HIPPOCAMPUS, VOL. 1, NO. 3, PAGES 240-242, JULY 1991
Multiple Representations in the
Hippocampus
random sample from the population. Thus, if two environments are independent, the active subset in each is an independent sample from the total pool of hippocampal complex-spike cells. As a consequence, most cells in the active
subset of one representation are not in the active subset of
the second. The second feature of complete remapping is
John L. Kubie* and Robert U. Mullert
that, for a cell that happens to be in both active subsets, there
is no relationship between its two spatial firing patterns. For
such cells, the location of the firing field in one environment
Departments of *Anatomy and Cell Biology and
is random with regard to the location of the field in the second
+Physiology, SUNY Health Sciences Center at
environment.
Brooklyn, 450 Clarkson Avenue, Brooklyn, N Y
F o r concreteness, we will describe as a prototype of com11203 U.S.A.
plete remapping the transformation that takes place between
a gray cylinder with a single white cue card on the wall and
The discovery of place cells (O’Keefe and Dostrovsky, a gray rectangular enclosure with a similar white cue on the
1971) is the finding that most strongly implicates a spatial wall (Muller and Kubie, 1987). In both environments, the
processing role for the hippocampus. In this essay we will rat’s task is to chase food pellets scattered on the floor, inreview evidence that the space represented by the hippocam- ducing the rat to visit all portions of each chamber. Since one
pus is “chunked” into segments called “environments.” This possible explanation of apparent remappings is that complex
is not a new idea; it was indirectly suggested several times topological transformations have occurred, this pair of enby O’Keefe and Nadel in The Hippocampus L I S 0 Cognirive vironments has the advantage that the rectangle is related t o
M u p (1978). A consequence of the notion that the hippocam- the cylinder by simple topological rules. The results were as
pus represents environments is that the hippocampus stores described above for remappings. On most occasions, a cell
many environmental representations. only one of which is with a firing field in one apparatus was not part of the active
active at any given time. The bulk of this essay is aimed at set in the second apparatus. On occasions when cells had
stating consequences of the fact that the hippocampus stores firing fields in both apparatuses, there was no predictable
relationship between the shapes or locations of their firing
(or has access to) multiple environmental representations.
Before proceeding, it is useful to make explicit what we fields. On qualitative analysis, no topological transformations
mean by an environment. We define an environment as the were evident.
Quirk ( 1990) quantitatively tested the topological transform
accessible space of a particular setting together with the cues
hypothesis
for neurons in the entorhinal cortex and the hipavailable for orientation. This definition is consistent with the
general experimental strategy of recording from place cells pocampus. His method stretched the firing rate map in a
while the rat is in an experimental apparatus that, itself, is square apparatus to a circle and compared the result to the
within a curtained enclosure.’ In such settings, it is relatively firing pattern in the cylinder. He found that stretching yielded
easy to demonstrate that place cell firing is determined by similar patterns for entorhinal neurons, but failed when apthe apparatus and other cues within the enclosure (O’Keefe plied to hippocampal place cells.
It is useful to consider the stretching hypothesis in further
and Conway, 1978; Olton et al., 1978; Muller and Kubie,
detail.
Implicit in this hypothesis is that any pair of cells with
1987). For instance, rotations of a set of controlled cues
neighboring
firing fields in one environment should have
within the curtains produces equal rotations of the spatial
firing patterns of place cells (O’Keefe and Conway, 1978). neighboring firing fields in any other environment. Therefore,
Thus, place cell firing signals the rat’s location with respect a powerful test would be to find cells with neighboring firing
to environmental cues and suggests that the rat hippocampus fields in one apparatus and observe their firing fields in another environment. Clearly, if the hypothesis is valid, the two
maps the current environment.
