Orientation and lateralized cue use in pigeons navigating a large indoor environment
AE Biopsychologie, Ruhr-Universität Bochum, 44780 Bochum, Germany
* Author for correspondence (e-mail: helmut.prior{at}ruhr-uni-bochum.de )
Accepted 2 April 2002
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Summary |
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Key words: orientation, lateralized cue use, brain, pigeon, Columba livia
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Introduction |
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Several studies support the view that visual aspects of the landscape are
used during homing. When pigeons have the opportunity to preview a familiar
landscape before departing they home faster than birds without this visual
information (Braithwaite and Guilford,
1991; Braithwaite and Newman,
1994
; Burt et al.,
1997
). Pigeons, however, tend to deviate in a predictable manner
from the correct direction at familiar release sites if their sun compass is
altered by clock-shifting (cf. Füller
et al., 1983
; Wiltschko and
Wiltschko, 1998
). Whether such findings are inconsistent with the
pigeons' use of visual information depends on the way they process this
information. If they were `piloting' by heading towards prominent landmarks,
they should not deviate after a clockshift. If, however, they were using
visual information just to recognize the site, they should show a systematic
deviation. For example, when clock-shifted, pigeons with lesions to the
hippocampus and released at familiar sites
(Gagliardo et al., 1999
)
deviated to the full extent predicted by the clock-shift, whereas control
pigeons showed only a small deviation from the home direction. This suggests
that intact control birds derived directional information directly from the
landmarks, while birds with hippocampal lesions used the landmark information
to recognize the site and to recall a bearing associated with that site.
Fairly clear-cut evidence for the use of visual information at the release
site was obtained in a recent study using a circular arena that confined the
pigeons for a brief moment before departure
(Gagliardo et al., 2001b
).
This design permitted assessment of the pigeons' bearings while the visual
cues were strictly controlled. Pigeons that were rendered anosmic to prevent
them from using olfactory cues, but could see the surrounding landscape, were
well oriented towards home. When the landscape was screened from view by
curtains, the pigeons were oriented randomly. Apart from the dependence of
performance on visual information, this study demonstrated the translation of
landscape information into a bearing under conditions controlled by what the
pigeons could see. Although evidence from field studies for the use of visual
information is increasing, it is still not clear which aspects of landmark
information are used by the pigeons and how this information is processed.
A quite different line of research investigated the use of visual landmark
information by pigeons searching for food in the laboratory. The environments
were rather small, but as the conditions in the laboratory allowed for
controlled manipulations of visual cues, these studies provided important
insights into the way pigeons process landmark information. In a typical
experiment, the birds searched for hidden food, and changes in their searching
activity after systematic changes of the visuo-spatial cues were assessed.
Such studies have shown that the size of the landmarks appears to be of minor
importance (Cheng, 1988).
Typically, pigeons appear to remember distances and directions to landmarks
following a two-step process. In the first step, the landmark matching
process, pigeons recognize landmarks or an array of landmarks. In the second
step, the search place matching process, they establish the direction to
individual landmarks (Spetch et al.,
1996
,
1997
). If a symmetric landmark
array was learned and then transformed during a test, for example by extending
the array from a square into a rectangle, pigeons used a spatial strategy
quite different from that of humans. While humans encoded a kind of rule in
terms of the overall array (e.g. `search in the middle'), pigeons tended to
encode the distance and direction to single landmarks or a small subset of the
landmark array.
To understand how pigeons might use such information in the real world, two points in particular need further evaluation. Firstly, which aspects of visual information do the pigeons use to determine a bearing upon being released? Do they recognize the release site by local features, or are they able to use the overall geometry of the surrounding landscape, which might provide a global reference frame accessible from a number of sites within a given area? For example, the area around Pisa in Italy, where many important homing studies take place, is characterized by a global reference frame consisting of a straight coastline in the west, the wall of the Apuan Alps in the north east, and the Tuscan hills in the south east. If a pigeon is released within this area, after gaining some height it will always be exposed to this global reference frame. The perspective might differ, but it will see this spatial reference frame, at familiar as well as at unfamiliar sites. On the other hand, local features and prominent landmarks might differ completely at different release sites. So, in principle, a mainly geometric global reference frame could guide the birds visually when released from familiar and unfamiliar places at short to medium distances.
