J. exp. Biol. 191, 107–123 (1994)
Printed in Great Britain © The Company of Biologists Limited 1994
107
THE ORIENTATION OF THE E-VECTOR OF LINEARLY
POLARIZED LIGHT DOES NOT AFFECT THE BEHAVIOUR OF
THE PIGEON COLUMBA LIVIA
M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
Neuroethology Group, Comparative Physiology and Utrecht Biophysics Research
Institute, Utrecht University, Limalaan 30, NL-3584 CL Utrecht, The Netherlands
Accepted 4 February 1994
Summary
Orientation with reference to the time-compensated sun-azimuth compass has been
established for the homing pigeon Columba livia. Previous qualitative studies claim that
pigeons are sensitive to the orientation of a polarizer and it has been suggested that these
animals are able to use sky-light polarization as an indirect reference to the sun’s position
when the latter is shielded from view. We report experiments which were undertaken to
quantify the sensitivity of the homing pigeon to the orientation of linearly polarized light.
The results of our initial experiments suggested that the animals responded to secondary
cues. Further experiments were carried out to avoid such artefacts. Under circumstances
where secondary cues were rigorously avoided, we were, however, not able to
demonstrate any directional response that was caused by the E-vector orientation of the
illumination. These results throw doubt on the suggested polarization-sensitivity of birds
in general.
Introduction
To choose a compass direction, a bird preferentially utilises the time-compensated sunazimuth compass (Schmidt-Koenig, 1979; Neuss and Wallraff, 1988; Wiltschko and
Balda, 1989). Release experiments with clock-shifted pigeons clearly show that even
when the information provided by the sun’s position is in conflict with other possible
sources of information, such as the direction and inclination of the geomagnetic field, the
former primarily determines the direction of departure. Moreover, a deterioration of
visual cues, such as that caused by mist during a flight, reduces the success of homing
(Schietecat, 1988a,b), which emphasises the importance of visual information during
flight.
The pattern of partially polarized light in the (blue) sky is linked to the position of the
sun. Information about the position of the sun is present in the direction of the electric
vector (E-vector) of this linearly polarized light, albeit with an uncertainty of 180 ˚. This
angle of polarization depends on the relative positions of the sun, the observer and the
point observed. The ability to perceive the orientation of the E-vector could thus be
Key words: polarization-sensitivity, Columba livia, psychophysics, suppression ratio, reaction time,
reflection artefact.
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regarded as an extension of the sun compass. It would, for instance, allow an individual to
estimate the sun’s position, given a few clear blue patches in an otherwise overcast sky.
Since von Frisch’s discovery (von Frisch, 1949) of the perception of polarized light by the
honeybee, behavioural as well as electrophysiological responses to linearly polarized
light have been demonstrated for many invertebrates and for some species of lower
vertebrates (for reviews, see Waterman, 1981; Wehner, 1989).
Evidence that birds are sensitive to the orientation of the electric vector stems from two
kinds of experiments. Polarotactic experiments with manipulated sky light were carried
out using dusk migrators in Emlen cages covered with a polarizer (for a review, see Able,
1989). The direction of the Zugunruhe was parallel to the E-vector. The polarizer changes
all aspects of the incident sky light, so these experiments do not exclude the possibility
that other factors that covary with the E-vector manipulation determine the results. For
instance, when the polarizer is rotated, the perceived intensity distribution across the
‘sky’ undergoes large changes. Helbig and Wiltschko (1989) did not exclude the
possibility that a type of phototaxis may have been responsible for their results.
Further information is obtained from experiments in which the animal’s ability to
discriminate between different orientations of the E-vector is tested by employing a
forced-choice procedure in the laboratory. Two such studies (Kreithen and Keeton, 1974;
Delius et al. 1976) led to the generally accepted conclusion that homing pigeons are able
to perceive the E-vector direction of linearly polarized light. From the latter study, it is
apparent that the illumination must reach a photopic level (higher than approximately
20 cd m22). Moreover, ultraviolet components are apparently not necessary because they
are not produced in large amounts by tungsten lamps (even less when intensity is reduced
by lowering the supply voltage) and they are not readily transmitted by polarization filters
(except specialized types). Emphasis is laid on the stimulation of the ventral part of the
retina (the dorsal visual field). Delius and Emmerton (1979) claim that this is why
Montgomery and Heinemann (1952) did not find any polarization-sensitivity in the
pigeon.
