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First published online August 22, 2008
Journal of Experimental Biology 211, 2817-2826 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019927
Exploration and navigation in the blind mole rat (Spalax ehrenbergi): global calibration as a primer of spatial representation
Department of Zoology, Tel-Aviv University, Ramat-Aviv 69978, Israel
* Author for correspondence (e-mail: eilam{at}post.tau.ac.il)
Accepted 30 June 2008
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Summary |
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Key words: open field, cognitive map, subterranean rodent, locale system
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Forming a cognitive map is generally ascribed to the process of exploration:
`The hippocampal locale system is assumed to form the substrate for maps of
environments an animal has experienced; these maps are established in the
hippocampus during exploration, a species-specific behaviour pattern concerned
with the gathering of information...'
(O'Keefe and Nadel, 1978). It
has been further suggested that exploration is necessary in order to form a
metric representation of the available working space or to identify the
relationships between the animal's movement and external cues
(Whishaw and Brooks, 1999).
Gallistel (Gallistel, 1990)
suggested that the cognitive map is formed by combining an egocentric
geometric representation with a geocentric measurement by means of path
integration of the available space. Jacobs and Schenk
(Jacobs and Schenk, 2003),
however, suggested that two phylogentically, and neurally-remote mechanisms,
positional (`bearing') and directional (`sketch') maps, are integrated in
forming the cognitive map. It was also suggested that map construction during
exploration involves a shift from sequential information processing, which is
based on piloting from one landmark to the next
(Zadicario et al., 2005), to
orienting, in which piloting also involves a calculation of compass direction
to one specific location and, ultimately, a shift to map navigation
(Avni et al., 2006). Even so,
the actual existence or nature of a cognitive map has not as yet been
established, with some claiming that a cognitive map either does not exist or
that its existence cannot be proven and it is thus irrelevant (e.g.
Bennett, 1996). Moreover, it
has not yet been empirically demonstrated how this spatial representation is
produced through exploration.
In the present study, we assumed that possession of any sort of global
spatial representation can be considered as having a cognitive map, as in the
general definition of a `cognitive map' used by Gallistel
(Gallistel, 1990), and unlike
the stricter definition coined by O'Keefe and Nadel
(O'Keefe and Nadel, 1978). We
posed the question of what is the very basic or primordial form of an initial
global representation. An initial (`draft') map could be formed, for example,
by first acquiring representation of the geometry of the environment and,
later on, adding featural cues to this draft
(Cheng, 1986;
Gallistel, 1990). Another
basic form could be that of a representation of the environment by its
principle or symmetry axes (Cheng and
Gallistel, 2005; Gallistel,
1990) (for a review, see Cheng,
2005). In any case, each of these primitive forms of global
environmental representation is acquired and constructed via
exploration of the environment. Accordingly, in the present study we
introduced our model animal, the blind mole rat (Spalax ehrenbergi),
into an unfamiliar environment and tracked its behaviour in order to uncover
the construction of spatial representation.
The blind mole rat is a subterranean rodent that digs a borrow system in
which it stays most of its life (Rado et
al., 1992). As indicated by its name, the blind mole rat is a
completely blind species (Cooper et al.,
1993); nevertheless, its circadian clock is influence by external
light (Oster et al., 2002).
Although mole rats' eyes had undergone degeneration during the course of their
evolution, the mole rats have evolved effective compensatory means to
efficiently navigate and find their way. Indeed, mole rats were found to have
strong tactile (Kimchi and Terkel,
2004; Klauer et al.,
1997) and magnetic sensory abilities
(Kimchi et al., 2004;
Kimchi and Terkel, 2001a), and
produce and utilize seismic vibrations
(Kimchi et al., 2005;
Nevo et al., 1991), all of
which could facilitate the mapping of an unfamiliar environment. Most
importantly, the mole rat seems to have developed a spatial representation
capacity that is comparable with that of sighted rodents, and in some cases
may even exceed them; e.g. mole rats were more efficient in learning and
solving a labyrinth than rats and voles
(Kimchi and Terkel, 2001b). A
mole rat in the wild spends most of its life in a closed tunnel system that
may span over 40 m in length. It repeatedly patrols and monitors this
territory for changes. For example, when the tunnel is breached to the
outside, the mole rat quickly identifies the location and runs there to seal
it (Rado et al., 1992;
Zuri and Terkel, 1996).
