-~
HIPPOCAMPUS,
The Theory That Wouldn’t Die: A
Critical Look at the Spatial Mapping
Theory of Hippocampal Function
VOL. 1, NO. 3, PAGES 265-268, JULY 1991
democratic fashion. Even a single counterexample should be
cause for rejection of a theory if it cannot be adequately explained. If the spatial nature of a given task succeeds in determining whether hippocampal disruption will influence
learning only some (or most or even almost all) of the time,
then it is not appropriate to ignore the counterexamples and
make sweeping generalizations. Rather. a new empirical generalization is needed-one that explains why, and the circumstances under which, the behavioral outcome varies.
Neal J. Cohen” and Howard Eichenbaumi
* B e c k m a n Institute and D e p a r t m e n t of Psychology,
University of Illinois at U r b a n a - C h a m p a i g n , U r b a n a ,
1L 61801 U.S.A. and +Department of Biological
Sciences, Wellesley College, Wellesley, MA U . S . A .
“Exceptions” in the rodent literature
In this brief paper we consider the spatial mapping theory
of hippocampal function offered by O’Keefe and Nadel(1978)
and revisited by Nadel in this issue, taking into account developments since 1978 relevant to evaluation of the theory.
We assess its ability to account for the phenomenology of
spared vs. impaired memory capacity following hippocampal
damage, and we conclude that it provides a successful account of only a limited domain of data. We suggest that a
broader view is required in which memory for spatial relations
is but a subset of the domain of memory (specifically, declarative memory), for which the hippocampal system plays
a critical role. At the conclusion of this paper, we also try to
make sense of the phenomenon of the spatial mapping theory-why, despite strong evidence of its inadequacies, the
spatial mapping hypothesis is a theory that refuses to die.
THE BEHAVIORAL DATA
The major claim of the spatial mapping theory with regard
to behavioral data is that “it is the spatial nature of a given
task that determines whether o r not hippocampal disruption
will influence learning” (Nadel, 1991). Considering the literature on hippocampal lesions in rodents, O’Keefe and
Nadel conclude that their theory “successfully handled the
vast preponderance” of the data, that it has been supported
“with a small number of exceptions,” and that it has “generally been supported” (Nadel, 1991). Accordingly, there are
agreat number of studies that can be, and are, cited in support
of the spatial mapping theory. However, there are real problems here. What about the “exceptions” in the rodent literature? Also, if the rodent literature provides the best case
for the spatial mapping theory, what about the human and
nonhuman primate literatures? Moreover, what about a
broader formulation in which the “exceptions” and the other
literatures can be accommodated?
“Exceptions” and the use of psychoarithmetic
in science
Arguing in favor of the spatial mapping theory because it
provides an account of most of the data is tantamount to
employing a rule of psychoarithmetic to judge the adequacy
of theories. It is apparently an attempt to let democratic principles determine which theories to support: majority rules.
Unlike politics, however, science does not proceed in purely
What of the “exceptions” that are summarily dismissed by
Nadel without discussion’? Although there is no shortage of
examples that could be chosen from the pre- or post-1978
literatures (Eichenbaum et al., 1990b). we shall limit ourselves here to our own recent work. In two sets of experiments, involving either spatial learning o r olfactory discrimination learning, respectively, we manipulated the memory
processing demands so as to encourage or hinder certain
types of processing on the identical stimulus materials, and
we included probe tests to assess the flexibility of the memory
representations acquired. Disconnection of the hippocampus
by fornix transection caused either severely impaired or intact learning capacity determined not by the spafiul processing demands, but rather by the representational demands
employed, across different trials with the identical (odor or
place) stimulus materials. Regardless of whether the task involved spatial information or olfactory information, learning
was impaired when the task requirements encouraged comparisons among multiple cues and a memory representation
based on significant relations among them; learning capacity
was spared when the task requirements hindered or eliminated the need for comparing cues and, instead. encouraged
approach responses to individual cues. For both the spatial
and the olfactory paradigms, animals with hippocampal system damage differed from intact animals by being unable to
use their memories flexibly: they could demonstrate learning
only in situations constituting repetitions of the learning
event.
In our studies of olfactory discrimination learning (Eichenbaum et al., 1988; 1989), we found rats with fornix transections to be severely impaired when odor cues were presented simultaneously, encouraging comparisons between
cue and response alternatives. In contrast, when the same
discriminative stimuli were presented separately, from the
same sites within the same apparatus, but the response requirement was t o complete o r discontinue a single behavioral
act, thus hindering a representation based on relations between cues, rats with fornix transections learned as rapidly
as o r more rapidly than intact animals. When we challenged
animals to use their acquired knowledge about familiar odors
in novel discrimination problems composed of stimuli taken
from previous problems and presented “mispaired” on probe
trials (Eichenbaum et al., 1989), we found a marked difference between rats with fornix transections and intact animals
in the flexibility of the representations. Normal rats sampled
each odor in a discrimination problem and readily performed
discriminations of familiar odor cues presented in novel pairings, whereas rats with fornix transections inflexibly sampled
the multiple odors presented on each trial as a compound
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HIPPOCAMPUS VOL. 1, NO. 3, JULY 1991
stimulus and failed to make use of their knowledge of the
familiar odors when presented in novel pairings.
