The extraordinary
navigational ability of animals, which enable some species to
carry out remarkably precise long-distance migrations and homing
behavior, has fascinated natural historians for as long as animal
behavior has been of interest. The observation of an arctic tern
(Sterna paradisaea) carrying out a yearly migration between
the arctic regions of the northern and southern hemisphere, a gray
whale (Eschrichtius robustus) migrating between cold water
feeding areas near Alaska and birthing sites around the Baja
peninsula, a loggerhead sea turtle (Caretta caretta)
migrating from feeding areas in the north Atlantic to egg
deposition sites on the coastal beaches in tropical and
sub-tropical North America, and a monarch butterfly (Danaus
plexippus) making a one-way flight from temperate North
America to their winter congregation site in central Mexico can
seem mystifying (Figure 1). In fact, the seemingly routine ability
of animals in general to accurately navigate space nurtures the
speculation that the evolution of spatial cognitive abilities may
have also served as pre-adaptation for other forms of cognition
and associated brain mechanisms (e.g., O’Keefe, 1996). But how do
animals navigate? The goal of this chapter is to review the
behavioral mechanisms that are exploited by animals as they
navigate large-scale, environmental space, as well present some
findings related to brain mechanisms that support this ability.
Because of their dramatic spatial behavior and extensive use as
experimental subjects, we will concentrate our review on
birds.
 |
Figure 1. Global migratory paths of four
exceptional navigators: A) gray whale (Eschrichtius
robustus); B) monarch butterfly (Danaus
plexippus); C) arctic tern (Sterna paradisaea);
D) loggerhead sea turtle (Caretta
caretta). |
The ability to
polarize space within some directional framework is essential if
animals are to maintain movement in a constant direction with
respect to the environment. Metaphorically, the challenge is
similar to a human navigator needing to use a compass to identify
directions in space and maintain a constant directional bearing
while moving. Animal navigators possess biological compasses based
on their sensitivity to the position of the sun projected on the
horizon, or azimuth, stars and the earth’s magnetic field. These
compass mechanisms, although providing only directional
information, form the basis from which richer, map-like
representations of space can emerge.
Sun compass.
For diurnal animals with
sensory access to the sky, the sun undoubtedly offers the richest
source of information to define compass directions and orient
movements in space whether it is a short-distance flight of a bee
navigating between its hive and a food source or a diurnally
migrating swallow making a journey of several thousand kms. The
discovery and properties of the sun compass in birds were
thoroughly investigated by numerous German researchers in the
1950s and ‘60s (Kramer, 1952, 1959; Hoffmann, 1954; Schmidt-Koenig
1958, 1961). Conceptually, the challenge the sun presents an
animal that wants to maintain, for example, a southerly bearing is
that the position of the sun in the sky changes during the course
of the day. To continue moving south, a bird in the northern
hemisphere would need to keep the easterly sun to its left in the
morning, fly toward the southerly sun at midday and keep the
westerly sun to its right in the evening. The changing azimuth of
the sun across the day needs to be calibrated with respect to
stable compass directions in space. Birds seem to carry out this
conceptually challenging computation effortlessly. They do so by
relying on their internal sense of time, which manifests itself in
the form of endogenous circadian rhythms. Endogenous, biological
circadian rhythms oscillate with a period of about 24 hours and
are entrained or calibrated against the light-dark cycle of the
environment. A point in time would correspond with a point in the
cycle of the circadian rhythm. As such, reading off the circadian
rhythm can be used to define time of day and therefore be used to
read off a compass bearing from the sun’s azimuth.
![]() |
Figure 2. Video illustration of a homing
pigeon experimental release that could be used to determine
the properties of the sun compass.
|
How do we know that the temporal
calibration of the sun compass recruits endogenous circadian
rhythms as the time giver? This was elegantly demonstrated in
birds (homing pigeons and starlings) by placing experimental
subjects in an environment where the light-dark cycle was shifted;
for example, the lights in the room would come on at midnight and
go off at noon basically advancing the day of the birds 6 hours
relative to the light-dark cycle of the natural environment. Birds
kept in these conditions for a week or so would experience a shift
in their circadian rhythms; a rhythm would recalibrate to the
changed light-dark cycle such that the circadian rhythm’s morning
would correspond or entrain to lights coming on, which would be
midnight with respect to the natural environment. Imagine now a
migratory bird or homing pigeon that would typically orient south
held in the shifted light-dark cycle for a week. The bird would
then be tested for its orientation, either by letting it fly (see
Figure 2 and 3) or in a cage, during the natural morning when the
sun is in the east. However, for our experimental bird the reading
of its circadian rhythm would indicate that it is noon (remember
its circadian rhythm has been shifted), and you would actually
observe the bird orient not in the desired southerly direction but
east (Figure 3)! Why? The midday sun is in the south, and
according to the bird’s internal rhythm, it is noon and it should
fly toward the sun. But the sun is really in the east during the
environmental morning; therefore movement toward the sun is
actually an easterly movement and the wrong direction. It is this
type of clock- or phase-shift experiment that has demonstrated
that birds, and other animal groups including monarch butterflies
(Mouritsen & Frost, 2002), use their internal sense of time to
calibrate the movement of the sun in the sky. This enables them to
use the sun as a stable reference to define compass directions in
space.
|
Figure 3. Effect of a phase-shift in the light dark
cycle on the sun compass orientation of homing pigeons. A.