A second important point arises from the fact that the multicomponent task
of spatial orientation is based on different contributions from the left and
right brain hemisphere. In order to understand what spatial information is
processed and how, it is crucial to evaluate the unique role of each
hemisphere. In birds, tests for lateralization can be carried out conveniently
by temporary occlusion of one eye. As the fibres of the avian optic nerve
cross over completely, visual input through the right eye is mainly processed
by the left brain hemisphere and vice versa (cf.
Güntürkün,
1997). On the basis of early findings, a complementary pattern of
avian visual lateralization had been suggested in which the right brain
hemisphere is mainly concerned with the processing of topographical
information, while the left brain hemisphere deals with recognising and
categorising the properties of objects
(Andrew, 1991
;
Bradshaw and Rogers, 1993
).
Several studies were consistent with this hypothesis
(Rashid and Andrew, 1989
;
Clayton and Krebs, 1994
).
There is, however, increasing evidence that both hemispheres contribute to
spatial cognition, so as things stand now, the challenge is to determine which
specific aspects of spatial information processing are contributed by the
right or the left brain hemisphere (Ulrich
et al., 1999
; Tommasi and
Vallortigara, 2001
). Pigeons show lateralization of object
discrimination, but not of spatial performance, when subjected to a working
memory task in a maze (Prior and
Güntürkün, 2001
), and the left hemisphere is
superior during homing from remote release sites
(Ulrich et al., 1999
; H.
Prior, R. Wiltschko, K. Stapput, O. Güntürkün and W. Wiltschko,
manuscript submitted for publication). Furthermore, a lesion study suggested
lateralized learning of the navigational map
(Gagliardo et al., 2001a
).
There are several possible explanations for a left hemispheric superiority
during homing. As pigeons have a better long-term memory for visual patterns
in the left brain hemisphere (von Fersen
and Güntürkün, 1990
), it might be more competent in
recognizing landmarks, which could be particularly important as pigeons
approach the loft. Also, the left and the right avian brain might differ in
rather fundamental aspects of spatial information processing. From experiments
where the shape of an indoor arena was varied during food searching by chicks,
Tommasi and Vallortigara
(2001
) concluded that the
right avian brain is mainly concerned with relational spatial information,
while the left avian brain encodes absolute metric information.
The present study considered both the role of different cues and perspectives and the question of lateralization. A large laboratory arena was used, and several aspects of a natural homing situation were simulated. There were three levels of visuo-spatial information. (1) A global reference frame was provided by the outer walls of the arena. An artificial `horizon' (see Materials and methods) prevented the pigeons from seeing straight ahead for more than 1-2 m from any place when walking through the arena. The global reference frame could be seen from anywhere. (2) Four prominent landmarks, tall enough to be seen from any place within the arena, formed an array around the target region. (3) There were many local cues, which were only visible from a very short distance. In principle, a pigeon could successfully find the goal along the familiar training route by `piloting' from one local cue to the next. Pigeons were tested with the original configuration of spatial cues from familiar (experiment 1) and new (experiment 2) release sites. Then how removal of landmarks and local cues affected the pigeons' performance was assessed (experiment 3). Finally a dissociation experiment was carried out (experiment 4). The landmark array was moved so that the target region predicted by the landmark array differed from the target region predicted by the global reference frame.
All experiments included testing for lateralization. Apart from the more
general question of whether pigeons can determine accurate bearings from new
places and whether the two brain hemispheres contribute differentially to
this, we formulated several more specific hypotheses. If the pigeon's
orientation guided by global cues does not show lateralization, as suggested
by the maze study (Prior and
Güntürkün, 2001), their performance should be the
same for tasks in which a global reference frame allows for orienting and is
not in conflict with local cues (experiment 1). If there is lateralization in
the processing of object-specific cues, performance with the right eye/left
hemisphere should be impaired when prominent landmarks or local cues are
removed (experiment 3). If there were, as in chicks, a pattern of
lateralization in which the left brain hemisphere specializes in object
information and the right brain hemisphere is mainly concerned with geometric
relational cues (cf. Andrew,
1991
), the right hemisphere should outperform the left hemisphere
when the birds approach the goal from new points in different directions
(experiment 2). Furthermore, in a case of conflicting information, birds using
the right eye should search in a target area predicted by prominent landmarks,
and birds using the left eye should search at the area predicted by the global
spatial reference frame (experiment 4).