In contrast to the situation in invertebrates, in birds there are no known structures
which could permit polarization-sensitivity. However, Young and Martin (1984) describe
a model in which tight coupling between both members of the double cone could provide
the basis for such a mechanism. An examination of the spectral properties of the
polarization-sensitive mechanism might provide a test for this model. More specifically,
we could expect the sensitivity to be determined by the absorption of light by the P567
pigment, which is screened by the yellow oil droplet of the principal cone. According to
Bowmaker’s (1977) calculations, this combination would peak at approximately 567 nm.
Previous studies have not conclusively shown how the polarization-sensitivity of the
pigeon depends on wavelength, so we set out to measure this function (experiment 1).
The usefulness of polarization perception depends on the resolving power of the
detection system. The experiments mentioned above are of a qualitative nature. So far,
no-one has measured discrimination thresholds (just noticeable difference; j.n.d.) for two
E-vector orientations. Experiment 2 was designed to measure the j.n.d. for sequentially
presented stimuli.
Although the experiments were initially designed to test the spectral sensitivity of the
Polarization-sensitivity of the pigeon
109
polarization-sensitive mechanism of the pigeon (experiment 1) as well as its E-vector
discrimination threshold (experiment 2), their purpose, as will be explained below,
gradually changed.
Part of this work was presented at the third international symposium of the Northern
Eye Institute, Manchester, UK (Coemans and Vos, 1989) and was also part of a short
communication (Coemans et al. 1990).
Materials and methods
Experiment 1
The pigeon’s sensitivity to the E-vector direction of polarized light was tested in a
symmetrical Y-maze. In the centre of the maze, the axis of a stimulus of linearly polarized
light matched the axis of a linear polarizer on the ceiling of one of the corridors. Pigeons
had to choose this matching corridor.
Apparatus
The apparatus consisted of a wooden Y-maze (Fig. 1A) which was 60 cm in height.
Each corridor was covered by a weakly illuminated sheet of a linear dichroic polarizer
(HN22, Polaroid Corporation) oriented parallel to the corridor’s longitudinal axis. The
orientation of the polaroid filters was checked with a polarizer of known orientation. To
obtain diffuse light, these polarizers were covered with a sheet of semi-opaque Perspex.
Luminance measured under the filter ranged between 30 and 50 cd m22. At the point
where the three corridors met, the ceiling consisted of a circular tray (20 cm inner
diameter) containing a polarizer covered with a sheet of semi-opaque Perspex. This
combination could be rotated to any orientation in either direction by a stepper motor. Its
absolute orientation was encoded by means of three photodetectors, each of which
corresponded with one of the corridors. The change to a new orientation took place in
total darkness. A random trajectory was used in order to exclude auditory cues.
The central polaroid was illuminated from above with a 100 W, 3400 K halogen lamp
(Osram) shielded by a heat-reflecting filter (Kodak IR301). Intensity (maximum
luminance of the polarization source was 240 cd m22) and colour could be varied by
inserting nickel alloy neutral-density filters (Oriel Corporation) and interference filters
(Balzers) into the light path. Unpolarized light passing non-normally through a flat
surface will be polarized to some extent. As a result of this, the surface of a subsequent
polarizer will not be illuminated homogeneously. A weak pattern coupled to the
orientation of the polarizer, and maximal at the edges of the filter (about 4 % intensity
modulation in our case), will therefore be formed. Changing the distance of the
illuminator from the surface alters the maximum angle of incidence and thus the visibility
of this pattern. To check whether the animal responded to this unwanted cue, a test was
designed in which the intensity of another light source was varied by changing its
distance from the filter surface or its power (100 W, 120 W or 200 W, tungsten, Philips).
Preliminary studies of the effect of colour were carried out with this source as well. We
used the following broadband colour filters: cinemoid no. 24 (green; passband with peak
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M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
A
F
CL
III
P
CP
Ph
II
I
L
B
STIMULUS
ON
Wait
CHOICE
STIMULUS
OFF
Food: 6 s
Time out: 22 s
NEW
POSITION
Rotate
to new position
Fig. 1. (A) Y-maze for testing the perception of polarization. The bird was trained to walk
from one corridor (I, II or III) into another on the basis of the orientation of the central polaroid
filter (CP). Each corridor had its own polarizers (P) in order to facilitate training (matching to
sample). Ph, photodetectors; F, pneumatic feeders; CL, illumination of the corridor; L, central
illumination. (B) Schematic course of the experiment. See text for further details.
at 510 nm; approximately 90 nm half-width); no. 45 (blue, very broad transmission
characteristic); and no. 46 (orange; 50 % cut-off point at 550 nm).
