1YIPPOCAMPUS, VOL. 1, NO. 3, PAGES 250-252, JULY 1991
Exceptions to the Rule of Space
Robert J . Sutherland* and Jerry W. Rudy?
*Department of P s y c h o l o g y , The University of
Lethbridge, L e t h b r i d g e , A l b e r t a , C a n a d a , T l K 3M4
and ? D e p a r t m e n t of Psychology, Muenzinger
Psychology Building, University of Colorado,
Boulder, CO 80309 U . S . A .
There are many points in Nadel’s paper with which we
heartily agree. At a general level we most strongly agree that
a good theory of hippocampal function should be explicit and
unambiguous about the kind of information that the hippocampal formation is handling. As Nadel points out. many contemporary positions are limited by their inability to say anything plainly about this issue-they are limited in that they
seem to make few clear predictions and seem to lack generality across species and behavioral paradigms. This has not
been the case with O’Keefe and Nadel’s position. A key point
that should not be lost is their assertion that the hippocampal
formation is essential for place learning. that is, for situations
in which the topographical relationships i n the environment
come to guide an animal’s behavior. This was a very bold
claim in the mid-1970s and, to the surprise of most of their
contemporaries, the subsequent experimental record is basically unanimous-they were right. Repeatedly, in the hippocampal lesion literature using nonprimates the presence of
a specific place learning requirement in a task. as opposed
to, for example, working memory, temporary memory buffer.
or other nonspatial requirements, has been shown to be critical in detecting a behavioral impairment.
For those of us convinced of the basic correctness of this
central assertion by O’Keefe and Nadel, more data demonstrating the existence of an intimate link between hippocampal circuitry and place memory do not further sprcjfictil1.v
strengthen O’Keefe and Nadel‘s theorv. For example. the
demonstrations that certain forms of spatial memory of birds
are affected by damage that includes the hippocampal formation will not allow, by themselves, further elucidation of
the specific contribution of hippocampal circuitry in solving
spatial problems. The same holds for the association between
variations in the size of hippocampal components and variations in performance in hippocampal-sensitive tasks. such as
two-way active avoidance. These new data do not add a novel
kind of support for O’Keefe and Nadel‘s explanation for ~ ’ h
the hippocampal formation is important for place learning.
The nub of our story is this: O’Keefe and Nadel assert that
instances of impaired learning and memory in animals with
damage to the hippocampal formation are caused by the elimination of an explicitly topographical, mnemonic representation of the environment, that the kind of information that
the hippocampal formation handles is necessarily spatial; we
part company with them here. We have chosen a different,
although not unrelated, path in accounting for the specific
contribution that the hippocampal formation makes to learn-
ing and memory. On reviewing the hippocampal literature,
we were impressed with two things: place learning is impaired
after HPC damage, and there are several instances of impairments that do not appear to fit well with the idea that the
hippocampal formation makes its special contribution to
memory by constructing and storing spatial maps of the environment. We have already dealt in detail with these “exceptions” (Sutherland and Rudy, 1989).Nadel acknowledges
that the last 15 years of experiments on the hippocampal formation have produced “a small number of exceptions” to his
position. It is in this small, unassimilated fringe (which Nadel
also acknowledges contains one of the human hippocampi),
where we set up camp. We felt motivated t o find some way
of characterizing the kind of information unique to the hippocampal formation so that both the place learning impairment and the “exceptions” could be explained in the same
manner. It was also important to us that our way of chara c t e r i h g hippocampal function should predict new behavioral situations in which hippocampal circuitry makes an essential contribution. We were also fortunate to have read
Hirsh’s (1974) paper, which prompted us to believe that following the path we have chosen was not altogether unreasonable.
Our position is that hippocampal circuitry is necessary if
a problem cannot be solved on the basis of strengthening o r
weakening associations between elementary stimulus events,
that is, if an animal must form associations between cue conjunctions and some other event. Topographical relationships
are but one example of the many kinds of cue conjunctions
or relationships that are possible. Essentially. the hippocampal formation enables an animal to disambiguate the significance of an elemental stimulus o r cue when the meaning of
that cue depends upon its relationship to one o r more other
cues. Place learning falls into the category of impaircd abilities precisely because if an animal must navigate to a specific
location using topographical relationships among cues. then
the way that an animal should move when it is facing any
particular cue is ambiguous: the cue’s significance for guidance necessarily depends upon its relationship to some other
element of the environment. starting location. other perceptible cues, etc. If the animal can solve the spatial problem by
using only a single element of the situation t o guide its movements, then by definition this would require only it taxon
strategy for solution, or, to use our terminology. a simple
association solution. Nadel states quite clearly that he is not
averse to the idea that one 01‘ the human hippocampi represents information that is more “abstract” than physical
space. We are saying something similar about the hippocampal formation in both hemispheres of all species-primates
y to birds to fish. Species differ dramatically in the kinds of
perceptual o r motor information represented by activity in
ensembles in neocortical zones and other structures that provide input to the hippocampal formation. ’Therefore, the kinds
of cues or events that can enter into hippocampal-based configural associations may differ dramatically among species.