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Materials and methods |
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Experimental environment
Experiments took place in a large indoor room, within which a rectangular
arena (6.5 mx10 m) was set up (see
Fig. 1). The outer walls of the
room were 4 m high and provided two of the arena walls. The other two arena
walls were wooden separations 2.5 m high. The room was brightly lit by
fluorescent lamps at the ceiling. Black curtains covered all windows so that
no sunlight entered the room. Approximately 100 cardboard containers (25
cmx22 cmx31 cm, lengthxwidthxheight) were distributed
randomly within the arena and provided an artificial `horizon' for birds
moving on the floor. The goal G was not visible until birds were 1-2 m away
from it. Four big landmarks, poles 140-200 cm high and at different distances
and directions from the goal, were visible above the artificial horizon. At
the top of each pole was fixed a piece of cardboard, 40-60 cm wide and 60-80
cm high, with a unique shape and colour pattern for each landmark. Local cues
were drawings and prints on the cardboard containers, which differed in size,
shape and colour.
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Monocular occlusion
Before training and testing began, birds were prepared for wearing eyecaps
as described (Ulrich et al.,
1999). In brief, a ring of Velcro was fixed around each eye with
water-soluble, non-toxic glue after clipping a circular strip of feathers. The
counterpart of the Velcro ring was glued to a circular cardboard eyecap (26 mm
diameter). The eyecap could be bent easily, to ensure a tight fit on the
pigeon's head. The eyecap was fixed about 10 min before starting a monocular
test, and was removed immediately afterwards.
General procedure
Birds were first trained to find the route to the goal from a start
position that was the same during all trials. In order to prevent the birds
from visiting sites to be designated as new sites during later tests, they
learned the final route from the starting position stepwise during the very
first trials. Birds started by finding a short route approximately 0.5 m from
the goal, and during subsequent training trials the route was elongated by
moving the start position further away until the birds began at the designated
start position, which was used during late training trials and tests in
experiments 1 and 3. Reaching the goal directly four times in a row was taken
as the criterion that the birds had learnt each step of the route. After
achieving this from the final start position, ten further training trials were
done. The four experiments described above were then performed, each
addressing a specific question. Every trial was videotaped, and a clock
integrated into the video recorder displayed the time to 0.1 s resolution,
which allowed for frame-by-frame analysis of the birds' performance. The
following parameters were derived for all experiments: the bearing of the
birds after they had moved 1 m from the starting point, the time they took to
reach the goal, and the length of the path taken. Individual paths were traced
with tracking software (Wintrack; cf.
Wolfer et al., 2001).
Statistical analysis
Analogous to a homing study in the field, our statistical analysis focused
on how the birds were oriented upon leaving the starting site and how
efficiently they reached the goal. For the initial orientation, we assessed:
(1) the mean direction, (2) the extent of directedness, (3) the observed
direction with respect to the goal direction, (4) the observed direction of
monocular birds with regard to binocular controls, and (5) dispersion
variation within the different treatments. Mean directions were calculated as
mean vectors. The length of the mean vector, ranging from 0 to 1, gives an
estimate of the birds' directedness. In homing studies, orientation in a
predicted (e.g. home) direction is usually analysed by the V-test.
Although the arena we used was fairly large, there might have been spatial
constraints, e.g. due to the distance of the starting locations to the outer
walls, so the V-test would have overestimated the direct flight of
the birds towards the goal. Therefore, a rather conservative and robust
approach was chosen. For each sample, linear confidence intervals of
coefficient Q=0.99 were calculated (cf.
Batschelet, 1981), and whether
they included the goal direction was checked. Similarly, we tested whether the
mean direction of binocular controls was within the confidence limits of
monocular birds. We calculated angular differences with regard to the goal
direction as a measure of dispersion. `Homing performance' was the average
speed of each bird calculated from the path length and the time taken to reach
the goal. Angular differences and `homing' speeds were compared by analysis of
variation (ANOVA) after checking for normality and homogeneity of variances. A
Fisher's LSD test was used for pairwise comparisons after significant overall
ANOVAs if the number of comparisons was small (approximately 3), because in
that case the test provides a good trade-off between power and security. For
higher numbers of comparisons, a Tukey's HSD test was used. Directional data
from experiment 4 were analysed the same way as in the other experiments, but
there were some differences in other performance parameters. As the search
time was fixed, the path lengths rather than the `homing' speeds were
compared. In addition, search activity at different locations was compared,
and for this the arena was divided into 0.5 m squares. The time spent in any
of these squares was measured, and for each bird data were combined to obtain
the distribution of search activity along the long and small axes of the
arena. As this measure had a non-parametric distribution, comparison between
eyecap conditions was done using Wilcoxon matched pairs tests.
