Behavioral Neurosciencc Copyright 1986 by the American Psychological Association, Inc.

1986, Vol. 100, No. 2, 147-154 0735-7044/86/$(m.75

The Hippocampal Memory Indexing Theory

Timothy J. Teyler and Pascal DiScenna
Neurobiplogy Program
Northeastern Ohio Universities College of Medicine

The hippocampal formation (comprising the hippocampus proper, the dentate gyrus, and the
subiculum) has been repeatedly implicated in information storage models of the mammalian
brain. The precise nature of the hippocampal role in the storage of information has, however,
remained elusive. Here it is proposed that the role of the hippocampus is to form and retain an
index of neocortical areas activated by cxpercntial events. The hippocampal index, thus, repre-
sents those unique cortical regions activated by specific events. The neuronal mechanism
underlying the memory index is hypothesized to be long-term potentiation. It is asserted that the
reactivation of the stored hippocampal memory index will serve to also reactivate the associated
unique array of neocortical areas and thus will result in a memorial experience. This hippocampal
reactivation of a neocortical array may also be involved in establishing a cortically based memory
trace.

The neuronal mechanisms underlying information storage Specifically, it is asserted that the hippocampus maps func-
in the mammalian brain are currently unknown. In the last tional units of the neocortex and other structures. In such a
decade, the phenomenon of long-term potentiation (LTP) has conception, incoming sensory information is registered at
received intensive study due to its potential as a neuronal various cortical sensory and association areas in assemblies of
mechanism underlying information storage. LTP is an endur- cortical modules. The memory indexing theory asserts that
ing change in synaptic efficacy seen at certain monosynaptic the cortical module, a replicating structure whose detailed
junctions, primarily in limbic structures of the mammalian anatomy changes from cytoarchitectonic area to cytoarchitec-
nervous system. Several recent reviewers have considered the tonic area but whose basic plan is replicated throughout the
question of LTP as a candidate for a mnemonic device cortex (Goldman & Nauta, 1977; Szenthagothai, 1975), forms
(Swanson, Teyler, & Thompson, 1982; Teyler & DiScenna, the basis for the cortical processing of environmental infor-
1984a). Although much remains to be learned about the mation (Mountcastle, 1979). In this model, incoming envi-
neuronal mechanism underlying LTP and its distribution in ronmental information is relayed to appropriate regions of
the brain, it is currently the best candidate for a neuronal the neocortex by thalamocortical and other pathways. This
mnemonic device. initial pattern of cortical activation serves to engage the activ-
The brain region evidencing the most pronounced LTP is ities of numerous cortical modules distributed in space and
the hippocampal formation (Racine, Milgram, & Hafner, time over the surface of the neocortex.
1983) comprising the dentate gyrus, hippocampus proper, Subsequent to the receipt of information from subcortical
and subiculum (herein referred to collectively as the hippo- structures, additional processing takes place within the cortex
campus). The anatomy and physiology of the hippocampus by means of ipsilateral association and commissural fibers of
have been analyzed with respect to the topology of its afferents the cortical mantle. It is this latter form of processing that is
and efferents and with respect to the nature of neocortical utilized by the organism to form links or associations between
interactions with the hippocampus (Teyler & DiScenna, stimulus patterns and events and to assign significance or
1984b). In short, it is asserted that the hippocampus may meaning to the incoming stimulus pattern (Barlow, 1980;
represent a coordinate system or index of neocortical loci. We Pandya & Seltzer, 1982).
suggest a role for the hippocampus and neocortex in the At its simplest level, incoming experiential information is
storage and recall of information in the mammalian central processed by the appropriate thalamocortical sensory systems
nervous system (CNS). In this article we attempt to develop and is registered in a widespread but nevertheless discrete
a plausible model for information storage and retrieval in the pattern of cortical modules. The representation of experiential
brain. information is localized both in time and space in the array
of active neocortical processing modules. Subsequent to the
registration and extraction of sensory information from the
Memory Indexing Theory
neocortical registration of the experiential event, the ipsilateral
The hippocampal memory indexing theory asserts that the association and commissural associational systems of the
hippocampus stores a map of locations of other brain regions. neocortex provide interlinkages between other cortical mod-
ules. These interlinkages are hypothesized to be the neuronal
substrates for the associative connotations of an experiential
This work was supported by National Science Foundation Grant
BNS 7823947 and National Institutes of Health Grant NS 16507.
event. These and similar ideas have featured prominently in
Correspondence concerning this article should be addressed to the theories of Eccles (1979), Edelman (1979), Hebb (1949),
Timothy J. Teyler, Neurobiology Program, Northeastern Ohio Uni- Marr(1971), Olds (1969), Sherrington (1947), Squire, Cohen,
versities College of Medicine, Rootstown, Ohio 44272. and Nadel (1983), and others.