The inside of the Y-maze was initially covered with matt black paint. At a later stage,
different materials were used (sandpaper and blotting paper) for reasons that are
discussed below. In some experiments, masking lights, consisting of small tungsten
lamps (3 W), were mounted above the entrance of each corridor. The filaments of these
lamps were shielded from view to prevent glare.
To prevent a bird simply walking from one corridor to another, a 4 cm high cardboard
platform was placed in the centre. The bird therefore had to jump onto and down from this
Polarization-sensitivity of the pigeon
111
obstacle. At the end of each corridor, an illuminated air-pressure-driven foodhopper
delivered mixed grains. At the entrance of each corridor, photodetectors monitored the
bird’s presence. All functions of the apparatus were controlled by a microprocessor.
Subjects
Initially, four mature homing pigeons, all of which had free-ranging experience, were
used in the experiment. They were housed indoors with daylight illumination. The birds
were deprived of food (at 80 % of their free-feeding weight) and kept on water and grit.
Three of the pigeons were successfully trained manually (more than 90 % correct
choices). Two of them performed well in the fully automated procedure.
Procedure
A session started when a subject was placed into one of the corridors. It had to choose
between the two other corridors on the basis of the orientation of the central filter.
Choosing the corridor lined up with the polarizer resulted in a 6 s access to food at the end
of the corridor (Fig. 1B). An incorrect choice resulted in 22 s of total darkness, during
which all activity was suspended (a time-out). The chosen corridor was taken as the
starting point for the next trial. One of the other two corridors was randomly assigned as
the next goal. The next trial started when the filter had rotated to its new position, which
took about 5 s. Results are presented as proportions of correct choices. Each session lasted
1 h and consisted of approximately 100 trials.
Experiment 2
The sensitivity of pigeons to the E-vector direction of linearly polarized light was
tested in a single-key Skinner box with an overhead source of polarized light. Pigeons
were rewarded with food when they pecked the key when the stimulus had a chosen
orientation [the number of pecks when the positive stimulus (S+) was presented is
designated as RS+]. Pecking the key when the stimulus’ orientation was orthogonal to this
led to a time-out [the number of pecks when the negative stimulus (S2) was presented is
designated as RS2].
Apparatus
The apparatus was made of white plastic-covered chipboard (40 cm330 cm370 cm;
Fig. 2A). Its inner walls were sandpapered in order to obtain a matt white appearance. At
a later stage (during experiment 2b and all subsequent experiments, as explained below)
these surfaces were covered with large sheets of white blotting paper. A pecking key was
located 15 cm above the floor of the box. In order to minimize reflections, it was either
illuminated from behind or covered with rough plaster. Underneath it, sunk into both the
wall and the floor, was a pigeon feeder driven by air pressure.
The ceiling of the box contained the source of polarized light and two room lights. The
polarized stimulus consisted of light (from a 50 W reflector tungsten–iodide lamp,
Philips) passing through a white semi-opaque Perspex diffusor and a linear dichroic
polarizer (HN22, Polaroid Corporation). The ceiling had a luminance of approximately
200 cd m22 (in the photopic luminance range). At a later stage, the ceiling was moved up
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M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
to a height of 1 m above the box floor, leaving a gap of 30 cm between the cover and the
rim of the box. This removed the reflections on the wall directly below the filter and made
it possible to use a video camera in order to monitor the bird’s behaviour. The polarizer
could be rotated to any position in either direction with the aid of a stepping motor. Its
position was controlled by means of four fixed photodetectors. The filter was rotated to a
new position in complete darkness, following a random trajectory in order to exclude
auditory cues.
As the experiments proceeded, additional cues were paired with the polarization cue, to
facilitate training. Four types of experiment were conducted. (a) No extra cue; (b) flicker;
implemented by switching S2 on and off (10 Hz under software control); (c) colour;
delivered as circular spots (4 cm in diameter), initially projected next to the key and later
next to the polaroid filter (Fig. 2A), produced by 50 W a.c.-driven tungsten–iodide lamps
in combination with an OG570 or BG38 (Schott) filter and neutral-density filters
(cinemoid- and inconel-coated glass substratum); (d) orientation; formed by rectangular
pieces of black cardboard 20 mm wide and of different lengths between 20 and 200 mm.
These were placed on top of the semi-opaque Perspex, parallel to the E-vector axis.
All functions of the Skinner box, as well as the course of the experiment, were
computer-controlled. Initially, sessions lasted 1 h. At the end of the experiments, they
lasted up to 5 h (approximately 50 trials per hour).
