|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online March 31, 2007
Journal of Experimental Biology 210, 1350-1361 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02744
Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria
1 School of Advanced Sciences, The Graduate University for Advanced Studies,
Shonan Village, Hayama, Kanagawa 240-1930, Japan
2 Department of Biology, Animal Physiology, University of Marburg, D-35032
Marburg, Germany
Author for correspondence (e-mail:
homberg{at}staff.uni-marburg.de)
Accepted 6 February 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
Key words: skylight navigation, polarization vision, insect brain, color vision, spectral opponency, Schistocerca gregaria
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
; Rossel and
Wehner, 1986; Lohmann and
Lohmann, 1996; Wiltschko and
Wiltschko, 1996; Wehner,
1997; Wehner,
2003; Dacke et al.,
2003a; Dacke et al.,
2003b; Mouritsen and Ritz,
2005). Sun compass navigation is a particularly common strategy.
In sun compass navigation, the animals adjust their navigational direction at
a certain angle to the solar azimuth, the horizontal component of the sun's
position in the sky. Celestial cues other than direct sunlight, however, are
also useful as a reference to the sun, especially when the sun is not visible
at dawn or dusk or when it is hidden behind clouds or large objects.
Scattering of sunlight in the atmosphere results in a polarization pattern, in
a spectral gradient, and in an intensity gradient along the sunlit sky.
Behavioral experiments have demonstrated that desert ants, monarch
butterflies, dung beetles and honeybees use the celestial polarization pattern
as a cue for navigation (Rossel and
Wehner, 1986; Dacke et al.,
2003a; Dacke et al.,
2003b; Wehner,
2003; Saumann et al., 2005) (but see
Stalleicken et al., 2005).
Desert ants and bees, in addition, can also navigate based on the spectral
gradient in the sky (Rossel and Wehner,
1984; Wehner,
1997).
The neuronal basis of polarized-light vision has been studied in several
insect species. Polarized light is perceived by a small dorsal rim area (DRA)
in the compound eye. Photoreceptors of the DRA show striking adaptations for
detection of polarized light: they are homochromatic, have microvilli that are
highly aligned in parallel, and often have wide receptive fields
(Labhart and Meyer, 1999;
Dacke et al., 2002;
Homberg and Paech, 2002). As a
result, photoreceptors in the DRA show high polarization sensitivity
(Labhart and Meyer, 1999;
Dacke et al., 2002;
Stalleicken et al., 2006).
Their axons project to dorsal areas in the lamina and medulla
(Blum and Labhart, 2000;
Homberg and Paech, 2002) and
provide input to polarized-light sensitive interneurons (POL neurons). POL
neurons show sinusoidal modulation of spiking activity depending on the
e-vector angle of polarized light. Various types of POL neuron have been
characterized in the optic lobe of several species
(Labhart, 1988;
Homberg and Würden, 1997;
Labhart, 2000;
Labhart et al., 2001;
Loesel and Homberg, 2001;
Pfeiffer et al., 2005). Among
these, POL-1 neurons of crickets with ramifications in the medulla have been
studied particularly well (Labhart et al.,
2001; Wehner and Labhart,
2006). Both in the field cricket and in the desert locust, POL
neurons have also been reported in the central complex
(Vitzthum et al., 2002;
Sakura and Labhart, 2005), a
brain area involved in visual memory and spatial orientation
(Strauss, 2002;
Liu et al., 2006).
Central-complex neurons have receptive fields oriented toward the zenith and
display a wide range of e-vector tunings
(Homberg, 2004;
Sakura and Labhart, 2005). In
the desert locust Schistocerca gregaria these neurons are sensitive
not only to polarized light but also to unpolarized light
(Vitzthum et al., 2002). In
contrast, the POL-1 neurons in crickets are not sensitive to unpolarized light
(Labhart, 1988). This
difference suggests that the sky navigation system of the desert locust might
be different in certain respects from that of the field cricket.
|
). It
receives input from line tangential neurons of the medulla. These neurons have
dendritic ramifications in the dorsal rim area of the medulla and axonal
projections through the anterior optic tract to the AOTu
(Homberg et al., 2003).
Recently, four types of POL neuron were identified in the AOTu of the locust
(Pfeiffer et al., 2005). Two
of them, LoTu1 (Fig. 1A) and
TuTu1, innervate the lower units of the AOTu bilaterally. Both cell types
respond to polarized light and to unpolarized light like POL neurons of the
central complex (Fig. 1B,C).