Experiment 1
After learning one particular route, each pigeon was tested on two
consecutive days. On the first day, half of the birds were treated in the
order `left binocular right', and the other half `right
binocular left'. On the second day the order was reversed. The
reason for two tests was identify differences between the first and the second
monocular trial, as it is known from other studies with monocular birds that
they tend to show systematic deviations towards the side of the uncovered eye
during first tests.
Experiment 2
In this experiment, the birds were tested from four new positions (cf.
Fig. 4), which were balanced in
route length and direction. In addition to a binocular trial from each of the
new starting sites, each bird completed four tests with eyecaps. Tests with
the same eye were made from release points at the same distance from the goal,
and the combination of release points and eyecap conditions was balanced
between subjects. Thus, for each position there was a within-subject
comparison binocular versus monocular and a between-subject
comparison between use of the left and the right eye.
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Experiment 4
Experiments 1, 2 and 3 tested whether the pigeons headed accurately for a
non-visible goal, independently of the eye/brain hemisphere used. Once in the
vicinity of the goal, however, they could see the goal. Experiment 4 tested
for the searching location of the pigeons after dissociating possibly relevant
cues. The two aspects that were of some importance in the earlier tests, i.e.
the global reference frame and the prominent landmarks, were arranged so that
two predicted different goals. The local cues, which apparently had no effect
on the searching activity of the pigeons, were randomised throughout the
entire arena so that they could not signpost the location of the goal. The
prominent landmarks were moved (cf. Fig.
8) so that the overall configuration of the landmark array and its
orientation with regard to the global reference frame were preserved, but the
goal location predicted by the prominent landmarks (G') was different
from the goal position predicted by the global reference frame (G). In this
test we were interested not only in the first choice of the birds but also the
subsequent search. There was therefore no goal. Thus, we could evaluate how
the birds would distribute their search behaviour guided by the global
reference frame and/or big landmarks only. The searching behaviour of the
birds was observed for a period of 5 min. All birds started from two new sites
(A and B) at opposite walls of the arena. Eight of the birds used the right
eye from site A and the left eye from site B, and seven birds received the
opposite treatment. We measured the time the birds took to reach an area
within a radius of 0.5 m around G or G' on their first choice, the
length of the search paths during a 5 min period, and the distribution of
searching activity among different patches in the arena.
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Results |
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Experiment 1
Experiment 1 tested the effect of monocular occlusion and possible
differences between the right and left brain hemisphere when navigating a
highly familiar route. The results of experiment 1 are given in Figs
2 and
3. All bearings had long
vectors (r>0.95 for all) indicating a high degree of directedness.
Despite being highly directed, the bearings showed two types of bias. Firstly,
on average the direction of the bearings would have led the birds to a place
closer to the short wall near the goal than to the actual goal position.
Except for the mean bearing of birds using the left eye on the second test,
the home direction was outside the confidence intervals of the mean bearings.
Secondly, there was a systematic bias in monocular conditions. Birds using the
right eye tended to deviate to the right side, and birds using the left eye
tended to deviate to the left side. This tendency was profound in the first
trial, but considerably reduced in the second trial. Accordingly, the mean
bearing of controls was outside the confidence intervals of the bearings of
either eyecap group in the first test, while there was no difference in the
second test. The dispersion for the monocular conditions on the first and
second trial was symmetric. Analysis of the angular differences by ANOVA, with
eyecap treatment and trial order as repeated measures, showed a significant
effect of trial order (F1, 14=24.21,
P<0.0005), but no effect of eyecap condition (F1,
14=0.10, P>0.75), and no interaction (F1,
14=4.05, P>0.05). Birds reached the goal sooner when they
could use both eyes (Fig. 3),
but there was no difference between the left and right eye, and the patterns
in the first and second trials were the same. Accordingly, an eyecap condition
x trial order ANOVA revealed a significant effect of eyecap condition
(F2,26=36.92, P<0.0001), but no effect of
trial order (F1, 13=1.73, P>0.2), and no
interaction (F2,26=0.72, P>0.4). Pairwise
comparisons of the conditions of viewing showed that the birds deviated from
the binocular condition with the left (P<0.0001) and the right
(P<0.0001) eye, but that there was no difference between the
monocular conditions (P>0.75).
