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First published online November 1, 2006
Journal of Experimental Biology 209, 4464-4474 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02560
A motion-sensitive neurone responds to signals from the two visual systems of the blowfly, the compound eyes and ocelli
1 Department of Zoology, University of Cambridge, Downing Street, Cambridge,
CB2 3EJ, UK
2 Department of Bioengineering, Imperial College London, South Kensington
Campus, London, SW7 2AZ, UK
* Author for correspondence (e-mail: mmp26{at}cam.ac.uk)
Accepted 25 September 2006
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Summary |
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Key words: ocelli, compound eye, vision, tangential cell, LPTC, blowfly, Calliphora, invertebrate, multisensory integration, electrophysiology, neural processing
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Sherman and Dickinson,
2003).
Each modality has inherent, unavoidable physical or neural limitations that
restrict its effectiveness as the sole sensor for a particular type of
in-flight stimulus (Hengstenberg,
1993; Keil, 1997;
Krapp and Hengstenberg, 1996;
Nalbach, 1993). Complementary
sensory modalities can be very important, to cover a large dynamic range and
therefore provide adequate information on flight perturbations. For instance,
in the fly visual system, self-rotations are estimated by integrating the
outputs of many elementary motion detectors (EMDs). EMDs receive their inputs
from the compound eye and locally analyse directional motion. However, because
an EMD, or Reichardt Correlator (Haag et
al., 2004; Reichardt,
1987), is a delaybased directionally selective mechanism, it
requires extra processing time, and this limits self-motion estimation to a
range of comparatively low angular velocities. To maintain flight and gaze
stability in the higher angular velocity range, flies make use of information
from other sensory systems including mechanoreceptors on the halteres
(Fraenkel and Pringle, 1938;
Nalbach, 1993;
Nalbach and Hengstenberg,
1994) and the wings
(Fayyazuddin and Dickinson,
1999; Heide, 1974),
and the photoreceptor-based ocelli.
The ocelli (simple eyes) of the fly are a set of three small single-lens
eyes which, by their construction, are well adapted to the task of rotation
detection in the manner of an artificial horizon
(Schuppe and Hengstenberg,
1993; Stange et al.,
2002; Taylor,
1981a; Taylor,
1981b; Wilson,
1978a). By having a retina
that is attached to the rear surface of the lens, the images at the level of
the photoreceptors are highly blurred, i.e. they are composed only of very low
spatial frequencies. It is believed that the ocelli do not make use of the
remaining image structure and are only concerned with integrating light over
their entire visual fields. Only for the dragonfly median ocellus is there
evidence that the ocelli utilise image structure
(Stange et al., 2002), based
partially on anatomical adaptations of the ocellus - an enlarged, astigmatic
lens and an effective `lens hood', which are not present in flies. The ocelli
are very effective rotation detectors, crucial to proper gaze and flight
stabilisation in dragonflies (Stange,
1981; Stange and Howard,
1979) as well as in locusts
(Taylor, 1981a;
Taylor, 1981b). Ocellar
contributions to gaze stabilisation have also been shown in the fly
(Schuppe and Hengstenberg,
1993).
The neural processing required for an ocellar-based rotation detector is
relatively simple, at least compared to the processing required for the
directional motion analysis of compound eye inputs. Ocellar second-order
interneurones (L-neurones) integrate the outputs of photoreceptors and code
light intensity information as graded potentials
(Simmons, 1999;
Simmons et al., 1994;
Wilson, 1978b). Although the
neural mechanism by which ocellar rotation detection is implemented is
unknown, one possible means of investigating this would be to directly compare
the outputs of L-neurones. L-neurones also have some of the largest diameter
axons in the fly nervous system
(Nãssel and Hagberg,
1985; Simmons et al.,
1994), which allow for fast signal propagation. It is these
functional adaptations of the ocellar system that facilitate fast motor
responses; in the locust, the ocelli are known to elicit compensatory head
movements twice as fast as the compound eyes
(Taylor, 1981a). However,
although a rapid response is desirable, motor responses elicited by the ocelli
may in general be quite jerky in comparison to those mediated by the compound
eyes, as has been observed in dragonfly
(Taylor, 1981a). The
integration of compound eye and ocellar outputs can realize a visual detection
of rotations that combines high speed with high precision. How and where does
such integration occur in the nervous system of the fly?