Under natural conditions, the properties of a circadian
rhythm would peak during midday and be associated with the
sun in the south. A pigeon needing to fly south would then
orient toward the sun at midday. B. After being held for one
week in a room where the light-dark cycle has been advanced
by six hours, the peak in the circadian rhythm associated
with midday would now occur during the natural morning. When
released now during the natural morning, the pigeon’s
subjective noon, the same bird needing to fly south would
again fly toward the sun, which would be east! Because of
the change in the circadian rhythm, the peak in the
circadian rhythm previously associated with midday and the
sun in the south would now actually correspond to
environmental morning and the sun in the
east. |
To end our discussion of the sun
compass, it should be mentioned that in addition to the disc of
the sun, birds can also orient to patterns of skylight
polarization derived from the sun. They can do so because the
properties of skylight polarization change predictably with the
changing position of the sun (e.g., Able, 1982). Bird visual
sensitivity to ultraviolet light, like that of bees, may be
important in detecting skylight polarization
Star compass.
The sun is not the only
celestial body that can be exploited to define directions in
space. Although nocturnal migrant birds can and do use the
position of the setting sun to orient their nighttime migrations
(Moore, 1987), they can also rely on the stars. But it is not just
any star or cluster of stars that can be used to guide migration.
It is the stars around the axis point of the night’s sky apparent
rotation that are preferentially relied on (Emlen, 1967). In the
Northern Hemisphere, these would be circumpolar stars like those
found in the constellations of the Big Dipper and Cassiopeia.
However, this star compass has properties different from the sun
compass. For example, orientation to the stars is not time
compensated; phase shifting migrant birds does not alter their
migratory orientation to the stars as it would sun compass
orientation. It is also notable that whereas birds can be trained
to use the sun compass to orient to a food source or other goal
unrelated to migration or homing, orientation by the stars has
only been demonstrated in the context of migration.
Geomagnetic compass.
The sensitivity of birds
to visual orientation stimuli is not surprising given that they
have well developed visual systems, and the idea of a sun and star
compass was quickly embraced by researchers. This was not the case
for the now well established behavioral ability of birds to orient
by the earth’s magnetic field. The problem with celestial cues is
that there are times, in some places frequently, when the sky is
obscured by clouds. Lengthy periods of time without access to
celestial orientation cues could substantially compromise survival
and reproduction if birds could not rely on some alternative
compass mechanism. In areas familiar to a bird, known landmarks
could serve as orientation cues. But what about a migrant flying
high over completely unfamiliar terrain? A sensitivity to the
earth’s magnetic field, the central nervous representation of
which still remains poorly understood, is the solution that
natural selection has provided birds for the challenge of compass
orientation without access to celestial cues. The experimental
demonstration of geomagnetic orientation is apparent when either
migrant birds or homing pigeons experience a shift in the ambient
magnetic field lines under conditions when they would rely on
non-visual cues for orientation. Simply, the birds shift their
orientation in parallel with the altered magnetic field. One
curious property of their magnetic compass is that it is not the
kind of compass that people use while hiking; a so-called polarity
compass. Rather, the bird geomagnetic compass is a so-called
inclination compass by which north and south are defined by the
angle the ambient magnetic field lines make with some vertical
reference like gravity (Wiltschko & Wiltschko, 1972).
Ontogeny: the importance of experience.
This book is about
spatial cognition, and the compass mechanisms described above
would not usually be considered in discussions of animal
cognition. At first glance they have an innate, reflexive quality
that might be of more interest to an ethologist than a traditional
comparative psychologist. However, as we will present below,
spatial behaviors readily identified as relying on “cognitive”
representations are grounded in these compass mechanisms under
field conditions. But labeling these compass mechanisms as innate,
even if they played no role in higher order spatial cognition,
would be an oversimplification. Young birds must experience the
sun’s arc across the sky if they are to use it as a compass cue
(Wiltschko & Wiltschko, 1981). Even seeing the movement of the
sun during only one part of the day, for example the afternoon,
enables young birds to make meaningful inferences about the sun’s
position at unfamiliar times of day, in this case the morning
(Budzynski et al., 2000). Birds must continually adjust to the
changing solar ephemeris due to the shortening and lengthening of
the day, a challenge compounded in migrants because of their
geographical displacements.