With regard to place learning, one of the most sensitive
assessments of hippocampal system damage involves the
Morris water maze. Rats learn to swim to the locus of an
invisible escape platform from various starting positions,
guided solely by distal visual (place) cues. Under these training conditions. rats with hippocampal-system damage demonstrate a severe and lasting impairment: conversely, when
the platform is made visible, providing a distinct taxon contiguous with the escape reinforcement. no deficit is observed
(Morris et al., 1982). Success o r failure on maze learning has
generally been attributed to place vs. taxon cues available to
guide performance in accordance with the O’Keefe and Nadel
hypothesis. However, Eichenbaum et al. (1990a) found that
rats with fornix transection either performed the response as
well as intact rats or failed completely in different versions
of the task guided by the identical distal visual (place) cues.
Rats with fornix transection failed when they were required
to start trials from a variable position in the maze, but learned
to locate the escape site rapidly when started from a constant
position. Thus, guided by the same sensory information, impairment o r spared learning was observed depending on the
demand for representing the relations among the varying visual perspectives associated with different swim trajectories.
In probe trials in which trained rats were required to find
the platform from novel start loci, intact rats consistently reoriented their swim trajectory toward the escape site. thereby
demonstrating the flexibility of their representation-the
ability to be expressed in novel test situations. In contrast,
rats with fornix transections required considerably longer periods to find the escape platform when required to begin from
novel start locations. They had difficulty from a variety of
novel starting points, including those from opposite directions, in which the most salient distal cues were near or far
from the start locus but, within the same series of trials. could
reliably reproduce near-perfect swim tra.jectories when the
conditions were identical to those used during training.
Despite major differences in the modalities of the cues,
responses, and motivations guiding performance in these two
paradigms. irnd in it~lietliero r not sptrrirrl procx~ssirigor pliice
lecirning pltrycd (in? role iti giriditig pe~forrntrnce,the behavioral outcome of hippocampal-system damage in both paradigms was determined by the extent to which performance
depended upon storing of the relationships among multiple
stimuli and flexible expression of memories.
Human and nonhuman primate literature
The spatial mapping theory was never able to accommodate the human amnesia literature without appeal either to
the “special pleading” that O’Keefe and Nadel correctly disdain, or to movement toward a more abstract construal of
their theory (cognitive mapping rather than just spatial mapping), in contradiction to the claim “We were referring to
space, and we meant space, not abstractly, but concretely
(Nadel. 1991). It has always been clear that human amnesia
cannot be construed as being limited to the spatial domain.
Nothing that has happened since 1978 helps their cause in
this regard. Accordingly, Nadel agrees to “toss in the towel”
and to admit that “at least in the case of the human hippo-
campal system. there is more than spatial mapping going o n ”
(Nadel, 1991).
Unfortunately, the situation seems little more promising in
the nonhuman primate literature. Recent years have seen reports of sparing and impairment in monkeys with hippocampal-system damage that parallel directly the pattern seen in
human amnesia (Zola-Morgan and Squire, 1985). Too, it has
become increasingly cleat- that monkeys with hippocampalsystem damage demonstrate either impaired or intact learning
with identical visual materials in the same apparatus when
the representational demands are varied, such as when the
task requires object discrimination learning as opposed to object recognition memory (in the delayed nonmatch-to-sample
[DNMS] task) (Gaffan, 1974: Zola-Morgan and Squire, 1985).
(Note that the notion that this task i s any less ecologically
valid for monkeys than running on elevated mazes in laboratories is for rats is too absurd for further comment.) In this
manner, the data parallel closely the “exceptions” from the
rodent literature, discussed just above. Indeed. in a study
strikingly parallel to our probe test study involving novel repairings of familiar odors (Eichenbaum et al., 1989), monkeys
with hippocampal-system damage initially trained to discriminate ob-ject-pairs were later impaired in recognizing the objects when they were presented separately (Saunders and
Weiskrantz. 1989).
EXPLORING A MORE ABSTRACT ACCOUNT:
COVERGENCE FROM DIFFERENT SOURCES OF
EVIDENCE
In our view, what determines whether performance on a
particular task will be impaired or spared after hippocampalsystem damage. regardless of the species of animal. is the
extent to which successful performance requires either ( I )
the comparison among stimuli presented either simultaneously, such as in place or sensory discrimination, o r sequentially, such as in working memory and delayed nonmatching
tasks (i.e.. in configurational o r temporal relations). and/or
(2) the expression of acquired representations flexibly, in
novel contexts. for example, by making a response inconsistent with thc behavior performed during acquisition of the
material, as in the working memory and D N M S tasks, o r by
demonstrating successful performance in the novel probe
tasks .