Evidence that mole rats possess a sort of `mental' or imaginary map of their
tunnel system comes from their striking ability to dig bypasses to reconnect a
tunnel bisected by an obstacle. Moreover, they are able to identify and
exploit the shortest available detour of the obstacle when provided with short
and long detour choices (Kimchi and
Terkel, 2003). Such efficiency in bypassing an obstacle to
reconnect to the tunnel system would be impossible without some sort of global
representation of the environment. In light of these abilities, we examined
the mole rats' behaviour in the present study when exploring an unfamiliar
walled arena. Specifically, we posed the question of whether a mapping process
could be identified in the structure of exploration of the mole rat and
whether some evidence of the animal's use of such representation might be
revealed.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Excavating their burrow system using their sharp
incisors, the mole rats' activity is entirely subterranean, and they can be
found above ground only when forced to be there in the brief period of
dispersal of the young, or when driven out of their burrow by another mole rat
(Rado et al., 1992;
Zuri and Terkel, 1996). Along
with their vestigial eyes and lack of external ears, mole rats have an
elongated trunk, relatively short legs and no tail, thereby being well adapted
to travel both forward and backward in their borrows
(Eilam and Shefer, 1992); they
are also well adapted to the low O2 and high CO2 levels
found in underground tunnels (Mendelssohn
and Yom-Tov, 1999; Nevo,
1999). Our study animals were housed individually in small cages
(35cmx25cmx20cm) under a 14h:10h L:D photoperiod. Food (carrots,
apples and standard rodent chow) was provided ad libitum.
Apparatus
Testing was carried out in a square open field (2 mx2 m) enclosed
with a 0.5 m-high opaque Plexiglas walls and a blue PVC floor, placed in an
air-conditioned room (22°C). During testing, the room was illuminated by
three 300 W light bulbs directed to the white ceiling, providing diffused
illumination of the arena. A video camera (Ikegami B/W ICD-47E, Tokyo, Japan)
was placed 2.5 m above the centre of the arena, providing a top view that was
recorded onto a computer by means of a video grabber (VideoHome GrabBeeX) as a
MPEG1 digital file.
Procedure
At the beginning of each test session, an individual mole rat was placed at
the bottom right corner of the open field, facing the corner and in contact
with the arena wall. The experimenter quietly left the room and the behaviour
of the mole rat was then video-recorded for 30 min, after which the animal was
returned to its cage. The arena was sprayed with detergent, wiped with a cloth
and dried before the next animal was introduced. Testing took place between
08:00–14:00 h, which is within the activity hours of mole rats in the
wild (Zuri and Terkel,
1996).
Data acquisition and analysis
The video files were analyzed using `Ethovision' (Noldus
Information Technologies, Wageningen, NL), which tracks the progression in the
arena, providing the time and location of the study animal five times per
second. For analysis, the arena was divided into a perimeter zone, which was
defined as a 0.15 m strip along the arena walls, and a centre zone, which was
a 1.7 mx1.7 m square, in order to differentiate between travelling at
the perimeter and through the centre. Additionally, corner zones were defined
as a 0.15 mx0.15 m square at each arena corner. Another division of the
arena into 36 identical 0.33 mx0.33 m sectors was applied in order to
depict the time that mole rats spent at various locations in the arena. The
mole rats greatly varied in behaviour over the course of the 30 min of
observation. Some individuals rapidly expanded their exploration whereas
others were slower to encompass the entire arena space; some quickly entered
the centre, others never did so within the observation period. To overcome
this variability, behaviour was compared in terms of the temporal order of
occurrence rather than in strict time frames. The temporal unit for comparison
was a lap; a path that encompassed the entire perimeter, starting and ending
at the corner in which the mole rat had been placed at the beginning of the
observation. From `Ethovision' we extracted the total distance that the mole
rats travelled in the course of observation, the time spent and the number of
visits (entries) to each of the 36 arena zones, the average travel speed, and
the speed when entering a corner zone. We further extracted or scored manually
from the video files the following parameters: (1) total number of laps; (2)
lap length – the distance (in metres) that a mole rat travelled
in a lap; (3) lap duration – the time elapsed (in seconds) from
departure until return to the start location of the lap; (4) number of stops
in a lap – a stop was defined as the absence of forward progression for
at least 1 s; (5) interstop distance – the distance (in metres) between
each two consecutive stops; (6) retreating – incidence of backward
walking that occurred when a mole rat stopped along a wall and then rapidly
moved backwards as if retreating along the path it had just travelled; (7)
retracing – the incidence of reversal of direction of progress
that occurred when a mole rat performed a U-turn to progress in the opposite
direction, thus retracing part of the path it had just travelled; (8) facing
the centre – incidence of a behaviour that occurred when a mole rat
stopped along the arena walls with its trunk in contact with the wall and
turned its head about 45° to face the arena centre; (9) corner shortcuts
– when a mole rat progressed along a wall toward a corner but instead of
reaching the corner it diverted in an arc toward the near half of the
perpendicular wall (see Fig.