For nocturnal
migrants that use the stars to orient, similar experience is
required. Failure to see the night sky during their first summer
renders young birds unable to use the stars to guide their first
migration. However, even experience with a night sky rotating
around a false axis, like a planetarium sky rotating around
Betelgeuse in Orion, or a completely artificial rotating night sky
is sufficient to enable young birds to adopt the point of rotation
as a migratory reference. In the northern hemisphere, young
experimental birds during their first migration will orient away
from the point of rotation, or “south”, thus displaying meaningful
migratory behavior (Emlen, 1970).
The type of
deprivation experiment that easily identifies a crucial role for
experience in shaping how birds use the sun and stars as a compass
has not been carried out with respect to the earth’s magnetic
field. However, geomagnetic orientation is responsive to
experience, and this is most apparent when conflicting information
about the direction of migration is provided by the different
compass mechanisms.
Compass mechanisms: interactions among the
different cues.
Some have
described the orientation mechanisms of birds as “redundant”.
However, the term redundant, suggesting that the different sources
of compass information provide identical information, is clearly
inappropriate. There is nothing redundant about the earth’s
magnetic field when the sun or stars are obscured by clouds.
Similarly, there is nothing redundant about the sun or stars for
birds near the magnetic equator where the inclination of the
earth’s magnetic field would render geomagnetic orientation
ambiguous. Multiple sources of compass information are clearly
adaptive. But multiple sources also raise the question of whether
orientation mechanisms are organized hierarchically; is one source
of information preferentially used over the others, and might
orientation to one cue be calibrated against another?
The answer to this
question is not straightforward. For young birds learning about
environmental orientation cues during their first summer, both
North American and European species seem to preferentially rely on
celestial cues, in particular the sun and patterns of skylight
polarization, as a geographic reference to define north. Young
birds will in fact use celestial cues to determine their migratory
orientation with respect to the ambient magnetic field (Bingman,
1983). The use of celestial cues to calibrate orientation to the
earth’s magnetic field is adaptive because whereas the point of
celestial rotation provides a temporally and spatially stable
reference to define geographic compass directions, variation in
the earth’s magnetic field in space and time render it less
reliable.
In adult,
experienced migrants the relationship between geomagnetic and
celestial orientation mechanisms depends on geographic location.
In Europe, magnetic field information is preferentially used to
calibrate orientation to celestial cues indicating an ontogenetic
shift in the hierarchy among the orientation mechanisms (Wiltschko
& Wiltschko, 1975). By contrast, in North America, at least at
more northern latitudes, celestial information continues to be
preferentially used to calibrate orientation to the ambient
magnetic field (Able & Able, 1990; Cochran et al., 2004).
These findings raise the question of why North American and
European experienced migrants should behave differently? A likely
answer is related to the relative stability of sun and geomagnetic
information as birds migrate in time and space (Bingman et al.,
2003). As a bird migrates south in North America, changes in the
angular distance between geomagnetic north and geographic north
(declination) and changes in the compass direction of the setting
sun are similar. There would be no advantage to shift away from
the developmental pattern of preferentially relying on celestial
cues. By contrast, as a bird migrates south in Europe, the angular
distance between geomagnetic north and geographic north remains
essentially constant while the direction of the setting sun
changes as the migratory season progresses. Therefore, for European migrants, it would be adaptive to
adopt the earth’s magnetic as the preferential orientation cue
once migration begins because of its stability as a directional
reference.
Compass mechanisms
enable birds to define directions in space to guide oriented
movement. However, a compass does not inform an organism of
where it is in space. That birds have a map sense of where,
in addition to a sense of direction, is readily attested to by their remarkable ability XXX to return to the same breeding and
wintering sites year after year, and their ability to do so even
after dramatic experimental displacements; the most notable
example of which is the homing ability of pigeons. However, not
all goal navigation necessarily requires a map sense of where.
Getting there without knowing where.
Many typically diurnal
songbirds will carry out their first migration at night alone in
the absence of any stable social network. Yet the vast majority of
these birds will reach their species typical over-wintering area
often thousands of kms away. It is difficult to imagine that such
birds have acquired map-like knowledge of their migratory route in
the absence of any previous experience, so how do they succeed?