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Experiment 2
Experiment 2 tested for directedness of the initial orientation and for
possible differences in navigation performance between the right and left
brain hemisphere when the birds started from new positions. The results from
experiment 2 are given in Figs
4 and
5. All bearings were highly
directed. In the binocular condition, the vector length was r>0.95
from all new starting locations. For the left-eye only condition, vector
length was r=0.91 from point A; from the other points it was
r>0.95. In the right-eye only condition, vector length was
r=0.94 from point A, r=0.99 from point B, r=0.95
from point C, and r=0.88 from point D. As in experiment 1, there
appeared to be some general tendency to head for a location which was slightly
closer to the short wall of the room than the actual goal. This bias was
smallest from starting point B and largest from point C, but it was in the
same direction from all starting points and under all eyecap conditions.
Accordingly, confidence intervals of the mean bearings of birds using the left
or right eye always included the mean direction of binocular controls.
Confidence intervals included the goal direction from starting locations B and
D. From A, only the bearings of the left-eye only group did not differ from
the goal direction, and from location C all bearings were different from the
goal direction. As in experiment 1, birds reached the goal sooner in the
binocular condition than in the monocular condition. Although the extent by
which the monocular speed differed from the binocular speed varied among
places, the difference between the monocular conditions was never significant.
ANOVA with the eyecap condition as independent variable and binocular
versus monocular vision as a repeated measure showed no difference
between the right and the left eye for any starting position (A:
F1, 13=0.01, P>0.9; B: F1,
13=1.16, P>0.3; C: F1, 12=0.42;
P>0.5; D: F1, 13=0.17, P>0.6).
There was a significant effect of binocular versus monocular
performance at three positions (A: F1, 13=30.62,
P<0.0001; B: F1, 13=32.83,
P<0.0001; C: F1, 12=24.62;
P<0.0005). From position D, this effect was not significant
(F1, 13=2.25, P>0.1), but there was a
significant interaction (F1, 13=5.81, P<0.5),
which was due to a difference between the binocular condition and the left eye
(P<0.05), but not the right eye (P>0.4).
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Experiment 3
The effects of removing prominent landmarks (experiment 3a) and local cues
(experiment 3b) were tested. As in experiments 1 and 2, the bearings were
highly directed and were closely similar in experiments 3a and 3b; therefore,
only bearings from experiment 3a (Fig.
6) are shown. Vector lengths were r>0.95 for all
conditions. All confidence intervals included the goal direction, and all
bearings of monocular trials were the same as those of binocular control
trials. There were no differences in angular dispersion in experiments 3a
(F2, 24=0.92, P>0.4) or 3b (F2,
28=3.28, P>0.05). In experiment 3a, when the prominent
landmarks were removed for the first time, the birds took longer to reach the
goal when they were using the right eye
(Fig. 7a). ANOVA with eyecap
treatment as a repeated measure revealed a significant effect of eyecap
condition (F2, 28=59.52, P<0.0001). Pairwise
comparisons showed a difference between the binocular and the monocular
conditions (P<0.0001 for both), and a difference between the left
and the right eye occluded (P<0.005).
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Removal of the local cues in experiment 3b had no differential effect on the left and right eye. In the right-eye only condition, birds quickly adjusted to the changes of prominent landmarks experienced in experiment 3a, and under both monocular conditions performed at a similar level to the left-eye only condition in experiment 3a (cf. Fig. 7a,b). Accordingly, ANOVA with eyecap treatment as a repeated measure revealed a significant overall effect of eyecap condition (F2,28=16.73, P<0.0005), but pairwise comparisons showed no difference between the monocular conditions (P>0.75) (although both differed from the binocular condition: P<0.0005 for both).
Combined analysis of experiments 3a and 3b with both experiment and eyecap treatment as a repeated measure showed no overall difference between experiments 3a and 3b (F1,14=1.65, P>0.2), but there was a difference between the eyecap conditions (F2,28=36.82, P<0.0001), and a significant interaction (F2,28=4.48, P=0.02). Further comparison of the monocular conditions revealed a difference between right-eye only performance in experiment 3a and all other monocular scores (right-eye only, experiment 3b: P<0.005; left-eye only, experiment 3a: P<0.005; left-eye only, experiment 3b: P<0.01). Left-eye only performance in experiment 3a did not differ from left-eye only (P>0.5) or right-eye only (P>0.95) performance in experiment 3b.
