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The Journal of Neuroscience, January 1, 1999, 19(1):311-315
Homing in Pigeons: The Role of the Hippocampal Formation in the
Representation of Landmarks Used for Navigation
Anna
Gagliardo1,
Paolo
Ioalé1, and
Verner P.
Bingman2
1 Dipartimento di Etologia, Ecologia ed Evoluzione,
Universitá di Pisa, I-56126 Pisa, Italy, and
2 Department of Psychology, Bowling Green State University,
Bowling Green, Ohio 43403
 |
ABSTRACT |
When given repeated training from a location, homing pigeons
acquire the ability to use familiar landmarks to navigate home. Both
control and hippocampal-lesioned pigeons succeed in learning to use
familiar landmarks for homing. However, the landmark representations that guide navigation are strikingly different. Control and
hippocampal-lesioned pigeons were initially given repeated training
flights from two locations. On subsequent test days from the two
training locations, all pigeons were rendered anosmic to eliminate use
of their navigational map and were phase- or clock-shifted to examine
the extent to which their learned landmark representations were
dependent on the use of the sun as a compass. We show that control
pigeons acquire a landmark representation that allows them to directly use landmarks without reference to the sun to guide their flight home,
called "pilotage". Hippocampal-lesioned birds only learn to use
familiar landmarks at the training location to recall the compass
direction home, based on the sun, flown during training, called
"site-specific compass orientation." The results demonstrate that
for navigation of 20 km or more in a natural field setting, the
hippocampal formation is necessary if homing pigeons are to learn a
spatial representation based on numerous independent landmark elements
that can be used to directly guide their return home.
Key words:
cognitive map; hippocampus; homing; navigation; pigeons; spatial memory
| |
INTRODUCTION |
The critical role of the amniote
hippocampal formation (HF) in spatial cognition when map-like (O'Keefe
and Nadel, 1978 ) or relational (Eichenbaum et al., 1994) landmark
representations are used for navigation is a well described phenomenon.
There is a considerable amount of data from rats (Morris et al., 1982; Eichenbaum et al., 1990) and birds (Sherry and Vaccarino, 1989; Strasser and Bingman 1997) demonstrating that hippocampal lesions impair or alter navigation by landmarks under laboratory conditions. The slower homing times of HF-lesioned homing pigeons (Columba livia) has also been used to suggest that the avian HF is critical for landmark navigation under natural conditions and distances of tens
of kilometers (Bingman et al., 1988a, 1995; Bingman and Mench,
1990).
When homing pigeons are released from an unfamiliar location, they are
limited to using their navigational map, together with some compass
mechanism to navigate home (Kramer, 1959). However, when pigeons are
released in a familiar area, they can also rely on a learned
representation of familiar landmarks to navigate (Hartwick et al.,
1977). (Familiar landmarks need not be exclusively visual but may
include stimuli from any sensory channel.) HF-lesioned pigeons also
succeed in learning to use familiar landmarks to navigate home (Bingman
et al., 1988b).
Familiar landmark navigation is complicated by the independent ability
of pigeons to use the sun as a compass ("sun compass") (Schmidt-Koenig, 1961). In fact, homing pigeons can use familiar landmarks for navigation relying on two distinct mechanisms. First, a
pigeon can navigate by directly referring to the landmarks experienced during training without referring to any compass mechanism, which we
will call "pilotage" (Bingman and Ioalé, 1989).
Alternatively, a pigeon can use the landmarks at a familiar location
only to recall the compass (sun) direction home flown from that
location, which we will call "site-specific compass orientation"
(Luschi and Dall'Antonia, 1993). These two strategies are strikingly
different in the amount of information that would be extracted from the landmarks. For pilotage, familiar landmarks are used to form a spatial
representation that directly guides navigation and is likely based on
pigeons learning the spatial relationship among numerous independent
landmark elements, including the home loft. For site-specific compass
orientation, local landmarks in the immediate vicinity of a training
location are used only to recall a compass direction, and it is the sun
compass that actually directs the flight home.