The answer is a remarkable example of genetic programming
(Berthold, 2003). Although the development of celestial sun and
star compass mechanisms requires experience, the initial
orientation angle a bird makes with respect to those cues seems to
be innate. Once a bird is able to define directional space using
the sun, stars or earth’s magnetic field, how they orient on their
first migration, although amenable to change, is innately
represented in the nervous system. This innate directional
preference can start a naïve migrant moving at least in the
direction of its population specific over-wintering site. In fact,
the genetic programming can be so sophisticated as to include
appropriate changes in direction, for example, when some European
species shift their orientation from southwest to south as they
approach Africa (Wiltschko & Gwinner, 1974).
 |
Figure 4. Hand-raised black caps from a northern
population that naturally migrate farther (blue) display
more nights with nocturnal migratory activity (A) and a
greater percentage of migratory active individuals (B) than
black caps from a more southern population (red). Crosses
between northern and southern population individuals produce
F1 birds (purple) that display intermediate levels of
migratory behavior. |
But what about distance, how
does a naïve migrant know how far it should fly? The solution to
this challenge seems to be time (Figure 4). The genetic program
that appears to guide a young bird’s first migration includes how
long it should be active migrating (Berthold & Querner, 1981).
This was elegantly demonstrated by studying different populations
of European black caps (Sylvia atricapilla). Identically
hand raised young black caps from a long-distance migratory
northern population and a short-distance southerly population were
tested in cages for the amount of nocturnal activity displayed
during their first fall migration. Young birds from the northern
population displayed substantially more migratory activity for a
longer period of time during the fall compared to the southern
population. Interesting from a genetic perspective, crosses of the
northern and southern populations produced young that displayed
intermediate levels of migratory activity. The genetic program
that guides a young bird’s first migration seems to control
distance by controlling the amount of time a bird engages in
migration.
In summary, a young bird on its
first migration succeeds in navigating to its population specific
over-wintering site without a map sense of where. A genetic
program that defines which direction and how long to fly seems
sufficient to get them close, and in the literature this type of
navigation is often referred to as “vector navigation”.
Getting there and knowing
where.
As programmed as a
young bird’s first migration may be, experience provides them with
opportunities for a far richer representation of space that
enables a map-like sense of almost global proportions. This map
sense can be used by birds to navigate to specific goal locations
following displacements to unfamiliar places sometimes thousands
of kms away. Layson albatrosses (Phoebastria immutabilis),
white-crowned sparrows (Zonotrichia leucophrys), European
starlings (Sturnus vulgaris) and routinely homing
pigeons (Columba livia) are examples of species that
have been used in displacement experiments, successfully
demonstrating ability to goal navigate over unfamiliar
terrain.
For a bird to have a map-like
representation of space, it needs to take advantage of some
spatial variation in the quality of environmental stimuli. For a
map of a familiar (experienced) environment, this variation may be
the spatial relationship among landmarks; such landmarks would be
typically visual (Biro et al., 2005; Gagliardo et al., 2001; Lipp
et al., 2004) but potentially of other sensory modalities as well.
In fact, the spatial relationship among the familiar landmarks and
goal locations is likely represented in a directional framework
defined by the sun or some other compass mechanism described above
(Bingman & Jones, 1994). An important point is that a bird
would not be able to extrapolate a map of familiar landmarks
beyond the range of sensory contact with the landmarks. But the
map sense of birds XXX extends well beyond the boundaries of
the sensory range of their experienced space.
|
Figure 5. Conceptualization of Wallraff’s gradient
model of a navigational map. In this hypothetical example,
variation in geomagnetic field inclination (far right black
lines) increases to the north (Y axis, orange dashes of
increasing thickness bracketed by arrows). By contrast, a
source of atmospheric odors (city to the left) creates an
odor gradient that decreases to the east (X axis, green
dashes of decreasing thickness bracketed by arrows). A
homing pigeon transported to a location southeast of home
would measure its relative displacement by determining the
difference between the local atmospheric odor intensity and
geomagnetic field inclination with the home values (relative
values ranging from +10 to -10). Once the direction of
displacement is determined, a homeward vector, or at least
direction, can be computed. |
The challenge of a map that
extends beyond the range of experienced space is that when a bird
is displaced beyond the boundaries of familiarity it must infer
its location relative to a goal location. As conceptualized by
Wallraff (1974), a bird’s map of unfamiliar space could be based
on the qualities of two environmental stimuli that vary
predictably in space in a gradient like fashion (Figure 5).
The gradient axes of the two stimuli must also intersect, not
necessarily orthogonally, to create a bi-coordinate grid-like
system. Using the homing pigeon as an example, let’s assume that
with respect to the home loft the quality of stimulus x increases
to the north and decreases to the south, the quality of stimulus y
decreases to the east and increases to the west. A pigeon learns
the predictable properties of this variation during flights over
familiar areas. More importantly, what a pigeon learns has the
properties of an algorithm such that it can infer how the
qualities of the stimuli change beyond its area of
familiarity. When a pigeon is now displaced to the southeast beyond the range of familiarity, it will detect an decrease,
compared to the home loft, in the quality of stimulus x and infer
its relative displacement northward. It will also detect a
decrease in the quality of stimulus y and infer its relative
displacement westward. The pigeon could then essentially locate
its position on the gradient map to compute a vector or at least
direction home to be read off one of its compasses.
