such an experiment. Figure 3a displays the
anatomy of both cells, a dCH cell filled with the calcium sensor
Calcium Green (Molecular Probes) and an HSN cell loaded with the red
fluorescent dye Alexa 568 (Molecular Probes) for anatomical
identification. The injection of 10 nA depolarizing current into the
axon of the dCH cell resulted in a strong fluorescence increase in all
lobula plate branches (Fig. 3b), and injection of 10 nA
hyperpolarizing current led to a significant decrease in fluorescence
(Fig. 3c). When the same amount of depolarizing current was
injected into the HSN cell, fluorescence increased in the dCH cell as
well (Fig. 3d). Injection of hyperpolarizing current into
the HSN cell led to a decreased fluorescence in the dCH cell (Fig.
3e). This parallels the results reported above with dual
intracellular recording techniques and demonstrates the usefulness of
calcium imaging for connectivity analysis.
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Figure 3.
Optical imaging of connectivity between HS and CH
cells. a, Anatomy of both cells (lens, Epiplan 10×,
0.20 NA). b-e, False-color images of relative change of
fluorescence (F/F) occurring in
the dCH cell under various stimulus conditions (b,
c, direct current injection into the dCH cell;
d, e, current injection into the HSN
cell). The dCH cell was filled with Calcium Green, and the HSN cell was
filled with Alexa (lens, Zeiss UC 20×, 0.57 NA).
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To obtain information about the spatial aspects of the connectivity, we
filled a vCH cell with the calcium indicator and recorded sequentially
from two HS cells, an HSE cell and an HSS cell (Fig. 4a). When we depolarized the
vCH cell directly by current injection into the vCH cell itself, a
strong fluorescence increase was observed all over the cell, within the
lobula plate arborizations, as well as the protocerebral ramifications
(Fig. 4b). In contrast, when the depolarizing current was
injected into the HSE cell, fluorescence increased only in the upper
part of the lobula plate branches of the vCH cell (Fig. 4c).
Depolarization of the HSS cell resulted in a fluorescence signal
restricted to the lower part of the vCH cell dendrite (Fig.
4d). The strong dependence of the dendritic location of vCH
cell fluorescence change on the exact type of HS cell into which the
current was injected was further demonstrated when the fluorescence
change was spatially averaged within the areas outlined in
Figure 4, c and d, and displayed as a time course (c, d, right). These data speak in
favor of a dendro-dendritic coupling between HS and CH cells.
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Figure 4.
Dendrotopic calcium accumulation in a vCH cell.
a, Anatomy of a vCH cell filled with Calcium Green and
an HSE and an HSS cell both filled with the red fluorescent dye Alexa.
b-d, False-color images of the fluorescence change in
the vCH cell. In c and d, the outlines of
the HSE and HSS cells are superimposed in black. Also
shown are the time courses of the relative change of fluorescence
within the areas outlined in c and
d during injection of depolarizing current into the HSE
(c) and into the HSS (d)
cell (lens, Zeiss UC 20×, 0.57 NA).
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Our finding of a dendro-dendritic coupling between HS and CH cells can
explain the previous observation of retinotopic calcium accumulation in
CH cell dendrites (Egelhaaf et al., 1993), even if CH cells did not
receive direct synaptic input from local motion detectors. To
investigate the consequences of this coupling on the visually evoked
calcium signal in detail, we optically recorded simultaneously from HS
and CH cells using two different calcium indicators, a short-wavelength
dye (Calcium Green) in the CH cell and a long-wavelength dye (Calcium
Orange) in the HS cell and presented a small local motion stimulus to
the fly. As can be seen in Figure 5, the
calcium signal in the CH cell was still local and comprised only a
fraction of the area of overlap between both dendrites. However, the CH
cell calcium signal appeared spatially blurred and enlarged compared
with the signal in the HS cell dendrite (Fig. 5c, compare
top and bottom rows). A quantitative evaluation of the data obtained in this and two other experiments revealed that,
given a threshold of 50% of the maximum calcium signal, the dendritic
area in HS cells activated by the local motion stimulus comprised only
8.7 ± 1.8% (SEM) of the area activated simultaneously in CH cell
dendrites. As a control, we also switched the dyes injecting Calcium
Orange in a CH cell and Calcium Green in an HS cell. The result was
again that the activated area in CH cells was substantially larger than
the one in HS cells.
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Figure 5.
Small local motion stimuli lead to locally
confined dendritic activity in both HS and CH cells. a,
b, Raw fluorescence images showing the anatomy of the
cells tested. The vCH cell was filled with Calcium Green, and the HSS
cell was filled with Calcium Orange. c, False-color
images of the relative fluorescence change in both cells after
local visual motion stimulation (12° × 12°). A Zeiss Epiplan 10×,
0.20 NA lens was used in the photographs of a, and a
Zeiss Epiplan 40×, 0.75 NA water immersion lens was used for the
images in b and c. Color scale identical
to Figure 3.