If an environment is what is mapped, what happens when cells must always have neighboring firing fields. Although,
the rat is put in a second o r a third environment‘! The ob- to our knowledge, this two-cell study has yet to be performed,
served results are quite simple. If the environments are suf- its outcome is almost certain. Given the unpredictable
ficiently different, a “remapping” will occur (O’Keefe and changes in firing patterns seen in single cell transitions, it is
Conway, 1978; Kubie and Ranck, 1984; Muller and Kubie, almost certain that in such an experiment, neighborliness
1987; Thompson and Best, 1989: Bostock et al., 1991). Re- would be destroyed. We will refer to the model where neighmapping has two fundamental features. First, the hippocam- borliness is maintained as the “stretched map” model and
pal representation of an individual environment makes use of the model where neighborliness is destroyed as the “scrama surprisingly small subset of potential place cells, the “active bled map” model. Complete remappings are consistent only
subset.” The size of the active subset is about 20% of the with scrambled maps.
pyramidal cell population, according to Thompson and Best
PROPERTIES OF MULTIPLE REPRESENTATIONS
(1989). Moreover, the subset used in each environment is a
-~
______
___
Lack of topographic organization
~~
~
~
~~~~~
’ Our definition describes experimental settings well but naturalistic
situations rather poorly. It is not clear what environmental boundaries
are in a rat’s real range. This is an important question. but outside
the scope of this paper.
In arguing that the hippocampus represents the accessible
space within an environment, one fact that has been troublesome to some is that there is no obvious topographic or-
240
MULTIPLE REPRESENTATIONS IN THE HIPPOCAMPUS / Kubie and Muller
ganization within the hippocampus. In general, cells that are
neighbors in the physical space of the hippocampus do not
have neighboring firing fields in the environment. This lack
of strict topography is evident when several neurons are
recorded from a single electrode. Neurons recorded from one
electrode are presumed to be near neighbors. If strict topography existed, such cells ought to have overlapping or neighboring firing fields. Several investigators have reported numerous instances in which distant firing fields are recorded
from a single recording site (O’Keefe and Speakman, 1987;
Muller and Kubie, 1987; although Eichenbaum et al., 1989,
have reported a weak topography). If one looks to isocortical
regions for instructive examples, this is worrisome. In isocortex in general, there is clear-cut topographic organization
in which neighboring neurons always have overlapping or adjacent receptive fields.
If, however, the scrambled map model pertains, lack of
strict topography is a necessary consequence. Imagine that
there is strict topographic coding of a single environment. In
such a situation, only neighboring neurons have neighboring
firing fields. If the hippocampus has an independent representation of a second environment (i.e., there is a complete
remapping), then almost no neighboring cell pairs will have
neighboring firing fields in the second environment. Thus,
topographic coding cannot exist in the second environment.
This same argument applies to all additional environments
that are independently represented. Therefore, at most, a single environment can have strict topography. Since it seems
unlikely that any environment is preferred, we argue that topographic mapping is unlikely in any environment.
A final point about the lack of topographic organization is
that it may be an inherent feature of allocortex. Although
isocortex can be characterized by crisp topographic representations of information, we know of no evidence of topographic representations in any allocortical structure. An example outside of the hippocampal formation is olfactory
cortex. The search for topographic organization within this
region has been in vain. Lynch (1986) has argued that coding
within olfactory cortex is not topographic. (Probably related
to the lack of topography in allocortex is the lack of pointto-point anatomical mapping of projections involving allocortical regions; Amaral and Witter, 1989.)
The cell population can identify the current
environment
Above, we noted that the active set of neurons is unique
to each independent representation. Thus, if some external
observer could monitor the output of the hippocampus for a
period of time while the rat walks about (about 1 minute),
most of the cells in active set of the environment would fire
and, in principle, the environment could be identified.
There is, however, a potential mechanism with much better
temporal resolution: monitoring the output of location-specific groups. We define a location-specific group as the set
of neurons that have place fields that overlap a particular
region of space. Thus, for every location in an environment,
there is such a group. Two points are important. First, when
a rat is in a location, all or most of the cells in the corresponding location-specific group will be active. This is an
implicit property of place cells: namely, when a rat walks
241
through a cell’s firing field, the cell will fire most of the time.
And, second, this set of neurons is unique, both to the location within the environment and to the environment itself.
This is a necessary consequence of complete remapping. Interestingly, if the stretched map principle applied, locationspecific groups would exist but would not be environmentally
specific. Each group could be activated in any environment.