Wallraff's elegant model can explain goal navigation from unfamiliar locations, but is it right? The first challenge is to identify environmental stimuli that have the requisite qualities of predictably varying in space. It is not surprising that properties of the earth's magnetic field other than those used to define compass directions have been popular candidate stimuli. On a coarse global scale, a number of geomagnetic parameters, e.g., geomagnetic inclination, vary predictably in space. Therefore, assuming a sensory system capable of detecting often very small differences, two of these geomagnetic parameters with intersecting gradient axes could be used to construct a map. Unfortunately, for homing in pigeons on a scale of tens to a few hundred kms geomagnetic variation can be very noisy and only poorly predict relative location. Also, there is practically no experimental evidence that favors the presence of a geomagnetic map in homing pigeons (Wallraff, 1999). However, recent work with migrant birds in Australia (Fischer et al., 2003), and theoretical considerations (Bingman & Cheng, 2005), are consistent with the possibility of coarse scaled, geomagnetic map information operational at much larger distances from a goal.
If not the earth’s magnetic
field, then what? Surprisingly, the answer seems, at least in
part, related to spatial variation in the distribution of
atmospheric odors (Wallraff, 2001). Numerous experiments carried
out in homing pigeons have demonstrated that olfactory deprivation
sabotages homing ability from distant, unfamiliar locations while
sparing homing from sites where familiar landmarks can be used as
an alternate source of navigational information. More impressive,
false olfactory information, in other words releasing pigeons from
one unfamiliar location while being exposed to odors from another
location, leads to predictable changes in the direction flown by
pigeons upon release. The orientation of the “fooled” pigeons is
consistent with them being released from the site recognized by
the odors and not their actual location.
Could variation in the spatial
distribution of atmospheric odors make up one or both of the
gradients in Wallraff’s model? Developmental studies have
demonstrated that even homing pigeons held in an outdoor aviary
without XXX the opportunity to fly can learn an olfactory
navigational map. Under these conditions, it is difficult to
imagine how a gradient map can be learned without a bird
experiencing quantitative differences in stimulus quality while
actively moving through space. Birds held in an outdoor aviary
learn an olfactory navigational map by associating different odor
qualities with winds from different directions. Rather than learn
a gradient map, they learn what has been described as a “mosaic
map”, in which patches of different atmospheric odor qualities are
associated with different compass directions (Papi et al., 1972).
Note again that a compass mechanism, like the sun compass, would
be used to represent how odors vary in space. When subsequently
released from a distant, unfamiliar location, a pigeon would
sample the odor profile at the release site, recall the wind
direction associated with that odor profile experienced at the
loft and then, using its sun or magnetic compass, fly off in a
direction opposite from the associated wind direction.
Interesting, such a mechanism would render what are ostensibly
unfamiliar locations “familiar”. The odor profile of unfamiliar
sites would be “familiar” to the pigeons because of the odor
profile having been transported to the loft by winds. Odor profile
would take on the quality of a landmark that could be experienced
remotely because of wind.
So does such a mosaic map of
atmospheric odors completely solve the problem of navigation after
displacement to a distant, unfamiliar location? Probably not. The
primary obstacle is that successful navigation can occur over
hundreds of kilometers beyond a range conceivable for wind borne
odors to be reliably brought to one site like a pigeon loft. How
would a pigeon discriminate between an odor profile from the north
50 kms away compared to one from the north 500 kms away? It may
well be that a mosaic map is operational over relatively short
distances (50-100 kms) and a gradient-like map is operational over
longer distances. But is there any evidence that pigeons can learn
two types of dissociable navigational maps? We will discuss the
role of the hippocampal formation in avian spatial behavior in
more detail below, but it is noteworthy that young homing pigeons
with hippocampal lesions are unable to learn an olfactory
navigational map when held in an outdoor aviary; a presumptive
mosaic map (Bingman et al., 1990). By contrast, young homing
pigeons with hippocampal lesions can learn an olfactory
navigational map if given the opportunity to fly freely from the
loft under conditions when the gradient quality in odor profile
could be sampled as the birds move through space (Ioalé et al.,
2000). The different effects of hippocampal lesions on
navigational map learning under conditions of varying experience
are consistent with the two map idea. One would be a hippocampal
dependent mosaic map operational over relatively short distances,
the other a hippocampal independent gradient map operational over
much larger distances.
It must be admitted that the
proposal of an olfactory navigational map has not been unanimously
embraced by researchers in the field. A frequent criticism has
been the intuitive difficulty accepting that the spatial variation
in atmospheric odors is stable and predictable enough in space and
time to support a gradient or mosaic map of the types described
above. This criticism has now been successfully answered by
research actually measuring spatial variation in trace atmospheric
substances over distances homing pigeons routinely return from. If
one looks not at one substance but the relationship among the
concentrations of numerous substances, the spatial variation of
that relational quality is stable and predictable enough to
support a gradient map and explain how homing pigeons can identify
the direction home from hundreds of kms away (Wallraff, 2004).