147
148 TIMOTHY J. TEYLER AND PASCAL DrSCENNA

A Neocortex

New
Memory
Formation

Hippocampus
MODULATING
INPUT
store new index

B
Recognition
Memory
associate

ft

11 recognize

SUBCORTICAL INFLUENCE

Recall
Memory

recognize index

D LEGEND

Memory Register
Failure Process
Store
Recognize
Associate

failure to recognize index

TIME

Figure 1 (see caption on facing page)

 HIPPOCAMPAL MEMORY INDEXING 149

The role of the hippocampus is to store a map or index of The initial experiential event will, by virtue of specific
those cortical modules activated by the experiential event. neocortical to hippocampal information flow, create an index
The hippocampal storage of the spatio-temporal pattern of in the hippocampal array of the pattern of neocortical
active cortical modules occurs, at least initially, through the modules activated. The hippocampal memory index will be
process of LTP occurring at hippocampal synapses by means established by the process of LTP occurring at multiple hip-
of neocorticolimbic pathways (Teyler & DiScenna, 1984b). pocampal sites, induced by activity in the neocortical-to-
For any environmental input it is assumed that a unique hippocampal pathways. Once the memory index has been
subset of thousands or millions of modules are activated established in the hippocampal array, it is subject to further
across cortical space and time. Correspondingly, the theory augmentation by repeated activation of the same neocortical-
asserts that during the memorial encoding process a similar to-hippocampal pathways. Alternatively, given no further ac-
number of hippocampal loci are activated and altered. Any tivity on those specific pathways, the hippocampal index will
given neocortical module, and thus any hippocampal index decay as a function of time, as does LTP induced by a
of that module, may participate in numerous memories. An nonrepeated tetanus in the laboratory.
analogy between the role of neocortical modules in memory If only portions of a previously indexed neocortical array
and the role of letters of the alphabet in language may clarify are activated by experience, then only that currently experi-
their role. enced portion of the stored hippocampal memory index will
be activated by the neocortical-to-hippocampal connections.
In this situation the experiential event matches only a subset
The Nature of the Engram
of the memory index. If the hippocampal activation exceeds
The hippocampal memory indexing theory suggests that some threshold level, the remainder of the hippocampal index
each experiential event is represented in a unique spatio- will be activated and will, in turn, reactivate the entire neo-
temporal array of neocortical modules. The theory asserts that cortical array. By this means, a partial experiential event,
information storage is accomplished by encoding the spatio- given that it is sufficiently complete to exceed a threshold for
temporal patterning of neocortical modules activated by ex- hippocampal memorial recognition, can be recognized as a
periential events. The initial storage of the spatio-temporal memorial event by its ability to recreate the pattern of neo-
pattern or index is accomplished in the hippocampus by the cortical modules activated by the original experiential event.
process of LTP. In the hippocampal memory indexing theory, Similarly, activation of an array of cortical modules by a
only the location and temporal sequencing of activated cor- stored hippocampal index will result in a representation of
tical modules are encoded. What is not encoded is a neuronal the original event. In behavioral terms, the former is analo-
transformation of the experiential event itself. Reactivation gous to recognition memory, whereas the latter process is
of those neocortical modules in the appropriate spatio-tem- analogous to recall memory.
poral sequence will simulate the original experience. Thus, if By such a means, the hippocampal memory indexing theory
the organism is reexposed to the original stimulus event, a can accommodate recognition and recall memory. In recog-
similar pattern of neocortical loci will be activated and will nition memory, the original stimulus event is presented again
be recognized as one previously encountered (see Figure 1). and activates an array of cortical modules similar to that it
The recognition of an experential event as a recently experi- had activated originally. The index for the array of cortical
enced one (e.g., memory) is effected by virtue of the fact that modules originally activated is stored in the hippocampus.
the spatio-temporal index stored in the hippocampus will be Reactivation of a stored hippocampal index results in a facil-
matched. itated hippocampal output and the recognition that this is an