Both intact and HF-lesioned pigeons succeed in learning to use familiar
landmarks for navigation. However, in the present paper, we show that
the landmark representations that guide their navigation are strikingly
different. Control pigeons learn a spatial representation that allows
them to directly use landmarks to guide their flight home: pilotage.
Hippocampal-lesioned birds, in contrast, learn to use familiar
landmarks only to recall the compass direction home: site-specific
compass orientation.
| |
MATERIALS AND METHODS |
Subjects. All pigeons were housed near Pisa, Italy.
Two independent series of pigeons were used. In series 1, 28 (16 controls and 12 HF-lesioned) pigeons with previous homing experience
limited to free flights around the loft were used. Surgery (see below) took place ~6 months before experimental training. In series 2, 44 (27 controls and 17 HF-lesioned) pigeons with previous homing experience limited to free flights around the loft were used. Surgery
took place ~1 month before experimental training.
Surgery. Aspiration procedures were used to lesion the HF,
consisting of a medial hippocampus and dorsomedial parahippocampus (Karten and Hodos, 1967), of the lesioned birds. The methods have been
described in detail elsewhere (Bingman et al., 1984). With aspiration
lesions, there is always the risk that any behavioral effects could be
caused by damage of fibers of passage. However, in birds, the
only fibers that pass through HF that do not originate or terminate
there is a projection from the hyperstriatum accessorium to the
midbrain (Reiner and Karten, 1983). Aspiration lesions to the
hyperstriatum accessorium have been repeatedly used as control lesions
(Bingman et al., 1984, 1988a), and no effect on homing behavior has
ever been observed after damage to this area. Therefore, it is unlikely
that any observed effects could be caused by damage to fibers of passage.
Training from familiar locations. Before the experimental
releases, the pigeons from both series were given eight training releases under sunny conditions from each of two locations: Livorno, 13.6 km southeast of home; and La Costanza, 16.7 km north of home. The
site of a training release switched randomly between Livorno and La
Costanza with the constraint that the same training location was not
used for 3 consecutive days. During the first seven training releases,
the pigeons were released together as a flock. During the last training
release, the pigeons were released individually, and vanishing bearings
were recorded.
Experimental releases: series 1. After training, the pigeons
were subjected to two experimental releases, one from each training location. The two landmark-based navigational mechanisms described above differ primarily in what guides the orientation of a pigeon; for
pilotage, a pigeon would refer to the landmarks themselves, whereas for
site-specific compass orientation, a pigeon, on sunny days, would
orient by its sun compass. Therefore, to determine which of these
mechanisms a pigeon was using, all pigeons before each experimental
release were phase- or clock-shifted 6 hr fast for at least 7 d.
Phase-shifting birds 6 hr fast leads to a counter-clockwise shift in
orientation compared with nonshifted birds when the sun compass is used
for orientation. Because the present study was performed in late spring
and summer, a 6 hr fast shift would cause a shift in orientation of
~120° if the sun compass was being used exclusively for
orientation. The orientation of pigeons relying exclusively on a
pilotage mechanism should not be affected by a phase-shift manipulation.
To examine landmark navigation, it was also necessary to eliminate the
possibility that the experimental pigeons could rely on their
navigational map to determine their location relative to home (Kramer,
1959). It has been overwhelming demonstrated that for pigeons in Italy
atmospheric odors are the crucial environmental stimuli used in the
operation of the navigational map (Papi, 1990). Therefore, to eliminate
the possibility that the pigeons would use their navigational map for
homing, all the birds were rendered anosmic by intranasal injection of
4% zinc sulfate (2 ml in each nostril) 24 hr before each release
(Benvenuti et al., 1992). In summary, for the experimental releases,
the anosmic HF-lesioned and control pigeons were unable to use their
navigational map to home and were therefore limited to relying on the
landmark representation acquired during training. Further, the same
pigeons were phase-shifted 6 hr fast, which permits dissociation of a pilotage landmark mechanism from a site-specific compass orientation mechanism based on the sun.
Series 1 birds were first released from La Costanza. Returning birds
were phase-shifted again for 7 d and then released from Livorno.