LoTu1 and TuTu1 show distinct e-vector tuning and receive polarized-light
input exclusively (LoTu1) or largely (TuTu1) via the ipsilateral eye.
Their responses to unpolarized light depend on stimulus position
(Fig. 1C). Two other types of
POL neuron in the AOTu have been studied less well. These neurons (TuLAL1a and
TuLAL1b) project to the lateral accessory lobe and provide input to POL
neurons of the central complex.
The spectral sensitivity of POL neurons in the locust is not known. In the
DRA of S. gregaria, there are blue receptors peaking at 450 nm with
high sensitivity to polarized light (polarization sensitivity, PS=6.92) and UV
receptors peaking at 320 nm with low sensitivity to polarized light (PS=2.04)
(Eggers and Gewecke, 1993). In
the rest of compound eye, there are no published data from S.
gregaria, but three types of spectral receptors were identified in
Locusta migratoria (Vishnevskaya
and Shura-Bura, 1990). These types of photoreceptor are maximally
sensitive at 360 nm (UV receptor), 430 nm (blue receptor), and 530 nm (green
receptor). Which type of spectral receptor dominates the responses of POL
neurons in the desert locust? POL neurons in crickets and desert ants are
monochromatic and tuned to the spectral sensitivity of polarized-light
sensitive photoreceptors in the DRA
(Labhart, 1988;
Labhart, 2000). Is this also
true for the locust?
In the present study, we focus on the two previously characterized bilateral POL neurons of the AOTu, LoTu1 and TuTu1. We penetrated these neurons and analyzed their spectral responses to polarized light and to unpolarized light by using a set of monochromatic filters. We show that both types of neuron are sensitive to polarized blue light. In response to unpolarized light, the spectral responses depend on stimulus position and show antagonism in the response to UV and green light. These responses might be an adaptation to the spectral gradient in the sky.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
Stimuli
Polarized and unpolarized monochromatic light were used for stimulation.
Both types of light stimuli were provided by passing the light of a 75 W xenon
lamp through a set of narrow band interference filters, neutral density
filters, and a circular neutral density wedge spanning 5 log units of
intensity. The interference filters and a shutter were controlled by a shutter
controller (Lambda 10-2, Sutter Instruments, Novato, CA, USA). The neutral
density wedge was adjusted by a custom-built control unit. Both devices were
driven by a custom-built program.
Unpolarized monochromatic light was produced by passing light through one of nine interference filters with a spectral range between 330 and 600 nm (330FS10–600FS10; LOT Oriel, Darmstadt, Germany). The maximum intensity of monochromatic light was adjusted to equal photon flux at either 16.5x1012 or 10.6x1012 photons cm–2 s–1. The intensity of the unpolarized monochromatic light was changed within a range of 3 log units with neutral density filters. Calibration of intensities was carried out with a radiometer (P-9201, Gigahertz-Optik, Puchheim, Germany). The duration of monochromatic light stimuli was either 500 ms or 1 s, separated by 1–3 s of darkness. Light passed through a UV-transmitting quartz light guide attached to a perimeter and was seen by the locust at a distance of 10 cm from the locust's head. The angular extent of the stimuli at the locust's eye was 2°. By moving the light guide along the perimeter, the light stimuli were administered from four directions: from dorsal (zenith), from frontal (elevation about 50°), and from lateral to the right or left eye at an elevation of 30–45°.
Polarized light was produced by inserting a UV transmitting polarizer (HNP'B, Polaroid, Cambridge, MA, USA) between the light guide and the animal. During stimulation, the polarizer was rotated through 360° in either direction at 20 or 21.8° s–1. We stimulated with both `white' and monochromatic polarized lights (UV, 330 nm; blue, 450 nm; green, 530 nm). The maximum intensity of each polarized monochromatic light stimulus at the surface of the locust's eye was adjusted to either 9.0x1012 or 10.6x1012 photons cm–2 s–1. The intensity of each polarized monochromatic light was changed within a range of 4 log units with neutral density filters.
Electrophysiology
After cropping legs and abdomen, locusts were fixed to a metal holder with
a wax-rosin mixture. The head capsule was opened frontally to expose the
brain. The metal holder was mounted in the center of a Faraday cage. Sharp
glass microelectrodes filled with 1 mol l–1 KCl (resistance
about 50–150 M
) and 4% Neurobiotin in 1 mol l–1
KCl (Vector Laboratories, Burlingame, CA, USA) at the tip were inserted in the
vicinity of the AOTu. After successful impalement we first stimulated with
polarized light. If the cell was polarization-sensitive, we measured the
spectral response properties to polarized light and to unpolarized light.