Experiment 4
Experiment 4 tested the performance of the left and the right brain
hemispheres after moving the landmark array so that different goal positions
were predicted by the global reference frame and the prominent landmarks.
Birds started from two new positions, and they had highly significant bearings
from both positions that were directed towards the goal location predicted by
the global reference frame (G, Fig.
8). With the left-eye only, vector lengths were r=0.89
from point A and r=0.96 from point B, and with the right-eye only,
vector lengths were r=0.87 from point A and r=0.95 from
point B. All confidence intervals included the goal direction G, but not the
alternative direction G', and the mean bearings predicted the location
of G almost perfectly. Consistent with this, the birds reached the goal region
quickly, and there was no difference between the left and the right eye
occluded (F1,14=0.57, P>0.4) in the time the
birds needed (Fig. 9). There
was, however, a considerable difference in the subsequent search pattern
between the two monocular conditions. When the birds used the left eye, they
stayed close to the area of the goal predicted by the global reference frame
during the whole search period. When using the right eye, birds tended to
continue to search further away from G, and much of this additional search was
near the location of the goal predicted by the prominent landmarks. This
difference in search activity was reflected in a path length that was about
60% greater in searches with the right eye only
F1,14=10.57, P<0.01)
(Fig. 9).
Fig. 10 shows the distribution
of search activity along the two main axes of the arena. Along the short axis,
where the predicted peak of activity was the same for G and G', the peak
for the left-eye only condition was sharper, but the difference of activity
allocated to the target region was not significant between the right and the
left brain (Wilcoxon test: Z=-1.36, P>0.1). Along the long axis of
the arena, birds almost exclusively searched at and around the location
predicted by the global reference frame when using the left eye only, and
there was virtually no search at the site predicted by the prominent
landmarks. When the right eye only was used, the peak of search was at G, but
the birds also searched at G'. Statistical comparison of the search
activity at both possible goal locations showed no difference at G (Z=-0.540,
P>0.5), but there was a significant difference between use of the
left and the right eye only at G' (Z=-2.557, P<0.01).
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Discussion |
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The ability of pigeons to determine fairly exact bearings from new
locations is of interest with regard to other laboratory studies as well as to
the possible role of visual cues during homing under natural conditions.
Laboratory studies have shown that the distances and directions to individual
landmarks are of paramount importance for the pigeon's use of landmark
information (Cheng, 1988). The
present study shows that not only can pigeons find places at a certain
distance and direction from landmarks, but also that they can determine the
direction towards a place of interest from new remote locations. This raises
the possibility that pigeons use a global reference frame (for example, with
coast lines and mountain chains as boundaries) to visually determine the home
direction from new places in the field.
In experiments 1, 2 and 3, which tested performance not only with the right
or left eye, but also with both eyes, binocular performance was clearly better
than monocular performance. This differs from the pattern observed when
discriminating for natural food
(Güntürkün et al.,
2000), but resembles findings observed when orientating in a maze
(Prior and Güntürkün,
2001
), suggesting that, at least in a rather complex spatial
environment, performance levels might profit from a panoramic view that
integrates visual input from both eyes. This does not preclude the
possiblility that under certain natural or experimental conditions the cues
available to one hemisphere might be sufficient for maximum performance, or
that binocular performance could even be impaired if environmental cues
provide conflicting information.
The high directedness in experiment 1 is not surprising, because the pigeons had been trained in that direction, and the possibility could not be excluded that the pigeons simply learned to move parallel to the long axis of the arena until they came close to the goal. However, the results from experiments 2 and 4 suggest the learning of a very accurate representation of where the goal is located relative to the global reference frame or the prominent landmarks.
An interesting finding from experiments 1 and 2 is that the pigeons
appeared to misrepresent the exact goal position in a manner that resembles a
classical `release site bias' (Keeton,
1973). Such a bias can apparently develop on the basis of a purely
visual relational framework. It is not yet clear why this bias was small or
virtually absent from some positions and fairly strong from others. Based on
the bias observed at the new site C, one might be tempted to assume that
orientation from a new site might be more difficult if the direction is
approximately opposite to the training direction. But the bearings from the
corresponding site D show nearly perfect orientation towards the goal.
Overall, two points about the `release site bias' are noteworthy. Firstly, the pigeons appeared to improve their directional orientation during repeated testing from different positions. While there was a systematic bias in departures from the familiar start position in experiment 1, directional orientation was almost perfect in experiment 3. Similarly, birds show almost perfect directional orientation from two new locations in experiment 4. Secondly, if a bias occurred it had the same direction and degree under the different eyecap conditions.