Birds were released singly and followed with 10 × 40 binoculars
until they disappeared from view. The vanishing bearing and vanishing
time of a bird were recorded, and then the next bird was released,
alternating treatment groups. An observer at the loft recorded the
arrival of the pigeons so that homing times could be calculated.
Circular statistics were used to examine the distribution of vanishing
bearings for each group for each experimental release (Batschelet,
1981). The Rayleigh test was used to determine whether the vanishing
bearings of a group deviated from uniform. The Watson-Williams
U2 test was used for between-group
differences in vanishing bearings, and the Mann-Whitney U
test was used for differences in homing times.
Experimental releases: series 2. Identical to series 1, the
series 2 pigeons consisted of a group of control (n = 14) and a group of HF-lesioned (n = 17) birds that were
both phase-shifted and rendered anosmic before the experimental
releases (see above). Two HF-lesioned birds only participated in the
second release from Livorno. In addition, a second group of controls
(n = 13), not rendered anosmic and therefore able to
use their navigational map based on atmospheric odors, was included to
determine whether the behavioral differences observed in series 1 was a
consequence of the two groups responding differently to the phase-shift
manipulation (see below).
Histology. After completion of the experimental releases, 10 remaining HF-lesioned pigeons from series 1 and series 2 were killed for histology and lesion reconstruction using procedures described elsewhere (Bingman et al., 1984). Because many HF-lesioned birds were lost, there is a danger that the remaining birds do not
adequately represent the lesion damage experienced by the group as a
whole. However, the behavior (orientation) of the remaining pigeons was
indistinguishable from the birds lost. Also, we have conducted numerous
experiments with HF-lesioned pigeons (Bingman et al., 1995), and the
surgical procedures have been standardized such that there is very
little variability in the extent of lesion damage among birds. The
avian HF is visible while aspirating, thus permitting excellent control
during lesion surgery. Consequently, we are confident that the sampled
pigeons offer a reasonable approximation of the lesion damage sustained
by the HF-lesioned birds as a whole.
| |
RESULTS |
Histology
Summarized in Figure 1 is the lesion
damage observed in the sampled pigeons. All birds sustained
considerable bilateral damage to the hippocampus, and most sustained
considerable bilateral damage to the parahippocampus. Occasional damage
to neighboring hyperstriatum accessorium, hyperstriatum ventrale, and
neostriatum was also observed. On average, pigeons sustained 77%
(SE = 2.0) bilateral damage to the hippocampus and 69% (SE = 2.9) damage to the parahippocampus. No one bird sustained >10%, and
no more than four birds sustained >5% bilateral damage to any other
structure. In general, the lesion damage resembles closely that
observed in other aspiration lesion studies (Bingman et al.,
1988a,b).
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Figure 1.
Lesion reconstruction summary of the 10 sampled
pigeons. Dark areas indicate lesion damage found in at
least 8 of the 10 pigeons. Striped areas indicate lesion
damage in at least 3 of the 10 pigeons. APH,
Parahippocampus; CDL, area corticoidea dorsolateralis;
E, ectostriatum; HA, hyperstriatum
accessorium; HD, hyperstriatum dorsale;
Hp, hippocampus; HV, hyperstriatum
ventrale; Imc, nucleus isthmi, pars magnocellularis;
Ipc, nucleus isthmi, pars parvocellularis;
LH, lamina hyperstriatica; N,
neostriatum; PA, paleostriatum augmentatum;
SGC, stratum griseum centrale; Tpc,
nucleus tegmenti peduncolo-pontinus, pars compacta; V,
ventriculus. Adapted from the atlas of Karten and Hodos (1967).