Subjects
Four inexperienced homing pigeons, all having several years of free ranging
experience, were used in the experiment. They were kept indoors with daylight
illumination (north-facing window). The birds were deprived of food (at 80 % of their
free-feeding weight) and kept on water and grit.
Procedure
A schematic course of a trial in experiments a and b is depicted in Fig. 2B. Initially, the
room lights were on. After the first key peck, they were dimmed and the polarization
source was switched on. During the next 14–20 s (randomly determined), the number of
key pecks was counted and the mean number of pecks per second calculated. This
pecking activity determined the duration of food access (1–8 s) after S+ as well as the
length of a time-out (total darkness during 2–20 s) after S2 (see the legend of Fig. 2B). In
order to maintain a strong coupling between pecking activity and food access, food was
delivered immediately after an additional obligatory peck when the counting period had
ended. After a reward or time-out, all lights were extinguished and the polarizer was
rotated to a new position. S+ and S2 were presented in random order (50 % each). The
number of consecutively presented S+ stimuli was limited to four.
In experiments c and d, the procedure was slightly different (Fig. 2C). In these cases,
we measured the reaction time (RT) as well. This is the period between the onset of the
stimulus and the first key peck. The reaction time was used as an indication of the
direction of the bird’s attention: frontal vision (the neighbourhood of the pecking key)
and the upper field of vision (the polarizer). This is explained below. Pecking activity was
counted in the 15 s following the first peck, and was used to determine food access or
Polarization-sensitivity of the pigeon
113
L
A
P
R
A
K
A
F
B
START STIMULUS ON
First peck
Wait
STIMULUS OFF
Count: 14–20 s
DARKNESS
Food: 1–8 s
Time out: 2–20 s
Rotate to
new position
C
STIMULUS ON (START)
First peck
Reaction
time
STIMULUS OFF
DARKNESS
Peck count: 15 s Random
Food: 1–8 s
interval Time out: 2–20 s
Rotate to
new position
Fig. 2. (A) Apparatus for testing polarization perception in a geometrically simple
environment. It employed a single pecking key and feeder apparatus. The number of pecks per
second (x) given during stimulus presentation determined the duration of access to food
(time=2x+1) after S+ (to a maximum of 8 s), or the length of a time-out (time=8x+2) after S2
(to a maximum of 20 s). P, polarizer; K, pecking key; R, room lights; L, light source; F, feeder;
A, additional cue (coloured spots); the arrows indicate that the position of the help cue could
change from session to session (see text). (B) Schematic course of experiments a and b
described in the text. (C) Schematic course of experiments c and d.
time-out duration. An example of pecking activity using an additional cue of coloured
spots near the pecking key is given in Fig. 3A. Because there are two positions of the
filter wheel for each E-vector orientation, these positions should be indistinguishable
from each other. To make sure that spots, or irregularities in the polaroid filter, did not
interfere with the experiment, we regularly compared the responses to these stimulus
pairs. Fig. 3B shows an example.
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M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
30
A
25
20
15
10
Pecking response (pecks per 15 s)
5
0
−5
0
2000
4000
6000
Time (s)
8000
10 000
12 000
18
16
14
B
12
10
8
6
4
2
0
−2
−4
0
90
180
270
Polarizer angle (degrees)
Fig. 3. (A) Typical recording of pecking responses, as pecks per 15 s, during an experiment.
The additional cue consisted of coloured spots next to the pecking key. Filled symbols,
responses to the positive stimulus (RS+); open symbols, responses to the negative stimulus
(RS2). (B) E-vector orientations repeat themselves after half a turn of the filter wheel (180 ˚).
This means that, for a specific direction of the plane of polarization, there are two possible
orientations of the filter wheel. To diminish the possibility that irregularities in the polarizer or
diffusor provided cues for the pigeons, both possibilities were used, each with an equal
probability. The figure shows means and standard deviations of the suppression ratios
depicted in A, when these are categorized for each orientation of the filter wheel.
During all experiments, we computed the moving average and standard deviation of the
pecking rates over the last five trials when the positive stimulus was presented. The mean
minus 1 S.D. was taken as a criterion level, which was used during the experiment to
evaluate the bird’s response. When the pecking rate elicited by the next negative stimulus
was below this criterion, the response was considered correct. In experiments c and d this
meant that the next trial was an S+ (a postponed reward); otherwise an S2 was given as a
correction trial. The results of these trials were discarded.