Thus, an important feature of multiple representations is that
the firing of the set of hippocampal place cells can signal not
only the rat’s location within an environment, but also the
identity of the environment.
Commitment and inertia
A question related to the hippocampal identification of an
environment is how the system first recognizes an environment and how the recognition is either maintained or altered
for the duration of the exposure to the environment. Two
general observations are pertinent. First, when a rat is introduced to an environment, place cell firing is robust the first
time the rat enters the cell’s firing field. We have also brought
rats by hand from outside the environment directly into the
recorded cell’s firing field, and invariably the cell fires as soon
as the field is entered. This suggests rapid recruitment of the
appropriate representation-a
process we call “commitment.” The second observation is that once firing patterns
are established in an environment, they are resistant to
change for the duration of a recording session (usually 16
minutes). This observation has been made under conditions
with removed sensory cues (O’Keefe and Speakman, 1987;
Quirk et al., 1990) or ambiguous sensory cues (Sharp et al.,
1990). For example, if a cell is recorded with the lights on
and the lights are turned off, the firing pattern will remain
unchanged. If the rat is introduced into a dark chamber, the
firing pattern will frequently be different. Most remarkably,
this “different” pattern will remain even after the lights are
turned back on (Quirk et al., 1990). Thus, the set-up conditions appear to have a profound impact that lasts throughout
an exposure to the environment. We call the resistance to
changing the current representation “inertia.”
We would like to speculate on what might happen when
the rat is first introduced into a familiar environment and commitment takes place. On first entering, the rat must be in the
location appropriate for the firing fields of a certain locationspecific group. We imagine that a significant fraction, but not
all, of the cells in this group are indirectly excited by the
sensory cues that are unique to that location (McNaughton,
1989). Furthermore, since this is a familiar environment, the
cells of the group are mutually excitatory. Therefore, when
a substantial fraction of the location-specific group is activated, the entire group will be activated. As described above,
activation of a location-specific group contains sufficient information to signal an environment. The success in activating
a group is documented by the observation that all place cells
appear to fire appropriately immediately on the rat’s introduction to the environment. Full activation of a single location-specific group is, therefore, the proposed mechanism
of commitment. Commitment requires recognition of a specific location in a specific representation.
As described above, the representation has an inertia-like
quality that lasts for the duration of a recording session. We
242
HIPPOCAMPUS VOL. 1, NO. 3, JULY 1991
suggest two mechanisms of inertia. In the first, activation of
a single location-specific group sets up a rapid cascading
chain activating neighboring groups, etc., until all members
of the active subset have been activated. By a currently unknown mechanism. this activation “tags” the members of the
active subset. leaving them in an excitable state, with the
excluded neurons refractory to activation. This mechanism
has the advantage of defining the active subset, a process
that has important advantages. The difficulty with this mechanism is that there is no direct evidence that tagging is possible.
The second proposed mechanism of inertia is simpler. It
also begins with the activation of a single location-specific
group. Triggering a location-specific group will excite members of adjacent location-specific groups. An adjacent location-specific group can be successfully activated by this excitation combined with the rat’s movement. For this adjacent
group to be activated it must be consistent with the rat’s
movement and with the initial group. As the rat moves
through the environment, a sequence of group excitations will
occur, each consistent with previous group excitations and
the rat’s movements. Thus, all activity will be consistent with
a particular environmental commitment made on initial entry.
This slow chain of group excitations will be broken only when
the rat is removed and enters a new environment, thus evoking a new representation.
CONCLUSION
A fundamental property of the hippocampal representation
of space is that space is “chunked” into units we have called
environments. The existence of many discrete representations raises fascinating questions in the realms of animal behavior, neuroscience, psychology, and artificial intelligence.
In this essay we have summarized some of the evidence that
discrete representations really exist and some of the properties of these representations. It is our feeling that in the 13
years since the publication of T l z ~Hippocampits as u Cognitiw M a p , we have learned a lot, but the issues, as they
have crystallized, have become more complicated. In particular, the process of creating, maintaining, and using multiple
independent representations deserves a great deal of attention.
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