As mentioned above, the fly visual system contains a class of interneurones
that are matched filters for particular selfmotions
(Krapp, 2000;
Krapp et al., 1998). In the
third visual neuropile of each half of the brain there are about 50 lobula
plate tangential cells (LPTCs). Many of them make direct synaptic connections
with descending neurones, which then convey sensory information to the various
motor systems. The neuroanatomy of ocellar L-neurones is also suggestive of
synapses with both LPTCs and descending neurones
(Strausfeld, 1976;
Strausfeld and Bassemir,
1985). Intracellular staining has shown that the terminal
arborisations of ocellar L-neurones and some VS neurones overlap with the
dendritic fields of descending neurones. It is known that descending neurones
respond to stimuli of different modalities
(Strausfeld and Gronenberg,
1990) but that the responses are quite complex, and this
complicates the electrophysiological analysis of multi-modal convergence. To
fully characterise the interactions of multiple modalities at a neuronal
level, it is necessary to be able to deconvolve the mixed responses of
individual cells.
Here we show that the activity of the well-studied tangential cell V1 (e.g.
Hausen, 1993) is driven by
illumination of the lateral ocelli. V1 was previously thought to be dedicated
solely to processing visual information from the compound eyes. Our results
suggest that V1 encodes a single, self-motion-related variable that is
independently sensed by two separate sensory systems, the compound eyes and
the ocelli. This discovery raises the possibility of a quantitative study of
the interactions between signals from the ocelli and the compound eyes by
monitoring the response of the identified V1 cell.
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Materials and methods |
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The legs, wings and proboscis of the fly were removed, and the wounds waxed
shut. The fly was mounted on a custom-built copper/plastic holder. The head of
the fly was aligned with the horizontal and vertical planes by using the deep
pseudopupil (Franceschini,
1975). The thorax and abdomen were bent ventrally by approximately
20° to gain access to the rear of the head capsule. The cuticle of the
right rear head capsule was cut open and the air sacs were moved aside to
expose the lobula plate (Fig.
1). A silver wire reference electrode was inserted into a small
hole in the left rear head capsule.
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Stimulus
Stimuli to the lateral ocelli were delivered via a pair of 62.5
µm diameter glass optical fibres, such that the light output of each fibre
covered only the lens of one ocellus (ocellar diameter 
100 µm) plus a
minimum area of cuticle surrounding it
(Fig. 1A). The fibres were
connected to a pair of blue LEDs, the intensity of which was controlled by the
analogue outputs of a data acquisition card (NI-6025E) at an update-rate of 5
kHz. The wavelength of the LEDs (
max=470 nm) was
sufficiently well matched to the absorption spectrum of the ocellar
photoreceptor pigment (Kirschfeld et al.,
1988) and was identical to that used in a previous study of fly
L-neurone responses to light stimulus
(Simmons et al., 1994). The
output intensities of the fibres were calibrated and normalised with each
other using a photoresistor.
The maximum intensity deliverable by our optical fibres was defined as Imax, and we chose our stimulus parameter to be intensity difference, where LED intensity difference, DI=(Left LED output-Right LED output). Our ocellar stimuli could therefore vary from Imax (maximum intensity at the left ocellus, zero at the right) to -Imax (maximum intensity at the right ocellus, zero at the left).
We used a CRT monitor to present pattern motion stimuli to the compound eyes. The monitor was driven by a dedicated visual stimulus card (Cambridge Research Systems 2/5), which operated at a refresh rate of 180 Hz. Compound eye stimuli consisted of a horizontal grating moving vertically downwards. The spatial intensity distribution of the grating was sinusoidal. To adjust the strength of the stimuli, we adjusted the contrast of the grating, rather than the velocity. In this way, the ocelli would see no overall change in brightness during compound eye stimulation. The grating was moved at a fixed contrast frequency of 5 Hz, with a spatial wavelength of 8°, across a display window of approximately 90° azimuth by 70° elevation.