Polarization-sensitivity of the pigeon
115
To analyze the data, we used the suppression ratio (SR; Smith, 1970), as well as the
difference in reaction time (DRT). In both cases, the response to S2 (RS2) was compared
with the response to the immediately preceding S+ (RS+). We calculated the suppression
ratio as follows:
RS+ 2 RS2
SR = ————— , for RS+ ùRS2
(1)
RS+
RS+ 2 RS2
SR = ————— , for RS+ <RS2 .
RS−
(2)
The equation is used to ensure that pooled results have a distribution which is
symmetrical around zero, when RS+ is approximately equal to RS2; otherwise, random
fluctuations would bias the ratio to negative values. The reaction time difference was
defined as:
(3)
DRT = RT2 2 RT+ .
We computed 95 % confidence intervals (t-test) for the reaction time data as well as the
suppression ratio data. The validity of P-values computed by means of the t-test when
testing the significance of the difference between RS+ and RS2 was regularly checked by
a permutation test (a random sample of N=1000 or N=10 000 was drawn from the
population of all possible permutations). Both tests were in good agreement, especially
when the differences between RS+ and RS2 were small.
Results
Experiment 1
After installation of the cardboard platform, the birds learned (>80 % correct choices in
five subsequent sessions) to choose the corridor indicated by the orientation of the
polarizer in the automated procedure. The luminance of the polarization source was
100 cd m22. We next measured the performance as a function of the intensity of the
central light source when this was varied by changing the lamp height (Fig. 4A).
Discrimination performance was found to be a function of luminance, which resembled
the earlier finding of Delius et al. (1976). This suggested to us that the above-mentioned
intensity patterns on the filter did not have any undesirable effect. However, visual
inspection of the experimental chamber, while the central filter was rotating at a constant
moderate speed (0.5 Hz), revealed distinct brightness cues reflected from the inner walls
of the Y-maze.
After installation of the halogen illumination, we experimented with lighter wall covers
in order to diminish these cues. Fig. 4B depicts the birds’ performance when intensity
was varied by neutral-density filters, after the walls had been covered with yellowishwhite coarse sandpaper. The main difference from Fig. 4A is a slight shift towards lower
light levels. The performance, however, depended in part on the corridor that the birds
were coming from: coming from corridor I resulted in a significantly steeper drop of the
curve as a function of light intensity (x2-test; P=0.0004; asterisks in Fig. 4B; no left/right
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M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
1.0
A
0.9
0.8
0.7
Proportion of correct choices
0.6
0.5
0
25
50
75
100
125
150
175
200
225
250
50
75
100
125
150
175
200
225
250
1.0
B
0.9
*
0.8
*
0.7
0.6
0.5
0
25
I (cd m−2)
Fig. 4. The combined psychophysical functions of the two birds from the fully automated
procedure. Discrimination performance is plotted as a function of intensity (I). Error bars
indicate 95 % confidence limits. (A) Walls covered with matt black paint. Circles, intensity
was changed by varying the height of the light source; squares, results of Delius et al. (1976)
for comparison. Both results are very similar. (B) Walls covered with yellowish-white coarse
sandpaper, containing grains with specular reflection properties. The intensity of the stimulus
source was changed by means of neutral-density filters. The whole curve is shifted somewhat
to the left compared with the curve in A. Asterisks indicate differences between corridors, as
explained in the text.
preferences, x2-test; [email protected]), compared with birds coming from corridor II or III.
Spurious intensity cues were still visible to us on the walls of the corridors.
Changing the sandpaper for white blotting paper affected the birds’ performances
profoundly: discrimination dropped to chance levels, whereas we expected at least 80 %
correct choices at this luminance (100 cd m22) (t-test; N=300; P<0.001). Performance
was also affected (60 % correct choices) when we mounted lights above the entrance of
each corridor in an attempt to mask the intensity cues apparent on the sandpaper walls
(t-test; N=245; P<0.001).
Polarization-sensitivity of the pigeon
117
The following control experiments were performed in the sandpaper-covered
apparatus. Removal of the polarizers above the corridors had no effect (t-test; N=116;
P>0.999). Replacement of the central polarizer by a 0.3 log units neutral-density filter
resulted in a drop to 50 % correct choices (t-test; N=170; P<0.001). Performance was not
influenced by insertion of broadband colour filters into the lightpath. Although one has to
be careful using a photometer when working with non-human subjects, we estimated that
the resulting luminances justified an expectation of 75 % correct choices for the green
filter (31 cd m22) and better for the other two filters. We found 77 % (green), 78 % (blue)
and 81 % (orange) correct choices, indicating that the addition of these colour filters did
not affect the behaviour of the pigeons (approximately 1000 trials for each colour filter).
