The binding and recall of snapshot memories in wood ants (Formica rufa L.)
School of Life Sciences, University of Sussex, Brighton, BN1 9QG, UK
* Author for correspondence (e-mail: t.s.collett{at}sussex.ac.uk)
Accepted 27 October 2003
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Summary |
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We approached this question by training ants to find food midway between two upright black cylinders of different sizes and then examined where they searched when they were given two cylinders of the same size. If the ants know which cylinder replaces the small cylinder and which the large, they should search at a position where the two equal-sized cylinders subtend the same angles as do the training cylinders when viewed from the feeder. Ants conformed to this prediction under one condition, searching at a shorter distance from the substitute for the large cylinder than from the substitute for the small cylinder. But, under another condition, ants were unable to distinguish between the two equal-sized cylinders. Ants failed when white curtains completely surrounded the platform on which the cylinders were placed. They succeeded when one side of the platform had a patterned curtain.
We suggest that ants take two snapshots at the feeding site, one when facing the small cylinder and one when facing the large cylinder, and that each snapshot includes the patterned curtain, if it is there. Ants will view the patterned curtain with the lateral retina of one eye when facing the small cylinder and with the lateral retina of the other eye when facing the large cylinder. Our data suggest that there may be associative links between these spatially separate components of the snapshot, which cause the memory of the small cylinder or the large cylinder to be recalled according to which eye sees the curtain. It seems that an extended snapshot not only enhances the accuracy of localisation but can also increase the reliability of snapshot recall, provided that the components of a snapshot are bound together.
Key words: wood ant, landmark guidance, snapshot, binding, configural learning, navigation
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Introduction |
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Contextual cues like the surrounding panorama, or perhaps an insect's
motivational state, seem to prime the recall of appropriate snapshots
(reviewed by Collett and Collett,
2002). The problem we investigate here is how ants might select
between snapshots within a single context. Does the recall of a snapshot just
depend on recognising the landmark that is fixated, or do other regions of the
snapshot contribute to recall? And are the different spatial regions of a
snapshot linked together so that each component of a snapshot can prime the
recall of other components? We have approached these questions by analysing
the behaviour of ants that are trained to a food site that lies midway between
two cylinders of different sizes and then tested with two cylinders of the
same intermediate size. Since it is unlikely
(Zollikofer et al., 1995
) that
the second cylinder is visible when the ant fixates the first cylinder,
questions arise as to whether ants store independent views of the large and
small cylinders, and, if so, what cues are employed to recall the correct
memory when ants face a particular cylinder. In tests with similar-sized
cylinders, accurate recall cannot be accomplished by relying solely on the
appearance of the cylinder. Other cues are required. This experiment was
therefore performed under two conditions. In the first condition, the
rectangular arena on which the experiment was conducted was entirely
surrounded by white curtains, thus minimising extra array cues. In the second
condition, the curtains on one side were patterned, so as to provide a strong
additional cue.
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Materials and methods |
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Apparatus
Experiments were performed in a 2.7 mx4.8 m rectangular arena with a
white plastic floor that was illuminated by banks of high-frequency
fluorescent lights fixed above a false translucent plastic ceiling. The
position on the floor of a glass microscope slide with a drop of sucrose on it
was marked by two upright black cylinders
(Fig. 1). The arena was
completely surrounded by floor-to-ceiling curtains. These were either all
white or one side was patterned with randomly arranged black shapes, each of
which subtended at least 5° when viewed from the starting point. The
patterned curtain covered the side of the arena that the ants approached so
that when ants were close to the food the cylinders were always viewed against
a white background (Fig.
1).
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When ants were trained with cylinders of unequal sizes, two groups of ants were used. One group had the smaller cylinder on their left and the other had it on their right. When there was a similar asymmetry in tests, two sets of tests were given with the smaller cylinder to one side in one test and to the other in the second test. Data from the two experiments or test types have been made compatible and then pooled.
Video recording
The ants' trajectories in tests were tracked with a fixed camera hidden in
the false ceiling 3 m above the centre of the arena. It was convenient to move
the cylinder array to one of three standard positions on the arena floor
before each unrewarded test. The test positions were not used in training. The
camera (Sony EVI-D30) has movable optics, allowing a high-resolution image of
any part of the arena to be captured. The camera is controlled by a PC
(Pentium II 233 MHz)running custom software
(Fry et al., 2000). The system
extracts the ant's position and longitudinal orientation at 50 Hz. Before
analysis, the output was smoothed by taking a moving average with a window
size of nine frames. The ant's path was recorded for 6 min or until the ant
approached so close to one of the cylinders that the tracking system `lost'
the ant.