5B); (10) crosscuts through the centre – when a mole rat
left the perimeter zone and returned to it by either travelling to the
opposite wall or to a distant half of a perpendicular wall (see
Fig. 5B); (11) behaviour at the
end of crosscuts – for each crosscut, behaviour when approaching the
wall was classified as: (i) bumping into the wall; (ii) approaching the wall
in the same direction as the preceding part of the crosscut; (iii)
intermittent travel (switching between progressing and pausing), which may
also include head turns; (iv) slowing down; or (v) curving the path to
parallel the wall. See Movie 1 in the supplementary material for
representative examples of these behaviours.
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RESULTS |
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). Only
for one mole rat was this the start corner, i.e. the position at which the
mole rats were introduced into the arena at the beginning of the observation;
whereas eight mole rats spent the extended cumulative time at the top right
corner of the arena (Fig. 1A,
inset). In contrast to the time spent at the various zones, there was no one
zone that the mole rats visited significantly more than any other zone
(Fig. 1B). Furthermore, for
only one mole rat was there a match between the zone where the greatest
cumulative amount of time was spent and the most visited zone.
Build-up of paths along the arena walls (laps)
When a mole rat was introduced into the arena at the beginning of the
observation, it initially performed a phase of building-up a path that
gradually covered the entire arena perimeter, whereas entering the centre of
the arena typically occurred only at a later phase of the observation. The
gradual build-up of the perimeter path is shown for one mole rat in
Fig. 2. As shown, the path was
first extended from the starting corner to an adjacent corner. By gradually
retracing and/or retreating along past paths and progressing to new sectors
along the perimeter, the path was then extended from one corner to the next,
until it had covered the entire perimeter. We defined such a roundtrip that
encompassed the entire perimeter as a lap, and subsequently used laps as the
structural units in the temporal organization of exploration in mole rats.
Accordingly, the following results are shown first for the build-up of
activity along the arena perimeter during successive laps and then for
crossing the centre. The mole rats greatly varied in their activity, as
reflected in the overall distance they travelled and in the number of laps. As
shown in Table 1, males were
more active, traversed greater distances and performed more laps compared with
females. Therefore, the data below are given separately for females and
males.
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Behavioural changes across successive laps
An observer could easily notice that the first lap substantially differed
from subsequent laps in that it took a long time to complete it. The first lap
also comprised slow progression, numerous backtrackings, frequent stops, and
many head turnings to face the centre. Backtrackings took the form of either
retreating (a fast backward withdrawal along the arena wall), or retracing (a
180° U-turn followed by forward locomotion along the arena wall; see Movie
1 in supplementary material). In order to highlight the difference between the
first lap and subsequent laps, we compared the first four laps performed by
each mole rat (Table 2A). We
limited the comparison to only the first four laps since this was the minimal
number of laps undertaken by all mole rats
(Table 1). The results of a
two-way ANOVA are summarized as gender effect (between females and males) and
over the first four consecutive laps (within-group effect). Except for the
distance travelled, there was a significant change over the first four laps in
all parameters, as detailed in Table
2A. A Tukey HSD test revealed a significant difference only
between the first lap and the three following laps
(Table 2A). The difference
between the first lap and the following laps is demonstrated in the change in
travelling speed between laps (Fig.
3A). Moreover, even for the distance travelled in a lap there was
a considerable, albeit non-significant, decline over successive laps
(Fig. 3B). Despite the
significant differences between males and females for all parameters shown in
Table 2A, none of the
interactions (laps x gender) were significant, implying that the same
trend of change across laps occurred in both females and males.