Experiment 2
Experiment a
Experiments started in a sandpapered matt white box. After the birds had learned to
peck the key for a food reward, they were trained daily for about 1 month to acquire a
stable pecking rate. After this, pecking was rewarded only when the source of polarized
light had the correct orientation (S+). These experiments proceeded first manually and
eventually automatically for about 2 months with daily sessions of 1 h. We found no
suppression of the pecking rate during S2.
Experiment b
We decided to present S2 in combination with a conspicuous additional cue, a 10 Hz
flicker, to three subjects. Pecking suppression was almost complete within one session.
Next, the onset of this flicker was delayed by means of a staircase procedure. This delay
could be increased or decreased in steps of 10 % of the duration for which the stimulus
was presented. When RS2 was below the criterion level, the delay of the flicker was
increased, otherwise it was decreased. When the delay reached 100 %, S2 remained
steady and the additional cue was not presented.
After three sessions, one bird could discriminate between S+ and S2 without the
additional flicker cue. We noted that this bird walked around in the box before it pecked
the key. To investigate the possibility that this bird scanned intensity differences on the
box walls, we changed their reflective properties by covering them with white blotting
paper. Following this procedure, discrimination between S+ and S2 vanished (Fig. 5A).
The results for the other two birds are presented in Fig. 5B. The suppression ratio
depended entirely on the delay to the onset of the flicker. When the delay was maximal,
the difference between the suppression rates following the presentation of S+ and S2 was
insignificant (N=129; P=0.26).
Experiment c
Experiments with several other cues demonstrated that these could be distinguished
into two classes. One group consisted of cues that were conspicuous, even when the
animal was looking towards the pecking key. We used flicker (as above), intensity
differences between S2 and S+, and differently coloured spots accompanying the
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M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
1.0
A
0.8
0.6
0.4
0.2
0
Suppression ratio
−0.2
−0.4
Session number
1.0
B
0.8
0.6
0.4
0.2
0
0
0.2
0.4
0.6
0.8
1.0
1.2
Delay
Fig. 5. Flicker was presented as an additional cue in experiment b. (A) The results of pigeon A.
Bars are mean suppression ratios of consecutive sessions (number of trials ranged from 40 to
140 per session); the three sessions in which flicker was gradually removed are not shown.
Left-hand arrow, introduction of flicker; middle arrow, flicker cues removed; right-hand
arrow, box walls covered with white blotting paper. (B) Mean suppression ratio (±95 %
confidence interval) of the final five sessions (962 trials) as a function of the delay of the onset
of flicker for pigeons B and C. The delay is presented as a fraction of the total stimulus
presentation time. Error bars indicate 95 % confidence intervals.
presentation of S+ and S2 projected next to the key. The pigeons were easily trained using
all of these cues. The other group consisted of cues that could only be seen when the
animal looked in a specific direction. These included coloured spots on the ceiling next to
the polarizer, or the silhouette of a bar placed on the polarized ceiling. Pairing E-vector
orientation with either of these cues did not enable the birds to peck successfully. As we
supposed that the E-vector-sensitive part of the eye was located in its upper field of
vision, we had, until these experiments, categorized an E-vector stimulus as belonging to
the first category. In the next set of experiments, we decided to direct the birds attention
towards the polarizer.
Polarization-sensitivity of the pigeon
1.0
A
20
Suppression ratio
0.8
20
0.8
0.6
0.6
0.4
10
0.4
10
0.2
0.2
0
0
0
0
−0.2
−0.2
−0.4
101
B
DRT (s)
1.0
119
102
103
104
105
106
−10
107
−0.4
101
102
103
104
105
106
−10
107
Attenuation
Fig. 6. Coloured spots were projected as an additional cue next to the polarizer in experiment
c. Psychophysical functions for pigeon B. Left ordinate and open symbols, suppression ratio
(SR); right ordinate and filled symbols, reaction time difference (DRT). Error bars indicate the
standard deviation. Each point is the mean of at least 60 trials. Discrimination performance is
plotted as function of the intensity of the additional cue. Results obtained from two
consecutive blocks of sessions. (A) In the first block, there was an apparent bias caused by
differential wall reflections. (B) In the second block the bias disappeared after the blotting
paper had been renewed.
The birds were trained to discriminate between S+ and S2 when polarization direction
was paired with differently coloured spots projected on either side of the pigeon key.