Regarding the question of lateralization, the results provide a clear-cut picture. Firstly, neither hemisphere appears to make use of local visual cues. Changing local features had no effect, perhaps because birds are predisposed to learn cues, which are more reliable under natural conditions. Local cues at short range, provided by the colour of the vegetation, can change rapidly. In terms of a differential contribution of the left and right brain hemisphere, the results do not support a pattern of contrasting hemispheric specialization. Experiment 2, where the birds had to orient from new places, showed that the left hemisphere is quite skilled in using a global geometric frame or prominent landmarks to determine the direction to the goal. Of course, determining a direction could be done by different processes, so the strongest evidence for analogous mechanisms in both hemispheres is the virtually identical `release site bias' under all conditions of viewing. Also in the peak of search activity with no goal, the parameter usually evaluated in other laboratory studies, the left hemisphere demonstrated high competence in finding this place immediately by means of a relational, mainly geometric reference frame. The difference between the hemispheres was that the left brain hemisphere attended to conspicuous object cues and the right brain hemisphere did not. Based on these findings the following model of visuo-spatial lateralization in pigeons is likely. Both brain hemispheres have a module that enables the birds to determine the direction to places, and to find places by means of a global reference frame, but the left hemisphere is considerably more specialized for the processing of object properties. Consequently, the choice of cues to be followed during monocular tests depends on intrahemispheric competition. If the right hemisphere is tested, global spatial cues are the only salient clues. If the left hemisphere is tested, the module for global spatial cues and the module for object cues compete for control of the task. If both types of cues predict the same location, they act in synergy. If the predicted locations differ, either a mixed pattern is observed, or the orientation along object cues might become dominant.
The results from experiment 4 are quite revealing. There was a similar tendency for both hemispheres to use the global spatial reference frame in the first place. With either eye/hemisphere the birds demonstrated an exact bearing from a new starting location towards the (non-visible) target area predicted by the global reference frame. Only later did a clear hemispheric difference emerge. For the right brain hemisphere, the location predicted by the global reference frame was the only site of interest. When the goal was not found at the expected site, they continued to search in the close vicinity. This led to a comparatively short search path and a plateau-like search maximum along the long axis of the arena, which included the location of the expected target and closely adjacent patches. For the left hemisphere, an alternative location was possible, and when the expected goal (G) was not found, the search was extended to the site predicted by the alternative cues (G'). The amount of search activity at G' is clearly smaller than the amount of search activity at G as both hemispheres initially preferred the area of G. But since the birds did at least some searching at G' when using the right eye and virtually no searching when using the left eye, a clear and significant dissociation between the conditions emerged.
One note of caution: although the results clearly show that both
hemispheres are highly competent in finding a place by a global reference
frame only, there is still the possibility that the overall importance of the
prominent landmarks would have been higher and the tendency of the left brain
hemisphere to attend to them would have been greater if the global reference
frame had been less stable. Previous studies on the use of landmarks often
tried to diminish the salience of a global reference frame by shifting the
landmark array during training (e.g.
Spetch et al., 1997). And it
has been shown that the reliability and stability of local versus
global cues do have an influence on the choice of cues by the birds
(Gould-Beierle and Kamil,
1996
; Kelly et al.,
1998
). Similarly, there is the question of whether the birds would
have responded differently to local cues if there had been landmarks of
natural vegetation, such as little shrubs. On the other hand, the basic design
of the present study corresponds to a natural situation, with a highly stable
global reference frame, less reliable prominent landmarks, and frequently
changing local cues. That pigeons showed no evidence of using the
short-distance local cues might reflect a natural readiness to use of cues,
which are probably reliable. Therefore, the pattern of hemispheric
contribution observed in the present study is likely to occur in natural
environments.