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Of the eight parameters shown in Table 2A, five decreased across the four first laps, reflecting that the mole rats first travelled slowly, so that lap duration was long, and also retreated frequently by backward walk or made frequent U-turns to retrace their former path. They also made frequent stops so that interstop distance was short in the first lap. In some of the stops during the first lap, the animals' trunk was aligned in contact with the arena wall while their head was turned laterally to face the arena centre. These behaviours declined over subsequent laps, in which the mole rats travelled faster, stopped less frequently and at greater inter-stop distances, and rarely retreated or retraced their paths (Fig. 4A).
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`Global' crosscuts through the arena centre
After the build-up of trajectories that encompassed the entire perimeter,
another notable change occurred, when the mole rats started to take crosscuts
through the centre of the arena. Individual mole rats greatly varied in their
tendency to enter the centre, with five of the males and two females doing so
frequently whereas the remainder never crossed the centre
(Table 1). Of those animals
that did cross the centre, six did so from the second lap onward, and one took
a crosscut during the first lap (Table
1). This latter exceptional mole rat differed from the others in
abandoning the arena walls at the beginning of the experiment. In all, as
illustrated in Fig. 4A,
crosscuts through the centre occurred at a relatively late stage, typically
after the completion of two laps. Once a crosscut had occurred, it was then
performed, by most mole rats, at least every other lap
(Table 1).
As seen in Fig. 4A, crosscuts did not converge to a specific corner (compare with Fig. 4B showing crosscuts through the centre in home base behaviour of other rodents). Moreover, arena crosscuts did not involve a departure or return to a specific zone. To highlight this aspect, we calculated an average number of crosscuts per zone for departure zones and for return zones. This was performed, for example for departures, by summing for each mole rat the total number of crosscuts and dividing this by the number of zones from which a crosscut had started. We found that in the 12 mole rats, the average ratio (± s.e.m.) was 1.21±0.12 crosscuts per zone for departures, with a maximum ratio of 1.8 crosscuts. A similar calculation for the zones at which crosscuts terminated, revealed an average ratio of 1.23±0.07 crosscuts per zone, with a maximum of 1.6 crosscuts. These ratios indicate that there was no specific zone at which crosscuts were repeatedly originated or terminated. Therefore, crosscuts through the arena centre did not converge or depart from one place but rather diverged over various perimeter zones.
Travelling through the centre was faster compared with the first lap [average ± s.e.m. (cm s–1): crosscuts 26.14±2.32; first lap 11.25±1.98; these were calculated only for mole rats that crossed the centre]. In crosscuts, mole rats typically moved continuously from wall to wall without stopping. Only 11% of all crosscuts included stops, with an average of 1.22±0.16 stops per crosscut (calculated for only crosscuts with stops). Interstop distance during crosscuts was higher compared with the first lap [average ± s.e.m. (m): 1.7±0.23; compared with the shorter interstop distance shown in Table 2A]. Because of these differences in behaviour, crosscuts do not seem to represent exploration of an unfamiliar environment as does the first lap.
Approaching the wall at the end of crosscuts could take a variety of forms. As shown in Table 3, in nearly half of the crosscuts, the mole rats curved their travel path to parallel the wall. Alternatively, mole rats switched to intermittent travel or slowed down toward the wall. These three forms of behaviour, which altogether characterized 70% of the crosscuts, may indicate that the mole rats adjusted their path when approaching the wall. In about 30% of the crosscuts, the animals maintained the same travelling mode from the start to the end of the crosscut, and in only one crosscut, a bump into the wall was noted (Table 3).
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As indicated above, crosscuts through the arena centre and corner shortcuts did not characterize the period of build-up (first lap) but were prevalent thereafter in those mole rats that had taken crosscuts and shortcuts. This is shown in Fig. 5B, where the number of corner shortcuts and centre crosscuts was very low in the first 5 min, when build-up occurred (as seen in the duration of the first lap in Table 2). After 5 min, the number of shortcuts and crosscuts increased and stabilized at a relatively higher rate (Fig. 5B).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Build-up of activity and patrolling the perimeter
Two phases of exploration were apparent: a build-up phase and a
free-locomotion phase. During build-up, mole rats travelled slowly along the
perimeter with frequent pauses to turn their head toward the open area, or to
retrace/retreat along previously travelled perimeter sectors, until their path
encompassed the entire perimeter. The gradual completion of the first lap took
a longer time in females, which also displayed more retracing and pausing
compared with males. This is in line with the finding that compared with
females, male mole rats are quicker to leave the start location and to enter
new areas, due to their active search for females
(Heth et al., 1987). Indeed,
Heth et al. (Heth et al.,
1987) noted that male mole rats had larger territories than
females, and that during the breeding season, it is the male that digs its way
to the female's burrow. This explanation is similar to the polygyny-range size
theory, predicting that polygynous males that actively search for mates, will
be better in navigation-related tasks compared with females
(Saucier et al., 2008). This
theory is considered strongest among those explaining sex differences in
spatial ability (Jones et al.,
2003). It is therefore possible that the quicker and less
`hesitant' completion of the first lap by males is a result of their presumed
adaptation to a larger territory and to their need to search for females.