Recordings
We recorded extracellularly from V1 using tungsten electrodes
(manufacturer: FHC) with an input resistance of 3±0.6 M
. The
extracellular neuronal signal was band-pass filtered (0.3-5 kHz), amplified,
and then sampled by a data acquisition card (AM Systems 1700 differential AC
and National Instruments 6025E, respectively) at a sample rate of 40 kHz onto
the hard-drive of a computer running Windows XP.
Cell identification and receptive field characteristics
In order to identify V1 recordings, the centre of the CRT was positioned at
an azimuth of -45° and an elevation of 0° (grey area in
Fig. 2) relative to the
reference frame of the fly head capsule, where 0° azimuth, 0°
elevation means the point directly in front of the fly. In this region of its
receptive field, V1 is most strongly excited/inhibited by downward/upward
motion (Krapp et al., 2001)
(Fig. 2). V1 can be easily
distinguished from the other spiking LPTCs sensitive to vertical motion in the
equatorial visual field, i.e. V2 and Vx. V2 is excited by pattern motion in
the opposite direction (upwards), and Vx in this area responds, but is much
less sensitive to, vertical downward motion
(Krapp, 1995)
|
):
 | (1) |
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(t), a train of N spikes as represented by a sum of delta
functions at times ti, with g(x), a
Gaussian with full-width at half-maximum (FWHM) of 2.35
.
R(t) was then normalised so that the integral of the entire
function was equal to the total number of spikes comprising the original spike
train:
 | (2) |
R(t) is referred to in the rest of the text as instantaneous firing rate. The FWHM of our smoothing function was always set as 5 ms. Errors on averaged data are always given as standard error of the mean (±1 s.e.m.) and are shown as white or shaded areas around the averaged data. Fits to the data in the last figure were obtained using the Matlab Data Fitting Toolbox, using a smoothing spline.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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To confirm that this effect is ocellar-mediated, we performed two control experiments. It was possible, though unlikely, that the unshielded compound eyes could see LED light reflected from surrounding objects, and that this was changing the spike rate in V1. We eliminated this possibility by moving the light guides from their positions above the lateral ocelli to a nearby piece of opaque cuticle, and then repeating the experiment. This extinguished the response of V1 to the LED stimuli. We were also able to discount the other possible explanation for the effect, i.e. that light was transmitted through the ocelli, the transparent tissue of the brain, and into the compound eye photoreceptors. We left the light guides in their positions above the lateral ocelli, and then cauterised the ocellar nerve by passing current through a small wire loop (see Materials and methods). The response of V1 to changes in illumination of the lateral ocelli was again extinguished (Fig. 3C). These controls demonstrate that V1 is driven by the ocelli.
Finally, to make sure that V1 had not been damaged during cauterisation, we tested the cell's response to directional motion stimuli displayed to the compound eyes before and after cauterisation. We found that the response of V1 to a moving grating (Fig. 3E, time course of grating contrast) after cauterisation (Fig. 3F) was very similar to the response before (Fig. 3D); the datasets prior to and after cauterisation lie within each other's error bounds (cf. coloured lines in Fig. 3D,F). These results show that cauterising the ocellar nerve did not impair the spiking activity of V1.
V1 spikes are phase-locked to ocellar stimuli
Using the same stimulus procedure as described above
(Fig. 3), we repetitively
stimulated the ocelli with trains of step changes in light intensity, and
calculated instantaneous firing rate (see Materials and methods) and spike
time histograms. Repetitions of the stimulus trains were separated by 2.5 s
intervals. In these experiments, V1 displayed marked phase-locking of spikes,
along with clear periods of complete inhibition
(Fig. 4A,B). The highest
temporal coherence was only seen for the first spike following excitatory
stimuli, hence the vertical lines seen in the spike raster plot
(Fig. 4B). At the stimulus
frequency shown here (10 Hz) the temporal coherence of the phase-locked spikes
slightly decayed with each stimulus cycle (cf.