These additional cues were projected at a higher position in subsequent sessions, until
they were eventually next to the polaroid filter. After the birds had been trained in this
way to discriminate between stimuli presented from above, the colour cues were
successively reduced in intensity from session to session using neutral-density filters. The
suppression values were found to be correlated with the intensity of the coloured spots
(r=20.95; P=0.0004). In some experiments, however, some discrimination remained
when the suppression data were considered: the suppression ratio remained between 0.1
and 0.3 (P<0.05). This was not so for the reaction time data (Fig. 6A). These showed no
significant difference when the additional cue was attenuated by more than 4 log units
([email protected]). Examining the birds’ behaviour under these circumstances with a video
camera revealed that when the stimulus was switched on, the birds looked towards the
polarizer. After a while (e.g. 10 s), they pecked the key a few times. Next, they made
scanning movements (they moved their heads continuously up and down) either in front
of a wall or in a corner, occasionally giving a peck on the key. As we thought that the
birds could be detecting reflection differences, we decided to change the reflective
properties of the walls. After the old blotting paper had been replaced with fresh paper,
the scanning behaviour did not alter but the performance after the presentation of S+ did
not differ from that after the presentation of S2, when the help cue was attenuated by
4 log units or more (Fig. 6B; [email protected]). We conclude that ‘used’ blotting paper generates
120
M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
1.0
Suppression ratio
0.8
0.6
0.4
0.2
0
−0.2
0
0.2
0.4
0.6
log(length/width)
0.8
1.0
Fig. 7. Typical example of psychophysical functions for pigeon C, when the orientation of a
bar was presented as an additional cue in experiment d. Discrimination performance (mean
suppression ratio ± S.D.) is plotted as a function of the logarithm of the length/width ratio of
the overhead bar. Filled symbols, the polarizer was in place; open symbols, the polarizer was
replaced by a 0.3 log unit neutral-density filter. Each point is calculated from at least 100 trials.
(weak) differential wall reflections because of its smutted surface. Comparing the
reaction time data and the pecking data in this way allowed us to decide whether the
pigeon was using information provided by a distinct cue, such as the coloured spots, or by
‘diffuse’ information in the neighbourhood of the pigeon key.
Experiment d
From the above experiments we concluded that pigeons are not able to utilize the
information provided by the orientation of the E-vector. We had shown that every other
(faint) discrimination cue was detected and utilized. One further possible explanation of
the apparent ability of pigeons to detect E-vector orientation under certain conditions
remained to be examined. Therefore, because an axial cue (the orientation of the
polarizer) might not readily be associated with a non-axial cue (flicker, colour), we
decided to test the effect of another axial cue.
Two birds were trained to respond to a bar placed upon the Perspex diffusor, parallel to
the E-vector direction. This was fairly easy as the birds were already trained to expect
information from above (we gradually replaced the coloured spots with an elongated bar).
Two experiments were conducted: (1) the polarizer was replaced by a neutral-density
filter of 0.3 log units and (2) the polarizer remained in place. The suppression ratios and
the reaction times of the birds were measured as a function of the length/width ratio of the
bar. We found no significant differences ([email protected]) between the curves (Fig. 7), except for
the differential reflection effects as described under experiment c (not shown).
Polarization-sensitivity of the pigeon
121
Discussion
When our results are compared with those of Delius et al. (1976), it could be concluded
that we had replicated the earlier results (Fig. 4A). However, we are unwilling to attribute
our findings to polarization perception, because the performance of the pigeons depended
on the wall covering used, a variable not manipulated by Delius et al. (1976).
We realized that painting the inside of the box black was not a good choice. The
amount of linearly polarized light which is reflected from a wall depends on the degree
and angle of polarization. When the angle of polarization is parallel to the wall
(horizontally polarized), the intensity of the reflected light will be maximal; when its
orientation is perpendicular to it (vertically polarized), it will be minimal. These effects
are ruled by physical laws (Born and Wolf, 1983) and therefore these intensity
differences are inevitable. There are two ways to make them subliminal. A rough surface
will depolarize the light and thus decrease the difference. A high albedo will increase the
background intensity and can thus mask the remaining small differences of intensity
caused by polarization. In our experiment with black surfaces, the birds could simply
compare light reflected from differently oriented walls. Inhomogeneities in the sandpaper
lining affect the maximum difference between those walls that are visible from each
corridor. This might explain the somewhat different results for corridor I.
The conformity of the results of Delius et al. (1976) (stimulus: E-vector direction) and
our results (stimulus: reflection differences) necessitated another approach to the study of
the perception of polarized light. We decided to abandon the Y-maze because it was
difficult to avoid reflection differences as there are too many surfaces that can be
compared in this respect. We therefore concentrated on the very different experimental
design of experiment 2.