We are comfortable with the idea
that homing pigeons can rely on atmospheric odors to construct a
navigational map, and that they do so in different global regions
with substantial differences in climate. There is evidence that
other species of birds can use a similar navigational mechanism
over relatively short distances (50-100 kms). But it seems
impossible to explain migrations of thousands of kms based on map
of atmospheric odors. What type of environmental stimulus could
serve as an element in a gradient map of this scale? Although not
necessarily satisfying given the general lack of empirical
support, and despite Wallraff’s admonishment (Wallraff, 1999),
there is a persistent temptation to think that at some point the
answer will be related to some variation(s) in the earth’s
magnetic field (Bingman & Cheng, 2005). However, one should be open to any theoretically
possible solution as the sensory and cognitive abilities of birds
continue to offer surprises.
Under natural
conditions, birds display an enormous range of spatial behavior
mechanisms including different compass mechanisms, vector
navigation, navigation by familiar landmarks, and mosaic and
gradient maps of atmospheric odors. But there is no reason to
think we have fully uncovered all the ways birds represent space
or their sensory basis. The different behavioral mechanisms would
be supported by different neural representational mechanisms,
which would to a lesser or greater extent be supported different
brain regions. To date, it is the hippocampal formation (HF) that
has been most extensively studied in the context of avian spatial
behavior, and not surprisingly, its importance appears restricted
to only a subset of the behavioral mechanisms described above.
Although playing some role in navigational map learning under
conditions of confinement in homing pigeons, the available data
indicate that the prevailing role of HF in the spatial behavior of
birds is in the map-like representation of familiar landmarks used
to guide goal navigation over familiar terrain.
Lesion and immediate early gene studies.
The very first study
examining the effects of HF lesions on the homing behavior of
experienced pigeons was accompanied by the disappointment of
beautiful homeward orientation from a distant, unfamiliar location
and the mystery that the lesioned birds never showed up at the
loft (Bingman et al., 1984). How could one explain an intact
navigational map but failed homing? The hypothesis that was put
forth was that as a pigeon approaches its home loft it becomes
increasingly reliant on familiar landmarks to guide the final
phases of the homing flight, and it is navigation by familiar
landmarks that engages HF. The importance of HF for familiar
landmark navigation has subsequently been demonstrated in numerous field and
laboratory studies, but we will only highlight two to illustrate
the complexity of this relationship.
Intact and HF
lesioned homing pigeons were trained from two familiar locations
and then tested to reveal the kind of landmark-based strategy they
learned to return from the familiar sites (Gagliardo et al.,
1999). When tested, the pigeons were rendered anosmic. Blocking
the ability to smell would eliminate the ability of the birds to
rely on their olfactory navigational map to return home, thus
forcing them to rely exclusively on their representation of
familiar landmarks. They also had their internal clocks
phase-shifted. Conceptually, homing pigeons could use familiar
landmarks as an independent map and guidance system, using the
landmarks to guide their flight home by serially locating their
position in space and noting their movement with respect to the
landmarks. Alternatively, they could simply use the landmarks at
the familiar release site to recall the compass direction flown
from that site during training, and then use their sun compass to
take up the homeward bearing. Phase-shifting would dissociate
these two strategies. Navigating home by gauging movement with
respect to the familiar landmarks alone would not be influenced by
the phase-shift manipulation. By contrast, recalling the compass
direction home and then orienting by the sun would result in a
shift in orientation away from the homeward direction.
|
Figure 6. A. Two five-landmark array environments
that differed in the spatial (topological) relationship of
the landmarks (e.g., the purple spool was counter-clockwise
of the star in one environment and counter-clockwise of the
red pyramid in the other). The green bowl contained food in
one environment (arrow); the blue bowl in the other (arrow).
The red bowl never contained food. B. Control pigeons (blue
line) successfully learned to discriminate the two landmark
arrays to choose the correct food bowl. At the end of
training they were getting close to 90% of all trials
correct. Although the HF lesioned birds (red line)
learned to preferentially choose the green and blue food
bowls and not the red, they never learned to associate the
green and blue bowls with the correct landmark
array. |
The results of this
study demonstrate how subtle the differences can be in the
navigational strategies used by control and HF lesioned pigeons.
Control pigeons oriented in a direction approximating the true
direction home, and therefore, were for the most part uninfluenced
by the phase-shift manipulation. They used the unspecified array
of familiar landmarks in a map and guidance-like fashion. By
contrast, the HF lesioned pigeons displayed a shift in orientation
away from the home direction indicating that they relied on their
sun compass once determining their location relative to home,
presumably by recognizing landmarks at the training site and then
recalling the compass direction home flown during training. It is
clear that the map-like spatial memory representation learned by
the control pigeons was much richer in terms of spatial
information available and the potential for inferring route
corrections in the event of displacement. This ability requires
recruitment of HF. Simply learning to associate a compass
direction with a cluster of familiar landmarks, instructed by the
olfactory navigational map available during the training phase of
the study, does not require an intact HF.
