Switching destinations: memory change in wood ants
Sussex Centre for Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
Author for correspondence (e-mail:
t.s.collett{at}sussex.ac.uk)
Accepted 21 April 2004
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Summary |
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Key words: wood ant, Formica rufa, route, snapshot memory, re-learning
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Introduction |
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In the present paper, we start by examining the directionality of snapshots. Do snapshots recorded at a goal only attract ants over a small range of directions? We approach the question by testing the ants' ability to reach a goal from different starting points. We then analyse a wood ant's changing paths, as it switches from feeding at a familiar site to feeding at a new one. How does an ant adjust the use of its visual memories of the two sites as it gains experience of the second site? What can an ant's path reveal about the dynamics of memory recall during a route and to what extent does an ant emphasise different snapshot memories at different stages of its route?
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Materials and methods |
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Apparatus
Experiments were performed within a rectangular arena (2.7 mx4.8 m)
surrounded by floor-to-ceiling white curtains and illuminated by banks of
high-frequency fluorescent lights fixed above a false translucent plastic
ceiling. The ants' trajectories were tracked with a fixed video camera hidden
in the false ceiling 3 m above the centre of the test arena. The camera (Sony
EVI-D30) has movable optics, allowing a high-resolution image to be captured
of any part of the arena. 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 a cylinder in the arena
that the tracking system `lost' the ant.
Experimental procedures
Foragers were normally released at a fixed starting point
(Fig. 1) close to a triangular
arrangement of cylinders (45 cm high x 15 cm in diameter). Since the
triangles were kept in the same position in the arena throughout the
experiments, we cannot say which landmarks guided the ants' paths. The
surrounding curtains, the overhead lights and the cylinders could all have
played a role. Over a sequence of trials, ants learnt to collect sucrose
solution from a microscope slide at a site 100 cm away (F1). After
30 visits to this site, the position of the feeder was switched. The line
connecting the feeder and starting point was rotated through 45°, so
defining the position of a second food site (F2). The last 35 visits to
F1 and most of the 30 subsequent visits to F2 were recorded. In some cases,
the experiment was speeded up by recording every other path for the first 10
runs after the switch. For a few trials after the switch to F2, ants were
helped in their search for the new food site. Once the recording session was
finished, we tapped the floor with our fingers a few cm in front of the ant
and it would usually follow our fingers to the food. Also to shorten the
experiment, ants were taken from the sucrose before they had finished feeding,
were placed in a container and the next ant started. After a group of about
five ants had been collected from the feeder, the group was replaced on the
sucrose and allowed to return to the starting position, from where the ants
were taken to the nest.
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The floor was washed periodically with water and alcohol to reduce odour cues. We could see no signs that our results are biased by chemical cues. Ants did not take the same route from one trial to the next or follow each other's routes. Ants frequently missed the feeder by a few cm and searched for it with no sign that they were attracted there by scent.
Analysis
The starting direction of each path (the first segment, b in
Fig. 1) was determined by the
direction of the line between the start and a point on the path, 30 cm from
the start. Many paths had a similar overall shape (e.g.
Fig. 3) in which a roughly
straight initial part was followed by a sharp turn, after which the second
part of the path was again roughly straight. The position of the turn was
determined by eye. The direction of the path after the turn (the second
segment, c in Fig. 1) was
determined in the same way as the direction of the first segment. The
principal axes of the ellipses in Fig.
6 werecomputed as described by Sokal and Rohlf
(1995, p. 586).
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Results |
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Ants (Cataglyphis sp.) are known to use path integration to
perform novel routes (e.g. Müller and
Wehner, 1988; Schmidt et al.,
1992
; Collett et al.,
1999
). They probably do so by subtracting the coordinates of their
current position, which they have obtained through path integration, from
those of the goal, which they have learnt on an earlier occasion
(Collett and Collett, 2000
).
The results of Fig. 2, in which
wood ants are displaced to a new site and so are deprived of accurate
knowledge of their current position, cannot be explained by path integration.