Action potentials were amplified with a custom-made amplifier, monitored with
an oscilloscope (Hameg HM 205–2; Hameg, Frankfurt/Main, Germany),
digitized at 25 kHz with a Digidata 1322A (Molecular Devices, Sunnyvale, CA,
USA) and stored on a personal computer using Clampex 9.2 (Molecular Devices).
After recording, the neurons were injected with Neurobiotin by administering
positive currents of 1–3 nA for 5–60 s.
Data analysis
The frequency of action potentials in the recordings was evaluated with the
threshold detection algorithm of Clampfit 9.2 (Molecular Devices). The mean
spike frequency during an interval of 1 s or 500 ms before the onset of the
light stimuli was used as background activity. Responses to polarized light
were analyzed using a procedure described previously
(Pfeiffer et al., 2005).
e-vector response plots were obtained by plotting means of spike frequencies
during consecutive 10° bins of the rotating polarizer against the bin
centers. e-vector angles eliciting maximal (
max) and minimal
(min) spike activity were determined by fitting
sin2 functions to the data sets using the nonlinear least-squares
Levenberg–Marquardt algorithm (Origin 6.0, Microcal, Northhampton, CA,
USA). To quantify the neuronal responses to polarized light stimuli, we
calculated the response value R, introduced by Labhart
(Labhart, 1996). Action
potentials were detected by a threshold function and their number was counted
in 18 consecutive bins of 20° using a custom-written semiautomatic spike2
script (Cambridge Electronic Design, Cambridge, UK). R was then
calculated as:
 | (1) |
the mean number of spikes per bin
during the 360° rotation. To compare the responses to three monochromatic
polarized lights, spiking activities at max were normalized
against the maximum response. In the intensity/response plots, spiking
activities at max were, likewise, normalized against the
maximum response. Intensity/response curves were obtained by fitting the data
with modified Naka–Rushton functions,
rA/rAmax=
In/(In+Kn), and
rR/rRmax=In/(In+Kn),
where I is stimulus intensity, rA is relative spiking
activity, rR is relative response, K is stimulus intensity
eliciting 50% rAmax, resp. rRmax, and
n is exponent (KaleidaGraph 4.0; HULINKS, Tokyo, Japan). To compare the
intensity/response curves for unpolarized and polarized light, differences
between spiking activity and background activity were used as data fit to the
Naka–Rushton function. The responses to unpolarized monochromatic light were evaluated by measuring the mean spiking rate during 1 s time intervals before the onset of the stimulus, during the stimulus and after the stimulus, using a semiautomatic script. Two-sided student's t-tests were used to determine statistical differences in the responses to different colors.
Histology
After the Neurobiotin injection, the locust was kept at room temperature
for at least 20 min to allow for diffusion of the tracer. The brain was
dissected out of the head capsule and fixed overnight at 4°C in 4%
paraformaldehyde, 0.25% glutaraldehyde, and 0.25% saturated picric acid in 0.1
mol l–1 phosphate buffer pH 7.4 (PB). Brains were
subsequently embedded in gelatin/albumin and fixed overnight in 8%
formaldehyde in PB at 4°C. Sections of 35 µm were cut with a vibrating
blade microtome (VT–1000S, Leica, Wetzlar, Germany). They were incubated
for at least 18 h at room temperature in streptavidin conjugated to
horseradish-peroxidase (Amersham Buchler, Brunswick, Germany) at a dilution of
1:200 in phosphate-buffered saline containing 0.5% Triton X-100. Sections were
stained with 3,3'-diaminobenzidine tetrahydrochloride and nickel
ammonium sulfate as described elsewhere
(Vitzthum et al., 2002).
Finally, the sections were mounted on glass microslides, dehydrated, cleared
in xylene, and embedded in Entellan (Merck, Darmstadt, Germany) under glass
coverslips. Neurons were reconstructed using a compound microscope with camera
lucida attachment. The terms ipsilateral and contralateral refer to the
position of the cell body.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
). The perikarya of both cell types lie in the inferior
lateral protocerebrum.
LoTu1
Recordings from LoTu1 confirmed our previous findings on responses to
polarized and unpolarized white light (Fig.