After building-up the first lap, the `mode' of travel changed, as the mole
rats travelled faster, covering greater interstop distances and making fewer
stops, head turns, retraces and retreats (see Movie 1 in supplementary
material). This change resulted in shorter lap duration and travel distance
compared with the first lap, and an appearance of smooth and continuous travel
along the perimeter. A reminiscent change in the mode of travel was found in
mole rats and rats over successive exploration trials in a maze
(Kimchi and Terkel, 2004),
probably indicating an increased familiarity with the environment. A process
of build-up of activity was also noted in other animals. For example, in
Lorenz's description (Lorenz,
1952) of water shrews, which have relatively poor vision and rely
more on their olfactory sense: "In a territory unknown to it, the
water-shrew will never run fast... it moves, in strange surroundings, only
step by step, whiskering right and left all the time... gradually the little
laps of the course which have been `learned by heart' and which can be covered
quickly begin to increase in length as well as in number until they fuse and
the whole course can be completed in a fast, unbroken rush."
Spatial behaviour of the studied mole rats was organized as a set of laps
that did not converge to a specific area. This is unlike sighted rodent
species that, when placed in illuminated environments, organize their
locomotion in relation to a focal location or home base, where they spend the
greatest cumulative duration of time and perform specific behaviours, e.g.
rats (Eilam and Golani, 1989;
Hines and Whishaw, 2005); mice
(Clark et al., 2006;
Drai et al., 2001); spiny mice
(Eilam, 2004); voles
(Eilam et al., 2003) and jirds
(Zadicario et al., 2005); (see
also Fig. 4). When tested in
dark environments, some rodent species form a home base
(Eilam, 2004;
Gorny et al., 2002;
Hines and Whishaw, 2005;
Nemati and Whishaw, 2007)
whereas others first use looping behaviour, travelling in entwined paths that
cross to form loops in varying locations, and only then establish a home base
(Avni et al., 2006). As opposed
to mole rats, the structural unit of home base behaviour is the round trip,
which starts at the home base and typically ends in direct dashing back to it
(Eilam and Golani, 1989;
Whishaw et al., 2001). In the
present experiment, although there was one zone where the mole rats spent a
significantly greater amount of time, their visits were scattered over the
various zones and no direct high-speed travel toward one specific zone was
observed. Indeed, a lack of home base behaviour was previously described in
the mole rat (Erez, 2005). The
organization of exploration as a set of laps is reminiscent of the `perimeter
patrolling' behaviour, which was suggested as a mechanism of gathering
information before establishing trails and home base
(Avni and Eilam, 2008).
However, travelling along the walls by the mole rat may simply be due to its
subterranean lifestyle of living in tunnels in its exact body width
(Rado et al., 1992;
Zuri and Terkel, 1996), and
thereby relying on the tactile sensation recorded by the numerous tactile skin
sensory structures (Klauer et al.,
1997). Indeed, mole rats were shown to be more efficient in
navigating in a maze with alleys the width of their body compared with
navigating in a wider-alley maze (Kimchi
and Terkel, 2004). In other words, the mole rats were able to
increase the amount of information gathered during exploration when contiguous
with the walls of the arena and thereby stimulating their tactile sensors. In
addition to their different spatial organization, sighted rodents tested in
dark conditions spend considerably more time in the open areas of the
environment than when tested in light conditions
(Brillhart and Kaufman, 1991;
Eilam, 2004;
Price et al., 1984;
Zadicario et al., 2005),
whereas the mole rats in the present test spent on average 98% of the time in
the perimeter (data not shown). Mole rats also differ from sighted rodents in
their activity level. As shown in Table
4, activity of mole rats falls near the average of sighted rodent
species tested in dark. However, mole rats activity is higher when compared
with sighted nocturnal rodents tested in light, but not when compared with a
sighted diurnal rodent (the fat sand rat) tested in light. This is in
accordance with the diurnal mode of activity in mole rats
(Zuri and Terkel, 1996). In
all, the results of the present test indicate that mole rats' spatial
behaviour differs from that of sighted rodents in a way that calls attention
to a possible mechanism of acquiring global spatial representation, as
detailed below.