The results of these experiments show that the pigeons utilized every cue that was
present, except for the orientation of the E-vector. This cue must have been a prominent
one, because it consisted of the difference in orientation between orthogonally oriented
polarizers. Our confirmation of the negative results obtained by Montgomery and
Heinemann (1952) was unexpected, as more recent investigations that claim to
demonstrate polarization-detection appeared to be rigorous (Delius et al. 1976; Kreithen
and Keeton, 1974). In order to explain the differences between our study and previous
studies, the following should be noted.
First, our pigeons clearly did not spontaneously pay attention to cues emanating from a
part of their environment that was not covered by their frontal visual field. In experiment
1, we added a cardboard platform. Jumping on and off this platform presumably forced
the pigeons to attend to their whole environment. In experiment 2, it was necessary to
guide the birds’ attention, by means of help cues, towards the cue being tested. Second, a
source of polarized light above the pigeons always produces intensity differences
between adjacent walls at eye level. Pigeons are very good at detecting minute luminance
differences (Hodos et al. 1985). An obvious way to overcome this is to make the
differences subliminal. Roughening the surface has a depolarizing effect, which
decreases the maximal difference. As pointed out by Umov (1905), the behaviour of dark
surfaces is very different from that of white surfaces when reflecting linearly polarized
122
M. A. J. M. COEMANS, J. J. VOS HZN AND J. F. W. NUBOER
light. On a dark surface, there are pronounced differences in intensity of reflection
depending on whether the E-vector of linearly polarized light is parallel or orthogonal to
the reflecting surface. We have measured these maximum intensity differences after
reflection (angle of incidence was 45 ˚) on the materials we used. We found that matt
black paint produces differences which exceed 0.2 log units, whereas (fresh) white
blotting paper yields values less than 0.03 log units. Hodos et al. (1985) found a mean
luminance difference threshold of 0.11 log units at 300 cd m22. Most pigeons should,
therefore, easily be able to detect the differences produced by differential reflection of
polarized light on a black surface. To eliminate spurious reflections as much as possible,
our experiments have shown that the surface’s albedo must be as high as possible.
These points, combined with the remark of Delius and Emmerton (1979) that they had
difficulties in training pigeons to discriminate the orientation of an overhead bar, make it
plausible that these authors actually trained their pigeons to discriminate intensity
differences at eye level. Their experimental apparatus had matt black surfaces. Moreover,
every orientation of the polarizer (0 ˚, 45 ˚ and 90 ˚) that they presented had a counterpart
in a parallel wall of their octagonal Skinner box. This ensures that remaining intensity
differences could have been large and were presented optimally for the pigeon. This
supposition is supported by an examination of the data presented in Fig. 4A.
Our results emphasize the technical difficulties involved in psychophysical
experiments concerning polarization perception. Consider the process of refraction, when
light passes non-normally through curved surfaces, such as those of the lamp bulb or
lenses of a slide projector. These surfaces polarize a light beam by a few per cent. When
we take this into account, an experiment requiring discrimination between a stationary
and a rotating polarizer could be performed as a flicker discrimination task. As pigeons
are very sensitive to intensity differences, this could be an alternative explanation for the
results of Kreithen and Keeton (1974), who employed heart rate conditioning to
determine whether pigeons were able to discriminate between a stationary and a rotating
polarized light source.
Replacing the polarizer with a neutral-density filter is a control experiment that proves
that the polarizer is crucial. However, it does not disentangle E-vector information proper
from unwanted reflections (or flicker), so it does not prove that polarization perception is
possible. To do this, the E-vector component must be left intact while the unwanted
components are varied. Changing the wall covering is such an experiment, as is the
application of background illumination.
It could be argued that we often required the birds to couple an on/off cue with an axial
cue. It might have been difficult for pigeons to achieve this association. However, in
experiment 2 the birds proved to be able to couple the orientation of an overhead bar (an
axial cue) with a colour cue (an on/off cue) within a few sessions. This is strong evidence
against this proposed argument.
Our experiments and studies that were executed under a natural sky (for instance: Able,
1982; Helbig and Wiltschko, 1989) differ in that the nature of our stimulus is exactly
known, whereas the colour and intensity distributions of the natural sky provide
additional directional cues, which might explain the positive results in the open-air
experiments.
Polarization-sensitivity of the pigeon
123
We thank R. J. Loots and W. Maasse for developing the electronic and mechanical
equipment and E. M. Brenner for helpful discussion. This work was supported by the
Netherlands Organization for Scientific Research (N.W.O.).
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