1) (Pfeiffer et al.,
2005). Dorsal polarized light led to tonic excitation that was
sinusoidally modulated in strength by the rotating e-vector
(Fig. 1B). Unpolarized
ipsilateral light led to an increase in spiking activity, while zenithal
dorsal stimulation led to tonic inhibition. Strong frontal illumination caused
an excitatory response or a phasic excitation followed by strong tonic
inhibition (Fig. 1C).
In the present study we analyzed the responses of LoTu1 to monochromatic
light stimuli. Dorsal polarized monochromatic light stimuli (UV, 330 nm; blue,
450 nm; green, 530 nm) at 9.0x109 photons
cm–2 s–1 were tested in seven recordings
from LoTu1. The background activity of these neurons was relatively low at
4.82±1.09 impulses s–1 (mean ± s.e.m.). The
excitatory response of LoTu1 to polarized blue light was stronger than the
response to polarized UV and green light
(Fig. 2A,B). In four
recordings, green light elicited virtually no response
(Fig. 2A), but in three other
LoTu1 cells, the response to polarized UV light was smaller than the response
to polarized green light. The mean spiking activity at max
during stimulation with polarized blue light was about two times the activity
at max when stimulating with UV light or green light
(Fig. 2B). The mean spiking
activity at max in response to polarized UV light did not
differ significantly from the response to polarized green light. The response
strength R (for definition of R, see Materials and methods)
showed the same results (Fig.
2B). Fig. 2C,D
shows the intensity/response curves from six LoTu1s (mean background activity,
8.65±1.82 impulses s–1). At the lowest light intensity
of logI=–4(10.6x108 photons
cm–2 s–1) LoTu1 did not show clear
responses. The activity at max saturated at intensities
between logI=–2 and –1.5, the response value R,
in contrast, only near logI=0. In one LoTu1, the response value
R at maximum intensity was smaller than the response strength at
logI=–3 and –2.
|
|
|
The responses of LoTu1 to unpolarized light were consistent among four to six LoTu1s (Fig. 3B). When stimulated dorsally, all LoTu1s were inhibited by blue light. In response to ipsilateral stimulation, four LoTu1s were excited by green and were inhibited by UV light as shown in Fig. 3A. One of two other recordings from LoTu1s with no background activity showed an excitatory response to green light and no response to UV light. The other LoTu1 showed weak excitatory responses to UV light and green light. When light stimuli were presented from the contralateral side, three LoTu1s were inhibited by blue light, but the mean spiking activity during stimulation was not significantly lower than background activity. During ipsilateral stimulation with a series of nine monochromatic lights, LoTu1 showed clear spectral opponency (Fig. 3C). Stimulations at short wavelengths, from 330 nm to 430 nm, inhibited the neuron, whereas stimulations at long wavelengths, from 500 nm to 550 nm, excited the neuron.
In one LoTu1 neuron, we successfully recorded the responses to polarized blue light and to unpolarized lights, adjusted to the same intensities (Fig. 4). LoTu1 (background activity 5.23 impulses s–1) started to be inhibited by unpolarized dorsal blue light at logI=–1.5 (Fig. 4B, arrow). This inhibitory response increased with increasing light intensity. The post-inhibitory rebound excitation after the stimulus also increased depending on stimulus intensity (Fig. 4B, open arrowhead). The neuron was inhibited by unpolarized ipsilateral UV light (Fig. 4B, arrowhead). In contrast to the blue-light inhibition, this inhibitory response outlasted the stimulus and led to complete inhibition by UV light above a light intensity of logI=–1 (Fig. 4B, double open arrowhead). The neuron only gradually recovered to background spiking after more than 3 s following stimulation at highest intensity. The response to ipsilateral green light became apparent at a light intensity of logI=–1.5 (Fig. 4B, double arrowhead). Comparison of the response/intensity curves for responses to unpolarized lights and to dorsal polarized light (Fig. 4C) shows that sensitivity to polarized light is already present at intensities below logI=–3. In contrast, clear responses to unpolarized light only occurred above a light intensity of logI=–1. These results show that LoTu1 is about 2.5 log units more sensitive to polarized light than to unpolarized light. The dynamic range of intensity coding for polarized and unpolarized light was very narrow and covered only about 1–1.5 log units.