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Local and global shortcuts (crosscuts)
The ability to perform shortcuts is considered as an indication that the
navigator possesses some sort of representation of the environment
(Bennett, 1996;
O'Keefe and Nadel, 1978;
Tolman, 1948). See also Foo et
al. (Foo et al., 2007), who
demonstrated the use of a beacon located at a target in order to perform a
shortcut. The mole rats displayed two types of shortcuts. In repeated visits
to the corners of the arena, travel speed when entering the corner zone
increased, and the mole rats occasionally took local shortcuts across the
corner, without travelling all the way into it. This suggests that they had
some way of sensing that they were approaching the corner. They also took
global shortcuts, for example between opposite arena walls, but only after
completion of the build-up lap.
The ability to take global shortcuts has been described in a variety of
rodent species, usually through homing experiments [but see Etienne et al.
(Etienne et al., 1998)], for
example, rats, mice, gerbils and hamsters are able to take a homing shortcut
after reaching a goal (Alyan,
1996; Etienne et al.,
2000; Mittelstaedt and
Mittelstaedt, 1982; Whishaw et
al., 2001). Although shortcuts can be performed by using visual or
other external cues, when these are unavailable (e.g. in darkness), animals
employ path integration (Maaswinkel and
Whishaw, 1999; Shettleworth
and Sutton, 2005), the process of computing one's location in
relation to its starts point of travelling
(Etienne and Jeffery, 2004;
Etienne et al., 1996). Indeed,
when tested in two maze types, mole rats employed path integration in order to
shortcut back to the start location, with the direction of path integration
affected by a magnetic compass in some conditions
(Kimchi et al., 2004). As
opposed to the above mentioned experiments, in the present study there was no
target destination for shortcuts. Instead, mole rat crossed the centre to
another wall, a behaviour that we termed `crosscut'. Global crosscuts were not
directed to a specific location; rather, they were scattered over all the
perimeter zones, reaching an average of 1.23±0.07 crosscuts per zone,
with the low standard error indicating that there was no one zone in which
many crosscuts terminated. This implies that crosscut ability probably did not
depend on visual cues (as the mole rat is blind) or on beacons located at a
target terminal for shortcuts. The use of beacons for crosscuts is unlikely
since this requires a beacon in each of the zones to which crosscuts were
taken (Shettleworth and Sutton,
2005), for example, this would require 23 beacons for the mole rat
that took a total of 37 crosscuts to 23 different zones. It should be noted
that while mole rats are blind, they possess other capacities such as magnetic
field sensation (Kimchi et al.,
2004) and seismic vibration sensation
(Kimchi et al., 2005;
Rado et al., 1998) which could
be used for crosscut guidance. Nevertheless, such capacities polarize the
environment, providing directional rather than the positional information
provided by beacons (Jacobs and Schenk,
2003).
Global crosscuts involved higher travel speed and greater interstop
distance compared with the first lap, indicating that they involve only
little, if any, exploration. The fast and uninterrupted travel through the
centre also does not seem to be an `escape' of stressed animals since the mole
rats could avoid the centre by remaining at the relatively safe perimeter.
Furthermore, before reaching the wall, in most crosscuts, mole rats displayed
a change in behaviour compared with the preceding part of the crosscut,
smoothly curving their path to parallel the wall (as in corner shortcuts),
travelling intermittently up to the wall, or slowing down. Implicit in these
behaviours is that the mole rats could estimate their proximity to the wall
and adjust their path to preclude bumping (the latter occurred in only one
crosscut; see Table 3;
Fig. 4; Movie 1 in
supplementary material). Indeed, mole rats where previously shown to be able
to estimate distances. When trained to traverse a tunnel toward a food reward
located in a fixed distance from the start point of the tunnel and then probed
without food, mole rats where found to stop and make a U-turn after traversing
the distance to the location of the food reward
(Marom, 2005). We therefore
suggest that the global crosscuts from wall to wall can be interpreted as if
the mole rats possessed a representation of the size and perhaps the shape of
the environment, which allowed them to compute crosscuts during laps. In other
words, the animals might have used a global representation of the arena,
perhaps in combination with path integration and/or directional cues such as
magnetic compass or seismic vibration, in order to estimate the travelling
distance and direction, i.e. the vector needed for a crosscut to another
wall.