Our view clearly predicts that it should be possible t o find
examples of impaired configural memory after hippocampal
damage, in addition to. and quite apart from, those involving
spatial mapping-this search is of course hopeless if O’Keefe
and Nadel’s theory is more in line with hippocampal function.
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EXCEPTIONS TO THE RULE OF SPACE / Sutherland and Rudy
We will describe three examples of memory impairments
that d o not confirm the spatial mapping position, but that are
predicted by configural association theory (Sutherland and
Rudy, 1989). If our interpretation of these results is correct,
it is probably the case that, at least in mammals, the memory
deficit after hippocampal damage includes relational information that is both spatial and nonspatial. Our first example
is that of negative patterning discrimination. In the version
of this discrimination problem that we have studied, animals
are rewarded with food for responding in the presence of a
light or a tone, but are not rewarded for responding if the
light and tone occur together. They readily learn to respond
quickly and consistently to either cue alone, and to withhold
responding to the compound light + tone. The rats clearly
cannot be responding on the basis of the reinforcement history of either of the two cues alone-if that were the case,
responding to the compound could never be lower than to
the individual cues-they must be using relational information to withhold response to the compound. We predicted
that rats with hippocampal damage would be unable to learn
or remember this discrimination. We repeatedly have confirmed these predictions of the configural position (Rudy and
Sutherland, 1989; Sutherland et al., 1989a; 1989b; Sutherland
and Rudy, 1989; Sutherland and McDonald, 1990). Rats with
neurotoxin-induced damage to the hippocampal formation respond as readily to the compound as to the individual elements, whether training occurs only after or both before and
after surgery. If there is a satisfactory spatial mapping account of these results, we have not heard it. For example, to
suggest that in the case of configural discriminations (and not
simple discriminations using the same cues) the relevant associations must be “embedded” in an essentially spatial representation and therefore be sensitive to hippocampal damage
is the kind of hypothesis drift that Nadel so poignantly abhors.
A second example is the transverse patterning discrimination. The problem requires the animal to visually discriminate between pairs of arms in a T-maze set within a swimming pool. On every trial the rat must choose to swim into
one of two arms; the arms can be white (W), black (B), or
striped (S). Training is divided into three phases. In phase 1
the rats receive a simultaneous choice between white and
black arms, with the white arm always containing the goal.
In phase 2, the rats continue to receive white vs. black trials
but, in addition, they receive black vs. striped trials, with the
black arm always containing the goal. In the final phase, rats
receive white vs. black trials, black vs. striped trials, and, in
addition, striped vs. white trials, with the striped arm always
containing the goal (thus, W + B - / B + S - / S + W - ) .
It is
only by the third phase that the cues are ambiguous for the
rat. In order to solve the problem through phase 3 the rat
must use the relationship between cues in the arms: prior to
that point, the rat can use simple associations involving the
cues to discriminate correctly. Damage to the hippocampal
formation disrupts acquisition and retention of the solution
to the transverse patterning problem, without disrupting the
acquisition of the simple associations at early phases of testing (Alvarado and Rudy, 1989). Again, it is difficult to come
up with a spatial mapping account of these results, but these
251
experiments were designed to test straightforward predictions of the configural position.