The ants' behaviour suggests instead that they were guided to the goal by
snapshot memories stored there. This behaviour reinforces the argument
presented in an earlier paper (Durier et
al., 2003
) that wood ants recall snapshots stored at the goal well
before reaching it. In interpreting the experiments that follow, we assume
that a direct path segment to the first (F1) or to the second feeding site
(F2) indicates that the ant is using a snapshot memory stored at F1 or F2,
respectively.
Ways of reaching the second feeder (F2)
Ants were given 30 trials with the food at F1, the food was then switched
to F2 and a further 30 trials were given. As the training to F2 progressed,
ants took a variety of routes to reach the new site.
Fig. 3 shows examples of the
changing paths of two ants. The first segment of one ant's path was directed
roughly at F1 throughout training (Fig.
3A). At some point on the way to F1, the ant turned sharply and
aimed at F2. These paths suggest that the start of the ant's trajectory was
set by a snapshot associated with F1 and that the trajectory later switched to
being driven by a snapshot associated with F2. This ant seemed to acquire a
two-stage route to F2 that may have been controlled by the sequential
activation of two snapshots.
The other ant illustrates a more commonly found pattern, in which the direction of the first segment of the trajectory rotated as learning progressed (Fig. 3B). For the first few trials, the first segment pointed at F1. It then gradually rotated to point more in the direction of F2. The initial segment was again often followed by an obvious turn towards F2. Turns were identified in 62.2% of the recorded paths of all ants. Analysis of walking speed before, during and after these turns indicates that ants did not slow down at the turn but that they transiently speeded up immediately afterwards.
The second segment
In the present paper, we focus on the portion of the path following the
turn (second segment). As training progressed, trajectories after the turn
were aimed more accurately at F2. Histograms of the directions of the second
segment are shown in Fig. 4A
over successive blocks of 10 trials. Directions are plotted as the angular
difference between the ant's heading and the direction of F2 from the turning
point. The accuracy with which the segments were aimed at F2 improved
significantly over the three blocks of trials, and the distance from the start
to the turn dropped (Fig.
4B).
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The second segment pointed directly at F2 at a stage in training in which
the direction of the first segment was still rotating, with the consequence
that the position of the turn varied. This variability allowed us to infer
whether during the second segment the ants were attracted to F2, headed in a
fixed direction or turned through a fixed angle. The best-controlled parameter
should be associated with the smallest standard deviation. We therefore
computed for each ant, over trials 525, the standard deviations of (1)
the angular difference between the direction of the second segment and the
direct path to F2 from the turn (angle in
Fig. 1), (2) the absolute
heading of the second segment and (3) the turn size as given by the angular
difference between the ant's overall direction from start to turn and the
direction of the second segment (angle
in
Fig. 1). The standard deviation
of (1), i.e. the precision of aiming at F2, was smaller than that of both (2)
and (3) for 12 out of 13 ants (
2=9.31, P=0.002),
supporting the conclusion that the controlled parameter is attraction to
F2.
A related question is whether those second segments that are aimed towards F2 tend to lie along the direct route between F1 and F2. To obtain an answer, we measured, relative to the direct path from F1 to F2, the directions of all those second segments, in trials 11 to 30, which were within 20° of F2. The observed distribution (Fig. 4C) has a mode at zero indicating that some paths do indeed lie along the F1 to F2 route. However, the distribution is not normal (KolmogorovSmirnov test, z=1.471, P=0.026) and the directions of 48% of the segments differed by more than 30° from the direct route between F1 and F2. Thus, the ants were not simply performing a fixed route between F1 and F2, but they could be attracted to F2 from different directions.
Interactions between first and second segments
The changing direction of the first segment (e.g.
Fig. 3B) may suggest that there
is increasing control of that segment by F2 as training progresses. Similarly,
the second segment is aimed more precisely at F2 with increasing number of
trials. Is there a trial-by-trial variation in the strength of control by F2
that is expressed jointly in the first and second segments? Our first step in
answering this question was to classify the trajectories in the following way.