A primitive global map?
Thus far, we have introduced two phases of exploring an unfamiliar
environment by the blind mole rat: (a) a gradual build-up of activity; and (b)
a subsequent phase of free locomotion along the perimeter combined with
crosscuts through the centre. These structural phases raise the question of
their function or their underlying mechanisms. Here we suggest that the
build-up and free-locomotion phases reflect a gradual establishment of local
and then global spatial representation, a sort of primordial `cognitive map'.
A model on the establishment of spatial representation suggests that spatial
learning and navigation are based on three phases of information processing
(Avni et al., 2006). First is a
sequential information processing (piloting) phase, in which animals travel
from one landmark to the next. The second travel mechanism is that of parallel
information processing (orienting), in which the traveller pilots from
landmark to landmark and in parallel maintains a compass direction to a
specific location (e.g. home base location). The third phase is that of
map-based navigation, or continuous information processing (navigating), which
relies on a detailed spatial representation containing `sets of connected
places' and providing `a large choice of possible paths between any two points
in the environment' (O'Keefe and Nadel,
1978). While piloting and orienting have been demonstrated in open
field behaviour of rodents (Avni et al.,
2006), map-based navigation in the open field has not yet been
shown. Nevertheless, we suggest that mole rat behaviour after the first lap
seems to reflect a basic form of navigating: the animals appear to travel
freely and continuously along the arena walls, taking crosscuts from wall to
wall and rounding their paths at the arena corners.
Specifically, we suggest that, upon being introduced into the arena, mole
rats first establish an estimate of the size of the available space and in the
subsequent phase they navigate along and within the represented arena. In
these hierarchical phases, the build-up of the perimeter path in the first lap
seems to be a stage of spatial calibration, in which the mole rats form
some representation of the environment in terms of size, and perhaps also of
shape (geometry). Whishaw and Brooks
(Whishaw and Brooks, 1999)
suggested that animals explore their environment in order to calibrate their
`working space'. Indeed, in the build-up phase, the animals travelled slowly
with frequent stops and retreats, thus allowing thorough exploration and
scanning of the perimeter (Kramer and
McLaughlin, 2001; Loewen et
al., 2005) while gaining the opportunity to gather the information
needed for mapping. Moreover, only after the build-up phase did the mole rats
start to take global crosscuts through the centre, which may indicate that
they had acquired a basic representation of the arena
(O'Keefe and Nadel, 1978;
Tolman, 1948) that was
probably sufficient to allow an estimation of travel distance to the other
wall. Indeed, an observer could notice the change in the behaviour of the mole
rats after the build-up phase, when in addition to crosscuts they started to
progress faster, in longer bouts, and with less stops and less retreating or
retracing. Further support for the notion that mole rats take crosscuts only
after gaining a certain estimation of the area size comes from the single mole
rat that took a crosscut through the centre in the first build-up lap. This
crosscut was tangled compared with the other crosscuts taken by this or other
mole rats, indicating that it was not a planned crosscut but rather a search
path (Muller and Wehner, 1994;
Zadicario et al., 2005).
Further research using manipulation of environment size is required for a
further understanding of how the build-up phase and the suggested process of
calibration act in the process of establishing a spatial representation
(map).
In summary, we suggest that the product of the slow and gradual build-up of a perimeter path is a process of spatial calibration – a sort of primeval representation (`map') of the space available for travelling. Exploration in the subsequent phase serves to validate and extend this `draft' map. We also suggest that this process is probably limited by species-specific perceptual or calibration abilities, and that if the available space is greater than can be estimated by that species' ability, the navigator must ignore, at least initially, some of the available space and focus on exploring only a limited part of the environment. The suggested process may offer a first characterization of the mechanism of build-up that leads to primitive map navigation in the open field. Studying the build-up process may assist in further understanding the process of establishing spatial representation.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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