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Behavior
Summarized in Figure 2 and Table
1 are the data and statistical analyses
from the experimental releases from the two series. It should be noted
that on the last training release from both sites, the control and
HF-lesioned birds were impressively and indistinguishably well oriented
toward home (Table 1). Examining the initial orientation recorded
during the experimental releases, the phase-shifted, anosmic control,
and HF-lesioned birds were strikingly different. The vanishing bearings
of the control birds, although shifted slightly counter-clockwise in
the expected phase-shift direction, were nonetheless close to the
homeward direction. This result demonstrates that their orientation was
primarily guided by familiar landmarks and not the sun compass. In
contrast, the vanishing bearings of the HF-lesioned birds showed the
typical large counter-clockwise displacement from the home direction
characteristic of fast phase-shift treatments, demonstrating primary
use of the sun compass for orientation. The control birds also
displayed consistently faster median homing times.
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Figure 2.
Vanishing bearings of anosmic controls
(filled circles), anosmic hippocampal-lesioned
birds (striped triangles), and control birds able to
smell (open circles) recorded during the experimental
releases from the familiar training locations. All pigeons were
phase-shifted. Each data point on the periphery of a
circle represents the vanishing bearing of one bird.
Arrows in each circle represent the
direction of the mean vector for each group. The length of the
arrow approximates the mean vector length for a group,
with the radius of the circle equal to 1.0.
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The data from the phase-shifted anosmic pigeons is entirely consistent
with the hypothesis that although HF-lesioned birds can learn to use
familiar landmarks to orient home (Bingman et al., 1988b), the
structure of their landmark representation is very different from that
learned by controls. However, previous research has shown that when
control and HF-lesioned birds are phase-shifted and then released from
a distant unfamiliar location (no familiar landmarks available) with
their ability to smell intact, control birds often show a smaller shift
in orientation compared with HF-lesioned birds (Bingman et al., 1996).
The difference in orientation under these conditions is generally only
~30°, considerably smaller than the 100° or larger differences
observed in the present study. Nonetheless, it was important to
determine whether the observed differences in orientation were indeed
attributable to differences in the learned landmark representations
rather than a general difference in how intact and HF-lesioned birds respond to phase-shifting.
Birds that can use both familiar landmarks and a navigational map to
determine their location relative to home rely primarily on their
navigational map, together with sun compass for navigation (Füller et al., 1983; Bingman et al., 1989). Therefore, the
series 2 control birds that were able to smell (navigational map
intact) were expected to show a qualitatively larger counter-clockwise shift in orientation compared with anosmic controls. Indeed, an examination of Figure 2 and Table 1 (series 2 only) reveals that the shift in vanishing bearings away from the homeward direction was
larger for the controls that were able to smell compared with the
anosmic controls, although a significant difference was only found from
Livorno. It is also worth noting that no statistical differences were
found in the vanishing bearings of the anosmic HF-lesioned birds and
controls able to smell. Therefore, the large difference in vanishing
bearings between the anosmic controls and anosmic HF-lesioned birds was
not a simple consequence of the groups responding differently to a
phase-shift manipulation.
| |
DISCUSSION |
It has been shown previously that both control and HF-lesioned
birds can rely on familiar landmarks from a training site to navigate
home when their navigational map based on atmospheric odors is rendered
dysfunctional (Bingman et al., 1988b). The present results, however,
demonstrate that the structure of the landmark representation used to
guide navigation is fundamentally different between the two groups. The
control birds were generally insensitive to the phase-shift
manipulation, displaying homeward orientation comparable to the last
training releases. This behavior is consistent with the learning of a
landmark representation that can directly guide the in-flight
orientation of a pigeon (pilotage) without reference to an independent
sun compass mechanism (Bingman and Ioalé, 1989). Their modest
shift in orientation in the expected phase-shift direction, however,
suggests that in addition to landmark-based pilotage, controls also
learned a site-specific compass orientation response that influenced
their behavior.
The behavior of the HF-lesioned birds could not be more strikingly
different. They were as well oriented as controls (similar mean vector
lengths) but showed a dramatic counter-clockwise shift in orientation,
demonstrating that they were relying exclusively on their sun compass
to guide their in-flight orientation. In contrast to controls, they
used familiar landmarks only to recall a site-specific compass
orientation response based on the sun compass (Luschi and
Dall'Antonia, 1993).
In our opinion, the data presented provide the first unambiguous
evidence demonstrating the critical role of the amniote hippocampal formation in landmark navigational learning in a natural field setting.