Fig. 4A, peaks of the grey top
trace). The standard deviation of the spike position, or `spike jitter', for
this cell was 0.3 ms for the 1st cycle, decaying to 3 ms for the 15th cycle.
The mean for the 1st and 15th stimulus cycle of 10 animals was 4 ms and
11 ms, respectively. The decay in temporal coherence appears to halt
after 500 ms of stimulation (Fig.
4A).
|
), and
this should be reflected in the responses of downstream neurones. We recorded
the activity of V1 in response to light intensity steps and to sinusoidal
changes in light intensity, for the purpose of qualitative comparison to
L-neurone responses. As before, stimuli were applied in near darkness.
For excitatory stimuli, both step (Fig.
5B) and sinusoidal (Fig.
5D) excitatory stimuli elicited the characteristic phasic-tonic
response shape of L-neurone responses to changes in light intensity
(Fig. 5A,C). For inhibitory
stimuli, any phasic inhibition of V1 was masked by the low spontaneous spike
rate of the cell. The peak instantaneous firing rate during the sinusoidal
stimulus (Fig. 5C) was
considerably smaller than that elicited by the step stimulus. This observation
suggests that, as in ocellar L-neurones, the peak response was related to the
rate of change of light intensity at the ocelli
(Simmons et al., 1994), which
in turn was closely related to the velocity of head rotation.
|
). The latency of the first spike, given by the time
difference between stimulus onset and the peak in the instantaneous firing
rate, had a median of 16 ms. In two recordings, however, the latencies
were markedly increased to 28 ms. The V1 cells studied in these two
experiments also differed from the other V1 cells in that they showed
particularly low spontaneous activities. On a graph of latency versus
spontaneous rate (Fig. 6C)
these two points appear at the top left. This graph suggests that the latency
of ocellar drive to V1 is in some way dependent on the present activity of the
cell. To assess the validity of this, we measured the peak latency again,
except this time the rate of V1 was raised by means of compound eye
stimulation (moving grating; see Fig.
3 and Materials and methods) during ocellar stimulation. By
raising the spike rate of V1 to >250 spikes s-1 in five cells,
we found that the peak latency was reduced by an average of 4 ms, from 16 ms
to 12 ms. These reduced latencies are shown in
Fig. 6C as blue crosses.
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V1's ocellar response increases with the rate of change of light intensity
After we found that V1 responds better to sudden steps than to more gradual
sinusoids we measured the relationship between V1's peak response and the rate
of change of light intensity in the two lateral ocelli. As in our previous
experiments (e.g. Fig. 3B) we
used stimuli where any change in light intensity in one ocellus was
accompanied by an equal and opposite change in the other ocellus. The
intensity of this symmetrical stimulus can be described as the difference
between the intensities in the left and the right ocellus,
DI=(IL-IR) and DI
ranges from -Imax to Imax, where
Imax corresponds to the maximum intensity of each of the
two matched LEDs. When DI is ramped at a constant rate from
Imax in one ocellus to Imax in the
other, the rate of change of DI is
2Imax/t, where t is the time it takes to
complete the ramp. We recorded the response of V1 for stimuli that first
ramped up and then ramped down at an equal (but opposite) rate
(Fig. 7A). The ramp up
corresponds to a clockwise roll (IL is increasing) and the
ramp down to an anticlockwise roll, consequently V1 is first excited by this
stimulus and then inhibited (Fig.
7A). The instantaneous firing rates and spike time histograms were
determined for stimuli that changed at a number of different rates. The
response to each stimulus was defined as the relative modulation,
Rmod:
 | (3) |
|
The relationship between Rmod and the rate of change of stimulus intensity is shown in Fig. 7B. We normalised the data by assuming that the largest response was generated using a step stimulus, and scaling the data between this and the zero response value of Rmod. The zero response point was set by calculating Rmod for data recorded where no stimulus was presented. The response rises in proportion to the rate of change of intensity in the range 0-50 Imax s-1, and tends to saturate for higher values. The observation that a steeper slope elicits a stronger response modulation is to be expected, since a steeper slope implies a faster rotation of the head.