Data analysis
The results are mostly presented as two-dimensional distributions in which
individual data points are not independent. For statistical tests between
distributions, each individual test trial from an ant was summarised to give a
single data point, and comparisons were made between populations of these data
points. Search distributions were compared by recording the mean position of
an ant along the line connecting the landmarks for each test trial, using
these mean `X positions' as independent data points. Note this test does not
provide statistical information about the position of the peaks of the
distributions. The relative fixation of the two cylinders during each of the
approaches of Fig. 5
wascalculated as the number of frames in which the ant fixated
(±20°) one cylinder divided by the number of frames in which the
ant fixated the other cylinder.
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Results |
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Evidence that ants facing a particular cylinder position themselves
relative to that cylinder comes from a test in which each cylinder indicated a
different search position. In training, the food was midway between two
cylinders of the same size (15 cm in diameter and 45 cm high) separated by 70
cm. Ants searched accurately when tested with this configuration
(Fig. 3A). Tests were then
given with cylinders of half the size (7.5 cmx22.5 cm) separated by 70
cm. If ants used the apparent size of each cylinder to control their search,
they should search in two positions, at 17.5 cm from each cylinder, which is
roughly what they do (Fig. 3B).
The data of Fig. 3C,D show that
the peak associated with each cylinder is generated primarily when the ants
face that cylinder, further supporting the hypothesis
(Judd and Collett, 1998;
Nicholson et al., 1999
;
Durier et al., 2003
) that ants
record snapshots when facing a landmark. Since the two training cylinders have
the same angular size when viewed from the goal, it is not clear whether the
ants have acquired a separate snapshot for each cylinder or whether they have
a single snapshot that they can apply to either cylinder.
Ants trained with a large and a small cylinder
What happens when the two cylinders viewed from the food site have
different angular sizes? Do ants learn a separate snapshot for each cylinder?
We trained ants to a food site that lay midway between a small cylinder (5 cm
in diameter and 15 cm high) and a large cylinder (15 cm in diameter and 45 cm
high) that were 93.4 cm apart. Two separate experiments were performed with
this arrangement of cylinders. In one experiment, the curtains surrounding the
rectangular experimental arena were all white. In the other experiment, a
black-and-white, patterned, floor-to-ceiling curtain was hung along the wall
that the ants faced as they approached the cylinders
(Fig. 1), so that when an ant
turned to face the cylinder on its left, the curtain would be seen by its
right eye, and vice versa. Ants were tested both with the training
configuration and with cylinders of intermediate size (7.5 cmx22.5 cm)
separated by 93.4 cm.
In the experiment with white curtains, ants tested with the training array searched in roughly the predicted position (Fig. 4A). In tests with medium-sized cylinders, the peak of the search distribution shifted a little way towards the medium-sized cylinder that replaced the large cylinder (Fig. 4B). But the peak was still a long way from the predicted site.
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These results cast doubt on several hypotheses. (1) Ants learn the apparent size of only one cylinder viewed from the goal, which they try and match to both the large and the small cylinders. If this were the case, ants searching between the two medium-sized cylinders should generate two search peaks rather than one. (2) Ants acquire a single snapshot that mixes the two cylinders (e.g. a superposition of two attractors, producing a minimum that is located in an intermediate position). According to this hypothesis, the peak of the search distribution should not be close to the predicted feeding site in tests with the training cylinders. (3) Ants learn two snapshots, one for each cylinder, and recall them appropriately. Had this been the case, the search peak should have been in the predicted location in tests with the medium-sized cylinders. (4) Ants learn the appearance of the two cylinders correctly but cannot identify them accurately in tests with either pair of cylinders. According to this hypothesis, the search peak would have been incorrectly positioned in tests with both the training and the medium-sized cylinders. One hypothesis that is consistent with the results of Fig. 4 is a variant of hypothesis (4) above: ants learn the two cylinders correctly and can usually identify them correctly in the training conditions in a direct approach from the starting point, when the cylinders can be recognised by their size. But ants are more likely to misidentify the cylinders when they are the same size, so that extra supporting cues are needed for their recognition.
With the white curtains, too little information may have been available for disambiguating the two test cylinders. The additional cue given by the patterned curtain dramatically changed the position of the ants' search peak. The ants now searched in the expected position with the training cylinders (Fig. 5B) and they searched close to the predicted position when tested with the medium-sized cylinders (Fig. 5D). These results are consistent with the ants recognising the cylinders correctly.
The ants' search behaviour when trained with the patterned curtain is
reflected in their approaches to the food site. In tests with the training
cylinders, ants walked relatively straight to the goal and tended to fixate
the two cylinders with roughly equal frequency
(Fig. 5A). Ants fixated the
larger cylinder more than the smaller cylinder in approximately half of the
approaches (28 out of 61 approaches, P>0.1, sign test). When
approaching the medium-sized cylinders
(Fig. 5C), ants fixated the
cylinder that replaced the large cylinder more often (64 out of 91 approaches,
P<0.01, sign test) than that replacing the small cylinder. This
behaviour is consistent with the ants tending to fixate landmarks that are
smaller than their expected size as viewed from the feeding site
(Durier et al., 2003).