It is appealing to label the
spatial learning of the control pigeons in the previous study as
reflecting map-like or spatial relational learning; what has been
called a cognitive map (O’Keefe & Nadel, 1978). However, under
field conditions it is prohibitively difficult to determine if
landmarks are actually being used and how they are represented
(but see Guilford et al., 2004; Lipp et al, 2004); the landmarks
can’t be manipulated. In a companion study (Figure 6), control and
HF lesioned pigeons were trained to discriminate between two
landmark arrays, which varied with respect to the spatial
relationship among the landmarks, to determine which one of three
possible goal locations contained food (White et al., 2002). The
landmarks used in the two arrays were identical, just their
spatial relationship with respect to each other varied between the
two conditions. Control pigeons were successful in discriminating
between the landmark arrays. In striking contrast, the HF lesioned
pigeons gave no indication of learning that the spatial
relationship among the landmarks was different in the two
conditions. This laboratory study, together with the previously
described field study, offer compelling evidence that the avian HF
is crucial for successfully representing landmarks in a map-like,
relational manner; a map that can then be used to guide to
navigation among goal locations.
The usefulness of
lesion techniques for the study of brain-behavior relations is
indisputable. However, it is desirable that conclusions drawn from
lesion studies be supported by less invasive experimental
procedures. One such procedure relies on the activation of
so-called immediate early genes that are thought to be often
recruited when some type of neuronal re-organization in support of
learning occurs. For both homing pigeons learning to navigate by
familiar landmarks (Shimizu et al., 2004) and a species of
songbird remembering the locations of cached seeds to be recovered
later (Smulders & DeVoogd, 2000), increased activation of an
immediate early gene has been observed in HF. Both the lesion and
immediate early gene data converge on the conclusion that the
avian HF is critical for landmark-based, map-like representations of space.
Unit recording studies.
The realization that the
avian HF is crucial when map-like representations are recruited to
navigate and recognize salient locations in space raises the
challenging question of how space may be represented at the level
of the response properties of HF neurons (units). As background to
this question are the well described “place cells” found in the
rodent hippocampus (O’Keefe & Nadel, 1978). Place cells are
neurons that routinely display large increases in activity when a
laboratory rat is at a restricted location in an experimental
environment. The place cell has shaped discussion of hippocampal
function since its discovery more than 30 years ago, and
necessarily looms as a standard by which HF unit response
properties in other species are measured. However, given the
substantial differences in spatial ecology and evolutionary
history between rats and birds like homing pigeons, it is likely
that the spatial response properties of HF neurons would differ
between the two groups in some adaptive fashion.
![]()
|
Figure 7. Video illustration of a homing pigeon,
navigating an analogue 8-arm radial maze (Hough and Bingman,
2004), with HF implanted electrodes connected to a recording
cable. |
In fact, recordings
of HF neurons carried out in freely moving homing pigeons
navigating a laboratory environment (Figure 7) have yet to reveal
place cells so easily encountered in rats. Rather, what have been
found are neurons of two types that are relevant to the challenges
of navigating and recognizing locations in space (Hough &
Bingman, 2004; Siegel et al., 2005; Siegel et al., 2006). One
type of neuron is characterized by a tendency to display increased
levels of activity (action potential firing rate) when a pigeon is
at or near a goal location; a type of neuron we have referred to
as a “location” cell. Although perhaps superficially
resembling place cells, these pigeon HF location cells differ from
rat place cells with respect to a number of response property
characteristics. The second type of neuron is characterized by a
tendency to display increased levels of activity when a pigeon is
moving through corridors that leads to and from goal locations;
what we have referred to as a “path” cell. The types of
response properties described are consistent with the speculation
that homing pigeon HF neurons participate in relating the position
of goal locations with the computation of navigational
trajectories that lead to those locations. But perhaps the biggest
surprise is that neurons with different response properties tend
to lateralize to the HF on different sides of the
brain.
A lateralized HF: Adaptation for navigating
avian space?