The first segments were placed into one of three categories: directed at F1,
directed neither at F1 nor at F2, and directed at F2. The first two of these
categories were then sub-divided into whether or not a second segment was
aimed within ±20° of F2. In Fig.
5, this classification is shown separately for successive blocks
of 10 trials.
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The proportion of trials in which the first segment was aimed at F2
increased with training. By the last block of trials, 45% of first
segments were directed at F2. The proportion of trials in which the second
segment was directed at F2 also rose with training. The proportion did not
depend on whether or not the first segment was aimed at F1 or neither at F1
nor at F2. Over the three blocks of trials, the percentage aimed at F2 was,
respectively, 13.4%, 50.8% and 66.7%, when the first segment was directed at
F1, and 0%, 45.2% and 50%, when the first segment pointed neither at F1 nor at
F2. Thus, the accuracy of aiming the second segment at F2 is not obviously
related to the direction of the first segment.
We have also plotted for each trial the direction of the second segment
against the direction of the first segment. Directions are given in terms of
the angular difference between the first or second segment and the direction
of F2 from the start or the turn, respectively ( and ß in the
inset to Fig. 6). Plots are
shown separately for each block of 10 trials. The conclusion from this
graphical analysis is also that there is no trial-by-trial correlation in the
magnitude of control that F2 exerts in the first and second segments. Thus,
the development of accurate control of the second segment by F2 seems to be
independent of the details of the first segment.
Displacement during training to F2
We know from Fig. 2 that
ants can reach a goal directly by a novel route. Since they do so after
displacement, their novel routes cannot be explained through path integration
but must involve the use of visual cues, and most likely snapshots stored at
the goal. The same argument cannot be extended automatically to cases of
retraining. Ants could, in principle, recall the path integration coordinates
of F2 relative to their fixed starting point and use this information to help
determine their route after the turn. We therefore performed displacement
experiments on ants during retraining. Although such experiments can show that
visual cues are sufficient to guide an ant to F2, they cannot, of course, show
that path integration makes no contribution to the ant's normal
trajectories.
Ants were trained for 30 trials to F1 and then retrained to F2 for a
further 10 trials, starting as usual from the same place on each trial (T in
Fig. 7A). Each ant was then
given six tests, starting alternately 15° anticlockwise (D1 in
Fig. 7A) or 30° clockwise
from the training position (D2 in Fig.
7A), with F2 as the centre of rotation. A few test trials were
aborted because ants were attracted to the cylinder nearest the release
point.
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In test trajectories with a sharp turn, the direction of the second segment
often pointed roughly at F2. If ants were to rely primarily on path
integration to plan a trajectory to F2 and assumed that they were starting
from their accustomed position, the second segment of their trajectories would
not point in the direction that the ants intended
(Fig. 7C). Their intention
could then be made apparent by shifting the trajectories through the vector
that connects the actual release site (D1 or D2) to the ants' normal starting
point (T). Fig. 7D shows, for
each trajectory, the angular difference between the direction of the second
segment and the direction of F2 plotted against the same angular difference
computed after the start of the trajectory has been shifted to T. The data
points will lie below or above the diagonal, depending on whether the paths
are determined primarily by a snapshot or by path integration, respectively.
The data points fell significantly below the diagonal, supporting the
hypothesis that ants aimed at a snapshot-defined goal (20 out of 29,
2=4.172, P=0.041).
Five ants were each given two final tests from a third start position (D3) that was rotated 100° from the normal start (Fig. 7B). Although the sample is too small for statistics, it is clear that more than half of the trajectories from D3 were directed at F2, indicating that the ants were guided directly to F2 by visual landmarks specifying that site.