TuTu1
We recorded the responses to dorsal polarized monochromatic UV, blue and
green light stimuli from three TuTu1 neurons. The mean background activity of
these neurons was 21.03±6.24 impulses s–1,
considerably higher than the activity of LoTu1. TuTu1 neurons showed
polarization-opponency in response to the rotating polarizer (see also
Pfeiffer et al., 2005). This
means that TuTu1 neurons were maximally excited at max and
were maximally inhibited at an e-vector orientation orthogonal to
max (min). The opponent response to polarized
blue light was stronger than the responses to polarized UV and polarized green
light (Fig. 5A,B). In two
neurons, the response to polarized UV light was slightly stronger than that to
polarized green light (Fig.
5A). The response strength R to polarized light was
significantly higher at 450 nm (blue) than at 350 nm (UV) or at 530 nm (green)
(Fig. 5B). In contrast, the
neural activity at max was not significantly different between
the responses to the three monochromatic polarized lights.
Fig. 5C,D shows the
intensity/response curves of three recordings from TuTu1. The neural activity
at max and the response amplitude increased with increasing
stimulus intensity. TuTu1 did not respond to polarized light at
logI=–4. At a light intensity of logI=–2, both
the activity at max and the response saturated.
|
We recorded the responses to unpolarized monochromatic lights from four TuTu1 neurons, but the responses were not consistent among the recordings. Fig. 6 shows two examples of the responses to unpolarized monochromatic lights applied to different eye regions. In Fig. 6A, TuTu1 showed spectral-opponency when light stimuli were applied from the ipsilateral direction. This TuTu1 was excited by UV light (Fig. 6A, double arrowhead) and was inhibited by green light (Fig. 6A, open arrowheads). When contralateral light stimuli were applied, the neuron showed an inhibitory response (Fig. 6A, arrow) with post-rebound excitation (Fig. 6A, open double arrowheads) to blue light. Another TuTu1 was inhibited by blue light at maximum intensity from dorsal and contralateral directions (Fig. 6B, arrows). This neuron was excited by both UV light and blue light coming from the ipsilateral side (Fig. 6B, arrowheads), but showed no clear response to green light. The third TuTu1 (not shown) was excited by UV light presented dorsally and ipsilaterally, but did not respond to blue light and green light from any directions. The last TuTu1 showed very weak responses that were similar in their properties to those of the neuron of Fig. 6A.
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
). In contrast,
both LoTu1 and TuTu1 neurons of the locust receive input from homochromatic
blue polarized-light sensitive photoreceptors (Figs
2,
5,
7), as well as from
polarization insensitive UV and green receptors (Figs
3,
4,
6,
7). Firm conclusions on the
biological significance of these wavelength-specific responses await further
studies. An attractive hypothesis, however, is that through chromatic contrast
signalling spectral gradients in the sky might contribute to sky compass
coding in these two neurons.
|
). LoTu1 and TuTu1 were most sensitive to dorsally presented
polarized blue light and showed much lower sensitivity to polarized UV and
green light (Fig. 2A,B,
Fig. 5A,B). This result is
consistent with the fact that only blue receptors in the locust DRA showed
high polarization sensitivity (Eggers and
Gewecke, 1993) and indicates that the polarized-light sensitivity
of LoTu1 and TuTu1 neurons is based on blue receptors in the DRA. The
polarization vision system of crickets, likewise, depends on blue
photoreceptors, demonstrated behaviorally, in photoreceptor recordings, and in
intracellular recordings from POL interneurons
(Labhart, 1988) (reviewed by
Labhart and Petzold, 1993). In
contrast, polarization vision in hymenopteran species (honeybee, desert ant)
relies on UV light (reviewed by Wehner and
Labhart, 2006).
The absolute sensitivity for polarized light is similar in LoTu1 and TuTu1.
The response threshold for polarized light was at a light intensity of
logI=–3.5 to –3, and saturation of the response at
max was reached at an intensity of logI=–2
(Fig. 2C,
Fig. 5C). This means that
1–1.5 log units above threshold, the responses of both POL neurons at
max are intensity independent. While the response strength
R of TuTu1 showed a similar intensity dependence
(Fig. 5D), the R value
of LoTu1 increased over 3–4 log units of light intensity and only
reached saturation around logI=0
(Fig. 2D). A likely reason for
this may be the increasing contribution of a polarization-insensitive
inhibition of LoTu1 by dorsal blue light above logI=–2, as
shown in Fig. 4C. The cricket
POL-1 neuron, in contrast, shows maximum response within 1 log unit of light
intensity (Labhart, 1988;
Labhart et al., 2001). Above a
light level of about 3x108 photons cm–2
s–1 of blue light (443 nm), its e-vector response becomes
intensity independent by receiving antagonistic input from photoreceptors with
mutually orthogonal microvilli orientation. The POL-1 neuron is, therefore, at
least 2 log units more sensitive to polarized light than the two locust
neurons studied here.