The theory behind this empirical generalization (Cohen and
Eichenbaum. unpublished observations: see Eichenbaum et
al.. 1990b. for our most recent elaboration of this view) is
that the hippocampal system plays a critical role in declarative memory, the system responsible tor the accumulation
of facts and data derived from learning experiences. This system stores the outcomes of processing by the (neocortical
sensory and limbic) modules that feed the hippocampal system. These stored outcomes of processing experiences are
represented within highly interconnected networks, with connections among informational elements forming multidimensional spaces characterizing possible relations. In this way,
declarative memory subserves a peculiarly relational form of
representation. This relational property of declarative memory in turn gives rise to the critical property of representational flexibility. That is, the full interconnectedness of such
SPATIAL MAPPING THEORY OF HIPPOCAMPAL FUNCTION / Cohen and Eichenbaum
a representational system produces the ability of information
to be activated regardless of the current context.
On this view, spatial mapping is but an example, o r a special case-albeit, for the rat at least, a particularly good
one-of the relational memory function of the hippocampal
system. Hence, it can offer an account of the exclusively
spatial data, as well as the “exceptions.” Here, the theory
is about the memory space supported by the hippocampal
system, rather than spatial memory.
We must stress that this account is supported by the convergence of data from rat, monkey, and human amnesia literature, as well as from physiological data-just the sort of
convergence among different types of data to which Nadel
aspires. With respect to electrophysiological data, studies reported subsequent to the compelling finding of place cells in
the hippocampus (cells showing preferential firing when the
animal was located in one o r another place in the environment), have found that the location of the animal was, at
most, only one variable necessary to predict the firing of these
cells; it was not sufficient, alone, to predict firing in any of
them. Thus, there are several reports of hippocampal neurons
that are activated selectively in relation to specific conjunctions of cues in several learning paradigms and species: some
cells are specifically active in relation to conjunctions of goal
box color and position in a spatial delayed response task in
rats (Wible et al., 1986). to conjunctions of odors and their
presentation position in rats performing our simultaneous
odor discrimination task (Wiener et al., 1989), and to conjunctions of two-dimensional patterns and their spatial or
temporal positions in visual recognition and delayed response
tasks in monkeys (Watanabe and Niki, 1985; Rolls et al.,
1989). In addition, there are descriptions of cells whose activity depends critically on variables that have no spatial component: the responses of these hippocampal neurons were
determined by both current and previous stimulus valence in
our successive odor discrimination task (Eichenbaum et al..
1986) and in an auditory discrimination task (Foster et al.,
1987). Most significant, perhaps, is that some of the same
cells that fire in relation to odor configurations in an olfactory
discrimination task have distinct and unrelated place fields
when rats perform a spatial navigation task in the identical
environment (Wiener et al., 1989). These findings indicate
that the hippocampus processes whatever critical relations
among cues and events it finds in the environment (Eichenbaum and Cohen, 1988), and is no more restricted to coding
of spatial relations than the behavioral impairment JblloMJing
hippocampal system damage is restricted to spatial learning.
Nadel makes some noises of being interested in moving in
this direction-of embracing a more abstract frameworkwhen he claims that their proposed locale and taxon systems
were intended as “corresponding roughly to the notions of
‘knowing that’ and ‘knowing how’ described by Ryle. But
nowhere in the original book, o r in Nadel’s current revisiting,
is this correspondence cashed out. This is too bad, as Ryle’s
distinction has a clear place in the declarative-procedural
framework that we offer. But, then, if they had cashed it out,
it would directly contradict his insistence that “We were referring to space, and we meant space, not abstractly, but concretely” (Nadel, 1991).
”
267
W H Y DOES THE SPATIAL MAPPING THEORY
REFUSE TO DIE?
Having shown that the spatial mapping theory can only be
viewed as a limited-domain account, providing an explanation for only a subset of the relevant data regarding hippocampus and memory. how d o we understand its continuing
appeal? This clearly could be the topic for another full paper:
we will, however, limit ourselves here to three brief thoughts.
First, the finding of place cells was among the most compelling examples ever reported of a behavioral correlate of
brain activity. The fact that both electrophysiology and the
lesion work show that hippocampal neurons are interested in
other relationships among stimuli in addition to spatial relationships hasn’t seemed to dampen enthusiasm for the original description. Second, space is so pervasive in both laboratory tasks and real-world functioning. particularly in the
rat, that it is difficult to ignore in theory development o r test
construction. ‘Third, limited-domain accounts have the appeal
of providing an explanation of (their limited domain of) phenomena in language that is very clearly and closely tied to
the data: predictions are easy to make within the restricted
domain. Broader theories that aspire to account for a wider
range of performances, across various paradigms and species
(the approach for which we argue), must necessarily be stated
in terms further removed from and less simply connected to
any particular datum. Nonetheless, it is in the direction of a
more comprehensive account that the data seem to point, and
the field seems to b e moving. Such a view should dis-place
the spatial mapping hypothesis.
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