V1's response to ocellar stimulation is robust
How does V1 respond to excitation by both the ocelli and compound eyes, and
is the ocellar input robust enough to be detected in the presence of powerful
inputs from the compound eye? By stimulating the lateral ocelli while
presenting a moving grating to the compound eye, we studied the time course
and amplitude of the ocellar-mediated response over the full range of activity
levels in V1. As before, the ocellar stimulus consisted of a train of step
changes in intensity designed to mimic successive clockwise and anticlockwise
roll rotations (cf. Fig. 8B,
stimulus trace). For compound eye stimulation we presented a moving sinusoidal
grating, whose contrast was varied to change the spike rate of V1
(Fig. 8C). The combination of
ocellar and compound eye stimuli elicited the responses shown in
Fig. 8A. The small peaks of
ocellarmediated responses are visible even at the highest spiking rates of V1
(300 spikes s-1). The response to ocellar stimuli is therefore
robust enough to be observed at all levels of V1's response range. The spike
raster plots (Fig. 8D) show
that the temporal coherence of ocellar-induced spikes was increased by raising
V1's spike rate, and as mentioned above, is accompanied by a reduction in
response latency. In the experiment shown in
Fig. 8 the peak-response
latency to the ocellar stimuli was reduced from approximately 18 ms to 13
ms.
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70 spikes s-1, and the magnitude of the ocellar
response tails-off slowly as the spike rate is further increased.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The
neurone's response increases with the rate at which light intensity changes at
the ocelli (Fig. 7), implying
that V1 might be able to code the angular velocity of the rotations sensed by
the ocelli.
Methodological limitations
Since the primary objective was to test whether the ocelli have any impact
on LPTC activity, we did not set up our ocellar stimuli for an exhaustive
analysis. We only stimulated the lateral ocelli and this limited the rotations
mimicked by our stimuli to the anterior-posterior axis. Under normal
conditions during a rotation about this axis, the frontal ocellus would also
be constantly illuminated. Nonetheless, the qualitative demonstration of the
interactions between the ocellar and compound eye visual systems we present
here is convincing. Our aim in future experiments is to stimulate all three
ocelli and quantify the integration of more realistic inputs from the two
visual systems.
Integrating inputs from compound eyes and ocelli
Though the visual system of the fly is among the best studied of all insect
model systems, there is little previous evidence for the integration of
compound eye and ocellar-mediated information in the optic lobes. Milde
recorded the responses to ocellar and visual stimuli of several types of
neurones in the protocerebrum of the honeybee
(Milde, 1986;
Milde, 1988). Both third-order
ocellar neurones and interneurones originating in the lobula or medulla of the
bee were found to respond to ocellar and compound eye stimulation, but in a
somewhat erratic way. Consequently, the responses of these neurones were not
fully characterised. In the locust, Simmons found that the descending
contralateral movement detector (DCMD), a well-characterised visual
interneurone thought to be involved in looming detection, responds to changes
in light intensity at the median ocellus
(Simmons, 1981). Simmons
concluded that the function of ocellar input to the DCMD is to transiently
boost the response of the cell to compound eye input when ocellar light levels
suddenly decrease.
The situation in the blowfly lobula plate is more clear-cut. We already
know that V1 is tuned to respond to the optic flow that is generated in the
compound eye by rotation about a specific horizontal axis
(Krapp et al., 2001), and we
have discovered here that it also responds to ocellar stimuli that mimic
similar rotations. We can now build on the knowledge that V1 encodes visual
information in a simple, explicable way to investigate two related sets of
problems. We can investigate ocellar function by monitoring V1 activity
induced by the ocelli, and we can study multisensory integration by measuring
how this identified neurone integrates rotation-related signals from two
different sets of sensors.