Spectral sensitivity of responses to unpolarized light
The spectral responses of the bilateral POL neurons to unpolarized light
are surprisingly complex. All three types of spectral receptors in the
compound eye contribute to the unpolarized light response. The spectral
responses are different at different stimulus positions, indicating that the
set of spectral inputs contributing to the unpolarized light responses differ
considerably depending on the eye region
(Fig. 7).
LoTu1 and one subtype of TuTu1 receive inhibitory input from blue receptors in dorsal eye regions (Fig. 3, Fig. 6). The sensitivity to dorsally presented blue light may code for brightness of the blue sky. At very high light intensities, the inhibition in LoTu1 by blue light can strongly suppress the responses to polarized light and may even become apparent when using polarized light as the stimulus.
In addition, the spectral response to unpolarized light shows opponency in
the response to UV light and green light in both bilateral POL neurons when
light was presented from the ipsilateral side
(Fig. 3,
Fig. 6). Spectral opponency is
a widespread phenomenon in color vision and has been demonstrated in neurons
of the optic lobe of the honeybee (Kien
and Menzel, 1977) and migratory locust
(Osorio, 1986). Sustaining
responses and narrow receptive fields of some green-UV color opponent neurons
of the locust medulla suggested that they might play a role in maintaining
flight posture relative to the horizon
(Osorio, 1986). Likewise, the
spectral opponency in LoTu1 and TuTu1 may not contribute to true color vision,
but may rather serve to evaluate the spectral gradient in the sky. At
positions near the sun, the chromatic contrast between long (green) and short
(UV) wavelength light is high, but becomes smaller with increasing angular
distance to the sun in the anti-solar hemisphere
(Rossel and Wehner, 1984;
Coemans et al., 1994). To
process all spectral information in the sky, an animal may code the intensity
of blue light as a reference and, at the same time, the difference of
intensities between green light and UV light. To further substantiate the
hypothesis that LoTu1 and TuTu1 neurons integrate polarization and chromatic
contrast of the sky, it will be necessary, however, to examine the azimuthal
dependence and receptive fields of the chromatic responses in more detail and
to test the combined effects of polarized and chromatic stimuli on the
responses of the neurons.
Pathway of visual inputs to LoTu1 and TuTu1
Which neurons provide input to the bilateral POL neurons? Previous
anatomical studies have shown that medulla line tangential neurons are the
most promising candidates to provide visual input from the ipsilateral eye
(Homberg et al., 2003). These
neurons have small diameter processes along the dorso-ventral axis of the
medulla – in addition to ramifications in the dorsal rim area of the
medulla – and send direct processes to the lower unit of the AOTu. This
morphology is ideally suited to integrate inputs from the DRA and the main
retina of the compound eye. In both LoTu1 and TuTu1, ramifications in the
ipsilateral AOTu are of smooth appearance and, therefore, most likely
dendritic, while arborizations in the contralateral AOTu have a beaded or
varicose appearance and are, therefore, most likely axonal
(Pfeiffer et al., 2005). These
morphologies suggest that the bilateral POL neurons receive information only
from the ipsilateral eye. In fact, LoTu1 receives polarized-light input only
through the ipsilateral eye, while polarization sensitivity in TuTu1 is
dominated by ipsilateral eye input
(Pfeiffer et al., 2005). In
addition, our present study suggests that TuTu1 at least responds to
unpolarized light perceived by both eyes. The information from the
contralateral eye may in part originate from the counterpart LoTu1 and TuTu1
neurons of the other brain hemisphere. In addition, medulla line tangential
neurons without ramifications in the DRA also project to the lower unit of
AOTu (U.H., unpublished observation). These neurons may provide selectively
unpolarized light inputs to the bilateral POL neurons in the AOTu.
Integration of unpolarized and polarized light signals in orientation
The bilateral POL neurons may be suited to integrate information on the
celestial polarization pattern and on the spectral gradient in the sky.