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Discussion |
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The data of Fig. 7B show
ants approaching a goal from a broad range of directions (>100°). How
do ants accomplish this feat if, as increasing evidence suggests
(Judd and Collett, 1998;
Nicholson et al., 1999
;
Durier et al., 2003
;
Graham et al., 2004
), they
record snapshots when facing conspicuous landmarks and their direction of
travel is predominantly forwards? A single snapshot stored at the bottom of a
circularly symmetric object, such as a cylinder or cone
(Judd and Collett, 1998
), can
attract an ant from many directions, but more typically a single snapshot will
only be matchable to a scene when the ant faces and moves in roughly the same
direction in which the snapshot was stored. One solution to this problem is to
store several snapshots at a single location, each taken when facing in a
different direction (Cartwright and
Collett, 1983
). There is evidence from ants trained to a feeding
site between two cylinders of unequal sizes that the ants store two snapshots
at the site, one when facing each cylinder
(Graham et al., 2004
). We
suggest that ants may equip themselves with multiple goal-related snapshots
recorded at one site, which together provide a more or less omni-directional
snapshot.
When ants gradually abandon one feeding site in favour of another, they often aim first towards the old feeding site (F1), or at some point between the two sites, and then turn abruptly to head towards the new site (F2). On their return from F2, they often head directly to the start. Three major changes occur as the ants gain experience of F2. The first segment of the route rotates away from F1, a finding that we will discuss in more detail elsewhere. Second, the initial vector becomes shorter so that the turn is closer to the start. Third, the segment of the route after the turn, which we have termed the second segment, is aimed more accurately at F2. The ant's ability to aim first at F1 and then at F2 within a single route (e.g. Fig. 3A) stresses that separate snapshots of the same scene taken from slightly different positions in space can act independently without mutual interference (although the rotating first segment suggests that sometimes the two snapshots are co-activated and that the ants are guided by a mixture of the two).
We wish to explain how, first, one snapshot and then another manages to capture full control of the ant's trajectory at different stages of the route. One class of model is that both the F1 and F2 snapshots are recalled at the start of each route and that, during training, the relative strengths of the two recalled memories gradually change in favour of the F2 snapshot. This model could be called static because for any single trip the attractor landscape set up by the two more or less omni-directional goal snapshots is fixed at the start. On early trials, the ant is first drawn by the F1 snapshot towards F1. At F1, the attractive force of the F1 snapshot is minimal and the ant is drawn to F2. When, with increased training, the unrewarded F1 snapshot becomes weaker and the rewarded F2 snapshot becomes stronger, the ant becomes attracted to F2 earlier in the route. One problem with this static model is to explain why, particularly in the early stages of training to F2, when the ant goes from F1 to F2, the ant is not then trapped by F1. Thus, on reaching F1, the ant may start moving towards F2, but its omni-directional F1 snapshot would act to draw the ant back to F1. A possible solution to this difficulty is to suppose that, despite the ant's ability to reach both F1 and F2 from different directions, their omni-directional goal snapshots retain a strong directional bias along the ant's normal route. For instance, snapshots taken at F2 when arriving on a direct path from F1 could be relatively stronger than those taken from other directions.
A second possibility is that ants recall snapshots sequentially. At the
start, they recall the F1 snapshot (or, when the first segment rotates away
from F1, a weighted combination of the F1 and F2 snapshots). At the turn, they
recall the F2 snapshot and de-activate the F1 snapshot. The migration of the
turn towards the start would then suggest that F2 is recalled earlier as
training progresses. Initially, recall of the F2 snapshot may be triggered by
the view from F1, but, with increased training, it may be activated from a
wider range of locations. The essential feature of this model is that ants are
guided by snapshots that are recalled at different stages along the route,
with recall driven either by what the ant sees or by more internally derived
signals. The attractor landscape set up by snapshots may then evolve during a
single trajectory. This model accounts naturally for the `trap-lining' that
has been reported in orchid bees (Janzen,
1971) and bumblebees
(Heinrich, 1979
;
Thomson et al., 1997
) as they
follow a fixed route from one flowering plant to another. So far, our data do
not allow us to decide definitively between the two models. But a rotating
initial vector that is followed by an abrupt turn towards F2 does perhaps
argue in favour of a dynamic model in which snapshot memories are switched on
and off during the course of a route.
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Acknowledgments |
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Footnotes |
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