Ocellar-mediated motor responses
How important are the ocelli for gaze and flight stabilisation? Arguably
the most complete picture so far is evident in locusts. Locust L-neurones were
shown to have a fairly direct route, via descending neurones, to the
flight motor system (Simmons,
2002) and are demonstrably important for flight steering
(Taylor, 1981a;
Taylor, 1981b). In
dragonflies, there is strong behavioural evidence that similar pathways exist
between ocellar neurones and neck muscles
(Stange, 1981;
Stange and Howard, 1979). The
morphology of third-order ocellar neurones in the cockroach is similar to
those in locusts, suggesting an analogous function
(Mizunami, 1995a;
Mizunami, 1995b).
In the blowfly, behavioural experiments investigating the phasic dorsal
light response, which is mediated by the ocelli, showed only small amplitude
compensatory head roll movements (Schuppe
and Hengstenberg, 1993) in response to differential illumination
of the lateral ocelli. The light level in these experiments, however, was only
changed in one ocellus, while the other two were occluded. The same
experimental paradigm was used in experiments to obtain the angular velocity
dependence of compensatory head roll movements
(Hengstenberg, 1988) for
compound eye-mediated reflexes. It was found that the response to directional
motion mediated by the compound eye was maximal at 70°
s-1, but that the dorsal light response, which also involves the
ocelli, extended with high gain up to angular velocities of 500°
s-1. The conclusion of this behavioural work was that the ocelli
act in conjunction with the compound eyes and mechanosensory halteres to
detect and monitor self-rotations. The sensitivity of the ocellar system to
changes in attitude during flight lies within an angular velocity range in
between that of the compound eyes and the mechanosensory halteres
(Hengstenberg, 1993). Our
recordings from V1 show that the LPTCs could play an important role in
combining information from ocelli and compound eyes, supplying descending
neurones and motor neurones with appropriate signals for attitude control.
What neural pathway conveys ocellar information to V1?
It is likely that a fast neural circuit connects the ocelli to V1, because
the short response delays (10-20 ms) seen in our experiments exclude
neuromodulatory effects. Because of the limitations of extracellular
recordings, we were not able to identify synaptic inputs to V1, but there is
circumstantial evidence for an interesting pattern of neuronal connectivity.
During the course of the ocellar-V1 experiments, several recordings were also
obtained from V2, another heterolateral LPTC
(Hausen, 1993). Like V1, this
cell also codes for selfrotation about a horizontal axis but, unlike V1, it
did not respond to stimulation of the lateral ocelli. This difference may be
explained by examining the function and morphology of the two cells. V1 and V2
are similar in that both cells send an axon from their dendritic input regions
to the lobula plate on the opposite side of the brain, where telodendritic
output arborisations are formed (Hausen,
1993; Krapp et al.,
2001; Kurtz et al.,
2001; Warzecha et al.,
2003). V2, however, most likely receives direct retinotopic input
from the compound eyes (Krapp,
1995), whereas V1 integrates the outputs of another set of LPTCs,
the VS cells (primarily VS1-3) (Kurtz et
al., 2001). It is possible then, that the reason we see
ocellar-mediated activity changes in V1 but not in V2, is that the ocelli
drive VS cells 1-3, which are presynaptic to V1. The connection between the
ocellar system and the VS cells could be either directly from ocellar
L-neurones, or via descending neurones, which, through electrical
synapses, influence the membrane potential of VS1-VS3
(Strausfeld and Bassemir,
1985). Recent work on the VS-V1 synapse would seem to support the
L-neurone-VS-V1 route. The relationship between presynaptic (VS-cell) membrane
potential and postsynaptic (V1) spike rate is almost linear
(Kurtz et al., 2001;
Warzecha et al., 2003), but
only above a certain level of pre-synaptic depolarisation. This fits with the
observation (Fig. 8B,C) that
the largest responses to ocellar inputs were observed when the activity level
of V1 was raised slightly above baseline by compound eye stimulation. In any
case, to identify the pathway mediating ocellar-induced activity changes in V1
further experiments are required, ideally monitoring the ocellar nerve
activity while recording intracellularly and extracellularly from VS cells and
V1, respectively.
Why convey sensory information from the ocelli to the lobula plate?