The
functional lateralization of the vertebrate forebrain was once
thought to be a uniquely human characteristic. However, it has now
been clearly demonstrated that the avian forebrain is similarly
lateralized with the different hemispheres preferentially
recruited in the control and expression of different behavior
(Güntürkün, 1997). This has been convincingly shown in the domain
of spatial behavior in a number of bird species such as chicks,
homing pigeons and songbirds. More recently, the asymmetrical
contribution of the HFs of the two forebrain hemispheres in
guiding spatial behavior has been revealed. In one lesion study
carried out in homing pigeons (Kahn & Bingman, 2004), birds
were trained to locate a food goal by relying on landmark cues
locally distributed in the experimental environment, which birds
could move through (Figure 8). They could also rely on distal cues
such as light fixtures and markings on the walls and ceiling in
the room where the experimental environment was located. Pigeons
with left and right HF lesions both learned the task without
difficulty. However, the spatial representation that guided their
behavior, as revealed by probe trials that set information from
the local landmarks in conflict with the distal room cues, was
notably different. Pigeons with left HF lesions overwhelmingly
relied on the distal room cues to locate the goal and behaved as
if the local landmarks did not exist. By contrast, pigeons with
right HF lesions used the distal room cues less and were more
reliant on the local landmarks to locate the goal. The results
suggest that the right HF may be more important for the
representation of goal locations reliant on global/distal
properties of an environment. It is interesting to note that
pigeons with right HF lesions can also use the sun compass to
learn the location of a goal or an olfactory navigational map;
both of these spatial abilities are impaired in pigeons
with left HF lesions.
 |
Figure 8. In a lesion study carried out in homing
pigeons (Kahn and Bingman, 2004), birds were trained to
locate a food goal by relying on landmark cues locally
distributed in the experimental environment the birds could
move through. Figure A shows the goal location in training
while figure B shows the birds selection of the goal
location in probe trials. |
The different
sensitivity of the right and left HF to different aspects of space
as revealed by the lesion studies is paralleled by unit recording
data (Siegel et al., 2006). The occurrence of location and
path cells described above do not distribute symmetrically in the
HFs of the two hemispheres. Location cells are more likely to be
found in the right HF while path cells are almost exclusively
found in the left HF. The spatial response profile of neurons in
the left and right HF also differ in other respects, the most
notable of which is the greater temporal stability or reliability
in the spatial variation in firing rate of left HF cells. Neurons
in the left HF likely participate more in representing aspects of
space that are stable in time.
Reconciling the lesion and unit recording
data.
Surveying the
lesion and unit recording data reveals a complex picture of HF
function and its apparent defining characteristic of
lateralization. This lateralized quality is interesting because
the human HF is also lateralized while there is little indication
of it in the rat. When the dust settles, lateralization, and
particularly HF lateralization in the context of spatial behavior,
may be a defining adaptive feature of the avian HF organization
that explains in part the extraordinary ability of birds to
navigate space (Bingman et al., 2003). But what is really
lateralized? As a working model, we view the right HF as
preferentially participating in the representation of goal or
“event” locations (location cells) defined by global spatial
features of the environment (lesion data). By contrast, the left
HF preferentially participates in navigating the environment and
computing trajectories among goal locations (path cells) relying
on map-like representations of landmarks learned with the
aid of directional cues like the sun compass. However, it
must be emphasized that the proposed functional asymmetry is in
some sense an experimental artifact. In intact pigeons, the two
HFs work cooperatively and collectively in supporting behavior;
goal navigation requires an ability to determine a path trajectory
or route as well as recognize the location of a goal once close. A
very large hippocampal commissure offers testimony that the two
HFs function as an integrated unit in the control of spatial
behavior. Indeed, XXX navigating by familiar landmarks in the field as
described previously is disrupted by either left or right HF
lesions (Gagliardo et al., 2002). Neurons in the left and right HF
may be preferentially sensitive to different aspects of space, but
both are required to support the challenge of navigating by a
map-like representation of familiar landmarks.
Traditionally, the
study of comparative psychology has relied on controlled
experimental settings in an intellectual environment shaped by
learning theory. Although undeniably successful as a science, this
research may have necessarily diminished the detection of species
differences as subjects were tested in laboratory environments
that often failed to promote the expression of species typical
behavior and the cognitive mechanisms that support them. The
research described in this chapter is inspired by a complementary
approach to comparative psychology that draws on the lessons of
ethology. It can be taken as axiomatic that during the course of
evolution species ecology and natural history have substantially
shaped the relationship among brain organization, behavior and the
underlying cognitive processes that support behavior. The unique
suite of spatial behavior mechanisms that birds rely on to
navigate space, from a magnetic compass and vector navigation that
require little experience to become operational to open-ended, HF
mediated familiar landmark navigation, can all be viewed as
adaptive responses to the challenges of their spatial ecology.
From this perspective it is easy to understand why the homologous
HF of rats and homing pigeons can differ in the qualities of space
represented. More subtle HF differences can be expected even among
different species of birds or any taxonomic group. In our view, a
growth area in comparative psychology is a revitalized interest in
an experimental philosophy that encourages the expression of
species typical behavior accompanied by research into supporting
neural mechanisms. The comparative study of spatial cognition is
an example of how successful this approach can be.
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