It is important to note that the landmark representation acquired by
the control birds was not a simple chaining of responses acquired
during training, i.e., fly to the barn, then the water tower, then the
power lines, etc. The vanishing bearings of the control birds were
shifted slightly compared with the last training releases, indicating
that they were not simply following the same path taken during training
and needed to make route adjustments during the flight home. Also,
pigeons are known to successfully rely on familiar landmarks for
navigation, even when they are released several kilometers from a
training release site (Bingman et al., 1989). Although speculative, the
characteristics of the landmark representation acquired by the control
birds suggests that the learned representation captured the spatial
relationship among numerous landmarks found between the release site
and the home loft: a kind of relational representation (Eichenbaum et al., 1994) with map-like properties (O'Keefe and Nadel, 1978).
It is clear that the pigeons with HF lesions failed to acquire a
similarly rich landmark representation. The birds did learn, and what
they learned would have gotten them home quickly if they were not
phase-shifted (Bingman et al., 1988b). However, the acquired landmark
representation of the HF-lesioned birds served only to recall an
associated sun compass direction. The deficiency of such an
impoverished spatial representation is highlighted by the considerably
longer homing times and the large number of HF-lesioned birds that
never returned home (Table 1). It is clear that the landmark
representation acquired by the HF-lesioned birds did not allow them to
readily correct for the errors in initial orientation created by the
phase-shift manipulation. In summary, they did not acquire a landmark
representation that would have permitted pilotage.
One curious finding is the slight difference in the behavior of the
control birds from Livorno and La Costanza. The data suggest that the
control birds were more likely to exclusively use a pilotage strategy
from Livorno than from La Costanza. If real, what might be the origin
of this difference? One possibility is that different locations will
vary in the richness and complexity of landmarks, and this may
influence the extent to which pilotage or site-specific compass
orientation will be used. The Livorno training site was near a large
urban center with heavy industrial landmarks visible for a considerable
distance. The La Costanza training site was in a more uniform
agricultural area. The difference in the type of landmarks at the two
locations may explain why pilotage was more apparent from Livorno.
Finally, it has been reported previously that when tested in an
experimental arena HF-lesioned homing pigeons are unable to use their
sun compass to locate a food goal (Bingman and Jones, 1994). The
success of the HF-lesioned birds in the present study to learn a sun
compass-based site-specific orientation response from a familiar
training location was therefore unexpected. In the arena study, the
HF-lesioned pigeons were limited to using their sun compass to learn
the direction of a goal while being held within an enclosed space. In
contrast, during training flights in the present study, HF-lesioned
pigeons were able to fly, use their navigational map, experience
landmarks, and orient by their sun compass. One can therefore reconcile
the apparently contradictory results of the present study and the
previous arena study by recognizing that the arena study took place in
a restricted stimulus-poor environment, whereas in the present study,
learning took place in a stimulus-rich natural setting that allowed the
expression of a broad range of behaviors. The results of the present
study highlight the unique importance of performing experiments under natural conditions in attempting to unravel the complex relationship among brain, behavior, and cognition. It would have been impossible to
reveal the fundamental difference in the landmark representations of
control and HF-lesioned birds in a laboratory setting. The relationship
between hippocampus and spatial cognition evolved under natural
conditions, and experiments performed under natural or semi-natural
conditions are a critical source of new perspectives needed for a more
thorough and perhaps more challenging understanding of the role of HF
in cognition.
| |
FOOTNOTES |
Received July 16, 1998; revised Sept. 11, 1998; accepted Sept. 23, 1998.
This work was supported by a NATO collaborative research grant (V.P.B.)
and grants from the National Institutes of Mental Health (V.P.B.) and
Consiglio Nazionale delle Ricerche (P.I.). We thank Meliha Duncan for
her help in preparing this manuscript.
Correspondence should be addressed to Verner P. Bingman, Department of
Psychology, Bowling Green State University, Bowling Green, OH 43403.
| |
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A. Kamil and K Cheng
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H. Wallraff, J Chappell, and T Guilford
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Top
Abstract
Introduction