Because the VS tangential cells are matched filters for selfrotation, they
are ideal targets for inputs from ocellar L-neurones. By integrating the
appropriate combination of ocellar L-neurone outputs, each tangential cell
could include ocellar-mediated information on rotations in a way that matches
its preferred rotation axis. Our data suggest that this may be the case for
the V1 cell, and thus for the inputting VS-cells, because the ocellarmediated
input to V1 conveys information about turns that is compatible with the
neurone's preferred axis of rotation.
The compound eye stimulus that most strongly activates V1 corresponds to
the optic flow generated by a rotation of the fly about a horizontal axis
intermediate between pitch and roll (Fig.
2). For the roll component this is a clockwise rotation that
decreases the light level in the right ocellus and increases it in the left
ocellus. Mimicking such an illumination pattern increased the V1 spiking
activity whereas the opposite pattern of illumination resulted in a reduced
spike rate. The integration of ocellar inputs at the level of LPTCs could very
well be advantageous in the context of sensorimotor transformation: it reduces
the need for ocellar-specific interneurones to transform information obtained
in sensory coordinates into the signals required by the motor system for
attitude control. A similar simplification of the sensorimotor transformation
has recently been suggested in the gaze stabilization system of the blowfly
(Huston, 2005; S. Huston and
H.G.K., unpublished data).
Any functional integration of ocellar information at the level of the LPTCs
would be meaningless if a major advantage of the ocellar system - its speed -
was negated. Our measurements of the latency of ocellar-mediated V1
modulations suggest that this advantage is maintained. We observed a median
(over ten cells) time-to-peak latency of 16 ms, with a minimum latency in
one cell of 10.5 ms, whereas the response latency in tangential neurones to
compound eye stimulation is about 25 ms
(Warzecha and Egelhaaf, 2000).
Our estimates of the latency will be slightly conservative in comparison with
the study mentioned in the previous sentence. This is because we looked at
peak latency, which is essentially the mean position of the first
post-stimulus spike, whereas Warzecha and Egelhaaf
(Warzecha and Egelhaaf, 2000)
based their estimates around discrimination of the neuronal signal from
background noise. The precise latency advantage of ocellar responses must be
confirmed using a single stimulus that drives both the ocelli and the compound
eye simultaneously with equivalent light intensities.
Multimodal integration in the lobula plate
The arguments presented above suggest how ocellar signals could be
integrated in the lobula plate to produce faster motor responses, by using the
VS cells as ready-tuned conduits to the motor system. There is preliminary
evidence that neurones in the fly lobula plate integrate other forms of
sensory input that are useful for controlling flight. Spiking in LPTCs can be
modulated by wind stimuli applied to the antennae, and by mechanical
stimulation of the abdomen (S. L. Maddess and S. Huston, unpublished
observations). Further investigation of these interactions, along with a
quantitative description of the integration of ocellar and compound
eye-mediated signals in V1 and VS neurones, promise considerable insight into
the neural principles of multisensory integration. Because the visual response
properties of LPTCs are exceptionally well characterised, such studies may be
able to identify some of the synergies that occur when different sensory
systems independently encode the same parameter to control a specific
behaviour and also show how these synergies are implemented in circuits
composed of identified neurones.
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Acknowledgments |
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|
References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Fayyazuddin, A. and Dickinson, M. H. (1999).
Convergent mechanosensory input structures the firing phase of a steering
motor neuron in the blowfly, Calliphora. J.
Neurophysiol. 82,1916
-1926.
Fraenkel, G. and Pringle, J. W. S. (1938). Halteres of flies as gyroskopic organs of equilibrium. Nature 141,919 -921.
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R, plotted against
the corresponding compound eye-only mediated value, at the time of each peak.
Positive y-axis values therefore indicate ocellar-mediated
excitation, whereas negative values indicate ocellar-mediated inhibition. To
obtain enough data points, both the curves shown in C (0-10% and 0-20%) were
used to stimulate the compound eyes. (F) Data from another animal (188
stimulus repetitions), presented in the same way as in E. Black lines in E and
F are interpolant smoothing splines, each obtained using the same smoothing
parameter (see Materials and methods).