The pattern of lateralization suggested by the findings of the present
study and supported by the findings from maze learning in pigeons
(Prior and Güntürkün,
2001) indicates a well-developed capacity for orientation
according to global cues in both hemispheres and an additional capacity for
attending to and memorizing conspicuous objects in the left hemisphere, in
contrast to suggestions that the right avian brain shows general superiority
for topographical information (Andrew,
1991
; Bradshaw and Rogers,
1993
). Therefore, a brief comparison with the main findings in
other avian models is appropriate. There are three avian models of cerebral
asymmetry in spatial memory: the pigeon, the chick, and pairs of food-storing
and non-storing passerine birds. Evidence in chicks is mixed. An early study
with rotation of the experimental array during tests suggested that
orientation according to global topographical cues when using right eye/left
hemisphere is random, whereas when using left eye/right hemisphere orientation
is good (Rashid and Andrew,
1989
). However, later studies indicated that orientation along
global spatial cues using right eye/left hemisphere is also possible. A recent
study using a test similar to experiment 4 of the present study, in that the
subjects had to recall a site from reference memory after a landmark was moved
so that global geometric information and landmark information predicted
different sites, birds using the right eye only searched in a slightly larger
area after landmark translation, but nevertheless showed fairly good
orientation according to global geometric cues
(Tommasi and Vallortigara,
2001
). Thus, the searching pattern of the chicks was similar to
that of the pigeons in the present study, and fairly consistent with the model
of lateralization we propose. On the other hand, studies in chicks using a
working memory task (Vallortigara,
2000
) suggested a pattern of lateralization resembling those
observed in a working memory task in passerine birds (see below). Therefore,
further studies are needed to clarify the extent by which differences between
avian studies are due to the species or due to specific task demands.
Comparisons with studies in passerine birds require caution as the tasks
conducted by these birds are not equivalent in the type of spatial memory
involved. In experiments with passerine species, birds had to relocate sites
with food items unique to the trial. In some studies with food-storing birds,
food items had been stored by the experimental subjects themselves. In other
studies, mainly designed to compare storing and non-storing species, birds
learned the location of a food item placed by the experimenter. In terms of
lateralization, both procedures yielded similar results, so they will be
discussed together. In a first series of experiments
(Clayton, 1993;
Clayton and Krebs, 1993
), which
did not evaluate in detail the nature of the spatial cues involved, it was
shown that after retention intervals of up to 3 h, information could be
retrieved with the right as well the left eye, but that after 24 h or longer,
information was only accessible when the right eye/left hemisphere was in
control of the task. There was a difference between a storing species, the
marsh tit, and a non-storing species, the blue tit, in that marsh tits
remembered information acquired via either eye while blue tits only
remembered information acquired with the right eye. If a similar pattern also
occurred during long-term retention of a particular site, as required in the
food-searching tasks in chicks and in the present study, passerine birds
should be able to relocate the goal when using the right eye, but not when
using the left eye, i.e. they should show a pattern different from both chicks
and pigeons. It has to be considered, however, that remembering a trial-unique
feeding location (the passerine's working memory task) and retention of a
stable site in reference memory might involve different brain systems.
A second series of experiments with storing and non-storing passerine birds
evaluated the role of different cues that might guide the birds' relocation of
a feeding site. In brief, birds had to remember where a food item was placed
in one of several feeders. Each feeder could be identified by one of two types
of cue, a global topographic cue (location within the experimental room) and a
colour cue on each feeder. Short retention intervals of 5 min were used. In
phase 1 of a trial, birds learned which feeder contained food. Before phase 2
of a trial, two of the feeders were swapped so that the positions predicted by
global spatial and colour cues were different. When using the left eye, birds
of all four species tested (marsh tit, blue tit, jay, jackdaw) made their
first choice according to the global cues. When using the right eye, all
species used the colour cues (Clayton and
Krebs, 1994). Data from the first choice made by the birds were
consistent with the assumption that both brain hemispheres show good
orientation according to global cues, and that the left brain has an extra
capacity for processing local cues, which may guide searching behaviour if
they are salient enough. A consequence of this assumption, however, would be
that birds using the right eye should search at the correct spatial location
on their second choice (as the right-eyed pigeons in this study, which
searched at the correct landmarks after not finding the goal at the location
visited first). This was not the case, however, as the second choice of
passerines with the right eye was random
(Clayton and Krebs, 1994
).
Again, possible differences in the type of task have to be considered. It
might be that passerines have a different pattern of lateralization of spatial
capabilities than chicks and pigeons. Together, the results from different
studies suggest that both species and task are important for the pattern of
lateralization observed. Therefore, further comparative studies with different
species and tasks are needed for a more detailed understanding of avian brain
lateralization.
Overall, the results from the present study further support the view that lateralization of spatial orientation in birds depends on a complex interplay of mechanisms in the left and right brain hemisphere. The present study shows that, at least in pigeons, visuo-spatial orientation along a global reference frame is performed skilfully by either brain hemisphere.
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