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To discriminate between a chemical and an electrical coupling of HS and
CH cells, we tried to block the effect of current injection into HS
cells onto the calcium signal in CH cells. In brief, blocking agents of
the nicotinic pathways, such as curare (n = 1),
mecamylamine (n = 2), and  -bungarotoxin
(n = 1), all of which were effective in
vitro (Brotz and Borst, 1996) and also eliminated the visual
response in HS cells in our in vivo experiments, failed to
disrupt the influence of HS current injection on CH cell potential
(data not shown). However, the gap junction blocker Carbenoxolone (Wong
et al., 1998) [2 µl of 10 mM Carbenoxolone disodium salt (Sigma) in fly hemolymph] completely blocked the influence of HS current injection onto CH cells in three of three different experiments on various cell pair combinations of HS and CH
cells. Although we cannot exclude other possible neurotransmitters at
the moment, we conclude that the connection between HS and CH cells is
not based on chemical transmission but rather through electrical
synapses of the gap junction type. However, we never observed any kind
of dye coupling between HS and CH cells, even when using small
fluorescent probes such as calcein (Molecular Probes).
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DISCUSSION |
The above results show that CH cells receive synaptic input on the
ipsilateral side from HS cells via dendro-dendritic electrical synapses. This particular kind of wiring between the dendrites of HS
and CH cells has interesting implications for a couple of previous
findings, which will be discussed in the following.
First of all, trying to fit passive and active membrane parameters of
compartmental models from faithfully reconstructed CH cells to a large
body of experimental data only led to unsatisfying results (Haag et
al., 1999). In particular, the experimentally determined spatial
integration properties of CH cells revealed a much stronger saturation
characteristic than was predicted from simulations based on estimates
of their dendritic membrane resistance. In the simulations, however, it
was assumed that CH cells received direct and exclusive synaptic input
from retinotopically arranged local motion detectors. As the above
results demonstrate, this assumption turned out to be wrong. Our
current modeling efforts on CH cells will show whether incorporating
the new findings about the HS-CH cell connectivity will eventually be
able to resolve these previous inconsistencies.
Another puzzle applied to dendritic calcium measurements in other LPTCs
and the finding of chemical output synapses in the dendrite of CH
cells. As was shown in VS cells, preferred as well as null direction
motion elicited a rise in dendritic calcium (Borst and Single, 2000;
Single and Borst, 2002). This finding was explained by the low
direction selectivity of the excitatory input, which presumably acts on
LPTCs dendrites via calcium-permeable nicotinic acetylcholine receptors
(Brotz and Borst, 1996; Oertner et al., 2001). If CH cells received the
same kind of input from local motion-sensitive elements as VS cells,
their dendritic transmitter release would substantially loose
directionality, a problem that may have been overcome by coupling CH
cell dendrites electrically to HS cells. Consistent with this kind of
connectivity, CH cells indeed do not show an increase but rather a
decrease in dendritic calcium during null direction motion (Single,
1998), as if the visually induced dendritic calcium concentration
followed the membrane potential solely dictated by a voltage-activated
calcium current (Haag and Borst, 2000).
An important aspect of the dendro-dendritic HS-CH cell coupling might
relate to the spatial blur of motion information in the CH cell
dendrite compared with the HS cell dendrite. CH cells have been implied
to be inhibitory onto a class of LPTCs selectively sensitive to
small-field or relative motion (Egelhaaf, 1985b; Gauck and Borst, 1999;
Kimmerle and Egelhaaf, 2000b). When CH cells were laser ablated,
small-field selective cells lost much of their response selectivity,
now responding stronger to a large-field stimulus than to a small
moving object (Warzecha et al., 1993). Assuming that these cells
receive a motion image like HS cells on their dendrite,
dendro-dendritic inhibition by CH cells would be analogous to
subtracting a blurred image from an original one, resulting in an
enhancement of motion discontinuities. In case of homogeneous
large-field motion input, this operation would result in a rather
complete cancellation of the excitatory by the inhibitory input,
whereas relative motion cues, such as occurring by either object motion
or by self motion in a three-dimensional environment, would lead to an
contrast enhancement at the motion edges, just like conventional
high-pass filtering in image processing. However, whether the
sensitivity of small-field-selective neurons in the fly lobula plate
indeed relies critically on the blurring of motion input in the CH cell
dendrite remains to be validated in future experiments.
Beside the functional implications of the dendro-dendritic coupling
between HS and CH cells for the response properties of CH cells, the
above experiments also demonstrate that, in HS cells of the fly visual
system, the dendrites act in different ways depending on what output
neuron is considered: whereas for the neuron postsynaptic to the axon
terminal all positional information is lost after spatial integration,
the partner cell postsynaptic to the dendrite receives spatially
resolved signals corresponding to the location of where in visual
space motion stimuli are occurring. The present data, thus, add a new
level of complexity to the processing capabilities of single nerve
cells (for review, see Hausser et al., 2000; Segev and London, 2000),
showing that, at least in the case considered here, the function of the
dendrite of a neuron cannot be described in isolation but rather
depends on which postsynaptic partner cell is being considered.
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FOOTNOTES |
Received Nov. 5, 2001; revised Jan. 16, 2002; accepted Feb. 4, 2002.
This work was supported by National Institutes of Health Grant
1RO1MH61598- 01 to A.B. We are grateful to Dr. Dierk Reiff for
discussions and carefully reading this manuscript.
Correspondence should be addressed to Alexander Borst at his present
address: Max-Planck-Institute of Neurobiology, Department of Systems
and Computational Neurobiology, Am Klopferspitz 18a, D-82152
Martinsried, Germany. E-mail: borst{at}neuro.mpg.de.
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