A third example comes from Y-maze experiments conducted on dry land. If a rat is required t o choose an arm whose
features match the features of the start arm, o r to avoid the
arm whose features match the features of the start arm, there
appears to be very little, if any, effect of damage to the hippocampal formation (Aggleton et al., 1986; Sutherland et al.,
1989b; Sutherland and McDonald, 1990). These experiments
have involved simple visual, tactile, and odor cues (obviously, if the relevant feature was spatial, the task would be
hippocampal-sensitive). If, on the other hand, the task is
modified so as to force the rat to use a nonspatial relationship
between features in start and goal arms to make correct
choices, then damage to the hippocampal formation disrupts
performance. We have modified this basic task to force a
configural solution in three different ways in separate experiments: ( I ) Rats had to choose between a black and a white
goal arm. If the start box was illuminated at the beginning of
a trial, then the white arm contained the goal: if the start box
was not illuminated, then the black arm was correct (Sutherland et al.. 1989b). (2) Rats had to choose between arms
that were black. white, or striped. If the start box contained
odor I , the rat had to avoid black, if odor 2, then avoid white,
and if odor 3, then avoid stripes (for more details see Sutherland et al., 1989b; Sutherland and McDonald, 1990). (3)
Rats had to learn a configural black vs. white discrimination
based upon time of day (Sutherland et al., l989a). In the
morning choosing the black and not the white arm was rewarded; in the evening choosing the white and not the black
arm was rewarded. In each of these Y-maze experiments the
control rats solved the relevant configural discriminations,
but in none of them did the rats with hippocampal damage
successfully discriminate.
These three examples do not provide an exhaustive list of
exceptions to the necessity for a spatial mapping requirement
in hippocampal-sensitive memory tasks, but they d o illustrate
the kind of new data that are problematic for mapping theory.
In contrast, these results fit well with a configural position.
We wish to address one final point raised by Nadel that
may illuminate a difference in a mapping treatment of place
learning vs. our configural account. Experiments specifically
designed to assess the effects of hippocampal damage on exploration have been few and far between, but we have conducted one that may be worth considering (Sutherland, 1985).
Control rats and rats with colchicine-induced damage to the
hippocampal formation were allowed to explore on a large,
circular table-top on which were placed 10 objects (e.g., cans,
bottles, plastic figures, etc.) surrounded by black curtains
upon which were hung several large “distal” cues. The rats
were always started in the center of the table, after having
sat for I minute under an opaque container that was raised
by a pulley system from outside the curtains. After the rats
had been placed on the table for many days, all of our measures of exploration (rearing, walking, object contacts, etc.)
decreased markedly to a low and stable level (habituation).
Before one subsequent session, we rotated the table (and all
of the objects on it) 180” relative to the cues on the black
curtains. According to cognitive mapping theory, the hippocampal damaged rats should not have shown a dishabitua-
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HIPPOCAMPUS VOI,. 1, NO. 3, JULY 1991
tion of exploration during the session after rotation. In fact,
both groups showed dishabituation (1.e.. both groups detected the transformation of object locations). This dishabituation occurred despite the fact that rats with the same hippocampal damage cannot learn to place navigate using the
same kind of distal cues. Although we do not hope to compel
everyone to the same conclusion as ours with these data
alone, they suggest to us that there may be a very important
difference. consistent with our account of place learning, between using cue constellations to flexibly navigate and detecting changes in cuc constellations (even if the change is a
topographical one). The existence of such a dissociation is
explicitly denied by O’Keefe and Nadel’s theory-for them
exploration and place navigation are based upon the same
mapping system. According to our position (which has clear
similarities to the account offered by McNaughton, 1989). the
critical feature of place learning situations that makes them
sensitive to hippocampal damage is the requirement that the
animal conditionally link navigational tmjectories to cue constellations, and not the spatial mapping aspect of the task.
At thisjuncture, we are also mindful of a conceptually related
dissociation described by McNaughton et al. (1989). In a single unit recording study, they showed that normal-looking
place fields with rather good specificity on an eight-arm radial
maze were present throughout the hippocampal CA 1 and CA3
subfields after extensive colchicine-induced degeneration of
the dentate gyrus granule cells. Surprisingly for a map-based
account, these same animals were clearly impaired in three
different tasks requiring place novigrlrion. We suggest that
the continued study of dissociations of this sort, between map
learning and place navigation learning, may be very profitable
in distinguishing between the cognitive mapping and configural accounts of hippocampal function.
Finally, we note that, at least within the nonprimate literature, at present there may be no compelling reasons to
doubt that the configural account may remain relegated to an
admittedly still small number of experimental exceptions to
the rule of space. It may be that in another IS years of cognitive map history the present troublesome experimental results will come to be understood as not problematic at all for
the mapping view. In many ways O’Keefe and Nadel are in
the cat-bird seat, and there is no reason why they should not
ignore the exceptions. After all, given the present situation,
it is certainly not unreasonable to believe that they may have
gotten the basic story right. However, we still hold that the
configural account is on the right path and. if it^ are right,
the number of acknowledged exceptions should multiply. In
that context, it is important that previously articulated positions hold fast and not exhibit the kind of drift that Nadel
wishes to avoid; in that way they may become the sort of
stationary beacons that mark our progress along the way.
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