Polarized light information at the zenith is used for coding the orientation
of the body axis relative to the solar meridian. However, sky polarization
alone is not sufficient to signal solar azimuth unambiguously, since e-vector
orientations alone do not allow the animal to discriminate whether the sun
occurs at an azimuth 
or at an azimuth +180°. POL neurons in
the locust, as reported here, might resolve this problem by coding not only
the e-vector angle of polarized light but also the spectral gradient in the
sky. Locusts may, in addition, use intensity gradients in the sky for
orientation, but whether and how intensity information is actually integrated
in the compass orientation system remains to be seen. Behavioral experiments
in homing bees have shown that intensity gradients do not provide substantial
information for navigation (Rossel and
Wehner, 1984).
The absolute sensitivity to polarized light is about 2 log units higher than the sensitivity to unpolarized light, as shown for LoTu1 (Fig. 4C). This suggests that, depending on light intensities, polarization input or unpolarized light input may dominate the responses of the neurons. At low light intensities, before dawn and after sunset or under a partly cloudy sky, the polarization vision system may be more important for orientation behavior. However, when the sky is clear and the sun is directly visible, sky chromatic contrast may prevail and provide the relevant information for orientation.
This study is the first to address the possibility that both e-vector angle
of polarized light and the spectral gradient in the sky are encoded in the
same neural system underlying compass orientation in an insect. Our results
support behavioral data indicating that celestial compass orientation in bees
and desert ants relies on both the celestial polarized-light pattern and the
spectral gradient in the sky (Wehner,
1989). Observations in bees, ants, and pigeons suggest that these
animals evaluate the intensity of long wavelength light with respect to the
relatively isotropic UV background for sun compass navigation
(Rossel and Wehner, 1984;
Coemans et al., 1994;
Wehner, 2003). Our findings of
spectral opponency in the responses to unpolarized light fit these behavioral
observations well and may be a first step in understanding how the integration
of different celestial cues used for spatial orientation is organized in the
brain.
|
List of symbols and abbreviations |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
max, min
|
Acknowledgments |
|---|
|
Footnotes |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
|---|
Blum, M. and Labhart, T. (2000). Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J. Comp. Physiol. A 186,119 -128.[CrossRef][Medline]
Coemans, M. A. J. M., Vos Hzn, J. J. and Nuboer, J. F. W. (1994). The relation between celestial colour gradients and the position of the sun, with regard to the sun compass. Vision Res. 34,1461 -1470.[CrossRef][Medline]
Dacke, M., Nordström, P., Scholtz, C. H. and Warrant, E. J. (2002). A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum.J. Comp. Physiol. A 188,211 -216.[CrossRef][Medline]
Dacke, M., Nordström, P. and Scholtz, C.
(2003a). Twilight orientation to polarised light in the
crepuscular dung beetle Scarabaeus zambesianus. J. Exp.
Biol. 206,1535
-1543.
Dacke, M., Nilsson, D. E., Scholtz, C. H., Byrne, M. and Warrant, E. J. (2003b). Animal behaviour: insect orientation to polarized moonlight. Nature 424, 33.[Medline]
Eggers, A. and Gewecke, M. (1993). The dorsal rim area of the compound eye and polarization vision in the desert locust (Schistocerca gregaria). In Sensory Systems of Arthropods (ed. K. Wiese, F. G. Gribakin, A. V. Popov and G. Renninger), pp. 101-109. Basel: Birkhäuser.
Homberg, U. (2004). In search of the sky compass in the insect brain. Naturwissenschaften 91,199 -208.[CrossRef][Medline]
Homberg, U. and Paech, A. (2002). Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct. Dev. 30,271 -280.[CrossRef]
Homberg, U. and Würden, S. (1997). Movement-sensitive, polarization-sensitive, and light-sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria.J. Comp. Neurol. 386,329 -346.[CrossRef][Medline]
Homberg, U., Hofer, S., Pfeiffer, K. and Gebhardt, S. (2003). Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J. Comp. Neurol. 462,415 -430.[CrossRef][Medline]
Kien, J. and Menzel, R. (1977). Chromatic properties of interneurons in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J. Comp. Physiol. 113, 35-53.
Labhart, T. (1988). Polarization-opponent interneurons in the insect visual system. Nature 331,435 -437.[CrossRef]
Labhart, T. (1996). How polarization-sensitive interneurones of crickets perform at low degrees of polarization. J. Exp. Biol. 199,1467 -1475.[Abstract]
Labhart, T. (2000). Polarization-sensitive interneurons in the optic lobe of the desert ant Cataglyphis bicolor.Naturwissenschaften 87,133 -136.[CrossRef][Medline]
Labhart, T. and Meyer, E. P. (1999). Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc. Res. Tech. 47,368 -379.[CrossRef][Medline]
Labhart, T. and Petzold, J. (1993). Processing of polarized light information in the visual system of crickets. In Sensory Systems of Arthropods (ed. K. Wiese, F. G. Gribakin, A. V. Popov and G. Renninger), pp. 158-169. Basel: Birkhäuser.