Likewise, the overall direction of the ants' approach was aimed at the feeding site in tests with the training cylinders. In tests with the medium-sized cylinders, the approach was biased slightly, but significantly, towards the cylinder that replaced the large one. The mean of the distribution of points at which each trajectory intersected a line parallel to and 5 cm in front of the line between the cylinders was almost midway between the training cylinders (mean ± S.D.=0.07±10.4 cm, N=59, where 0 cm is the midpoint). With the medium-sized cylinders, the intersection points shifted towards the substitute for the large cylinder (mean ± S.D.=5.8±12.6 cm, N=90). The two distributions differ significantly (Wilcoxon test, t=3.00, P<0.01).
Taken together, the searches and approaches suggest that (1) ants
identified the two training cylinders, (2) they knew which medium-sized
cylinder corresponded to which training cylinder, and (3) on their approach to
the medium-sized cylinders they fixated preferentially the cylinder that
appeared smaller than its expected size when viewed from the feeder
(Durier et al., 2003).
Ants trained with the white curtains behaved somewhat differently. Ants approaching the training cylinders fixated the small cylinder significantly more frequently than the large cylinder (37 out of 53 approaches, P<0.01, sign test), suggesting that without the patterned curtain they often misidentified the training cylinders. However, in tests with the equal-sized cylinders, they approached the medium-sized cylinder replacing the large training cylinder more than the other medium-sized cylinder (43 out of 57 approaches, P<0.01, sign test), indicating that, to some degree, these ants do know which cylinder is which.
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Discussion |
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There are three rather different ways in which ants might use the patterned
curtain to identify the medium-sized cylinders correctly. The first is to
store two snapshots at the feeder site, one for each cylinder, and to use the
retinal position of the image of the curtain to help decide which snapshot to
recall. The second is to store just one snapshot when fixating one cylinder
and ignore the other cylinder, again using the retinal position of the curtain
to distinguish between the cylinders. The third is to store one snapshot and
to use the patterned curtain as a polarising or compass cue that tells the
ants what orientation they should adopt when they search close to the food
site (c.f. Åkesson and Wehner,
2002; Collett and Baron,
1994
). The data of Figs
3 and
4 suggest that in some
situations both cylinders do contribute to the ants' search. The evidence that
both cylinders contribute to the ants' behaviour in the experiment with the
patterned curtain is no more than circumstantial. It comes from the roughly
equal fixation of the two cylinders in approaches to the training array, which
suggests that each cylinder is identified correctly. There is also no evidence
that, when the ants search close to the usual feeder site, they fixate one
cylinder more than the other or that their pattern of fixation differs with
the presence or absence of the patterned curtain. In principle, direct
evidence of two snapshots could be obtained by separating the medium-sized
cylinders as in Fig. 3C,D. The
hypothesis would then be supported if individual ants searched at a different
distance from each cylinder. Unfortunately, the search behaviour of individual
ants was too erratic for this test to be feasible.
What we can say with certainty is that the curtain was essential for ants
to identify the medium-sized cylinders correctly. By fixating one or other
cylinder, the ant determines the retinal positions of other visual features in
the room. We suggest that these simultaneously viewed features, with retinal
position as one parameter, are bound together into a single snapshot.
Specifically, when facing and learning the appearance of one cylinder, the ant
also learns the retinal position of the patterned wall and forges associative
links between these two components of the snapshot. The view of the patterned
wall in a particular retinal position when ants face one or other cylinder can
then help them recall the correct memory and identify the cylinder that they
are facing. The failure of ants to search correctly when the surroundings are
all white and the landmarks are identical supports the hypothesis of such an
associative link between memories of the peripherally viewed wall and the
centrally viewed cylinder. In general, associative links between spatially
separated parts of a snapshot will make recognition more robust. In recent
years, there have been a number of studies showing that bees can form
associative links between different visual stimuli (Srininvasan et al., 1998;
Zhang et al., 1999;
Giurfa et al., 2001
) and that
the same visual stimuli can be bound together in different combinations in
different contexts (Fauria et al.,
2000
). The present study indicates that associative links may be
formed between items viewed simultaneously by different regions of the retina.
We suggest that learning an extended, as opposed to a narrow, snapshot can
have two somewhat separate benefits. First, it improves an insect's precision
in locating a goal, as demonstrated earlier
(Cartwright and Collett, 1983
;
Wehner et al., 1996
;
Durier et al., 2003
). Secondly,
an extended snapshot, with binding between its components, enhances the
reliability of snapshot recall.
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Acknowledgments |
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