Labhart, T., Petzold, J. and Helbling, H. (2001). Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J. Exp. Biol. 204,2423 -2430.[Medline]
Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., Heisenberg, M. and Liu, L. (2006). Distinct memory traces for two visual features in the Drosophila brain. Nature 439,551 -556.[CrossRef][Medline]
Loesel, R. and Homberg, U. (2001). Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J. Comp. Neurol. 439,193 -207.[CrossRef][Medline]
Lohmann, K. and Lohmann, C. (1996). Orientation and open-sea navigation in sea turtles. J. Exp. Biol. 199, 73-81.[Abstract]
Mouritsen, H. and Ritz, T. (2005). Magnetoreception and its use in bird navigation. Curr. Opin. Neurobiol. 15,406 -414.[CrossRef][Medline]
Osorio, D. (1986). Ultraviolet sensitivity and
spectral opponency in the locust. J. Exp. Biol.
122,193
-208.
Pfeiffer, K., Kinoshita, M. and Homberg, U.
(2005). Polarization-sensitive and light-sensitive neurons in two
parallel pathways passing through the anterior optic tubercle in the locust
brain. J. Neurophysiol.
94,3903
-3915.
Rossel, S. and Wehner, R. (1984). Celestial orientation in bees: the use of spectral cues. J. Comp. Physiol. A 155,605 -613.
Rossel, S. and Wehner, R. (1986). Polarization vision in bees. Nature 323,128 -131.[CrossRef]
Sakura, M. and Labhart, T. (2005). Polarization-sensitive neurons in the central complex of the cricket, Gryllus bimaculatus. Neuroforum 2005, Suppl.154B .
Sauman, I., Briscoe, A. D., Zhu, H., Shi, D., Froy, O., Stalleicken, J., Yuan, Q., Casselman, A. and Reppert, S. M. (2005). Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46,457 -467.[CrossRef][Medline]
Stalleicken, J., Mukhida, M., Labhart, T., Wehner, R., Frost, B.
and Mouritsen, H. (2005). Do monarch butterflies use
polarized skylight for migratory orientation? J. Exp.
Biol. 208,2399
-2408.
Stalleicken, J., Labhart, T. and Mouritsen, H. (2006). Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J. Comp. Physiol. A 192,321 -331.[CrossRef][Medline]
Strauss, R. (2002). The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12,633 -638.[CrossRef][Medline]
Vishnevskaya, T. M. and Shura-Bura, T. M. (1990). Spectral sensitivity of photoreceptors and spectral inputs to the neurons of the first optic ganglion in the locust (Locusta migratoria). In Sensory Systems and Communication in Arthropods (ed. F. G. Gribakin, K. Wiese and A. V. Popov), pp.106 -111. Basel: Birkhäuser.
Vitzthum, H., Müller, M. and Homberg, U.
(2002). Neurons of the central complex of the locust
Schistocerca gregaria are sensitive to polarized light. J.
Neurosci. 22,1114
-1125.
Wehner, R. (1989). The hymenopteran skylight
compass: matched filtering and parallel coding. J. Exp.
Biol. 146,63
-85.
Wehner, R. (1997). The ant's celestial compass system: spectral and polarization channels. In Orientation and Communication in Arthropods (ed. M. Lehrer), pp.145 -185. Basel: Birkhäuser.
Wehner, R. (2003). Desert ant navigation: how miniature brains solve complex tasks. J. Comp. Physiol. A 189,579 -588.[CrossRef][Medline]
Wehner, R. and Labhart, T. (2006). Polarization vision. In Invertebrate Vision (ed. E. J. Warrant and D.-E. Nilsson), pp. 291-348. Cambridge: Cambridge University Press.
Wiltschko, W. and Wiltschko, R. (1996). Magnetic orientation in birds. J. Exp. Biol. 199, 29-38.[Abstract]
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  L. Blackburn LOCUSTS' LIGHT RESPONSE J. Exp. Biol., April 15, 2007; 210(8): i - ii. [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
400–800 nm; visual angle: 3°;
frontal: 13 µW cm–2; contralateral, ipsilateral, dorsal:
2–4 µW cm–2). Positive deflections in the bottom
trace indicate duration of light stimuli.