Figure 1. A graphic depiction of the main features of the hippocampal memory indexing theory. (A:
New memory formation. Experiential information is input and registered [black dots] in multiple
neocortical loci, here shown as four discrete spatiotemporal neocortical loci. The activated neocortical
loci are registered or. indexed in the hippocampus, subject to modulatory influences acting on the
hippocampus. The new hippocampal index is stored [encircled black dots] by the process of long-term
potentiation. The activated neocortical loci are not permanently altered and abate with time [dotted
circles]. B: Recognition memory. Exposure to information previously encoded into memory activates a
set of neocortical loci and their associated hippocampal index [black dots]. The neocortical activation
of a previously encoded hippocampal index results in a facilitated hippocampal response [black dots
with sunburst], resulting in the experience of a memorial event. The recognition of a memorial event
may be associated with subcortical influences serving to integrate cognitive and visceral homeostatic
responses to the memorial event. The associative linkages between memorial events are represented by
facilitated patterns of additional neocortical loci [dotted circles, arrows, black dots]. C: Recall memory.
Exposure to a subset of information previously encoded will initially activate only a portion of the
established hippocampal index. Given activation of a suprathreshold subset of the hippocampal index,
the entire hippocampal index is activated [black dots with sunburst], which leads to the activation of
the full neocortical array [here shown as four neocortical loci]. Subsequently, facilitated intracortical
connections [dotted circles, arrows, black dots] lead to associations between the recalled event and other
events. D: Memory failure. Exposure to a subset of information insufficient to reactivate the entire
hippocampal index will be perceived as a nonmemorial event.)
150 TIMOTHY J. TEYLER AND PASCAL DiSCENNA

event that has occurred in the past. The organism thus rec- On the basis of the above, the hippocampus would appar-
ognizes the event. Whereas the recognition process is driven ently store every experiential event. Although there are some
by external stimuli that create a pattern on the cortex that is researchers who believe that all experiences are stored in the
then recognized by the hippocampus, in recall the hippocam- CNS, there are reasons to believe that experiential events are
pus is able to activate an array of cortical modules in the modulated in their importance, to affect either their storage
appropriate spatio-temporal sequence to bring about a recol- efficacy or their retrieval efficacy; that is, memory storage or
lection of the experiential event. retrieval is a graded process that can be modulated by other
Another way of viewing the hippocampal memory indexing agents or processes. It has been shown that hippocampal
model is to consider that in this model the hippocampus is activity is capable of being modulated by numerous agents,
continually and automatically testing each pattern of cortical including circadian influences (Harris & Teyler, 1983), neu-
activation to determine whether it matches patterns that have roendocrine effects (Reiheld, Teyler, & Vardaris, 1984; Teyler,
been stored in the hippocampus. If a match is achieved, either Vardaris, Lewis, & Rawitch, 1980), norepinephrine (Bliss,
identically or partially, then this means that a previously Goddard, & Riives, 1983), and biogenic amine levels (Gold,
experienced (memorial) event is again impinging on the or- Delanoy, & Merrin, 1984). The theory postulates that the
ganism. The hippocampus thus "tests" every pattern of neo- encoding of the cortical array in the hippocampal index is
cortical activation with respect to its history to the organism. capable of being modulated by these and presumably by other
The repeated registration of a previously experienced event unknown modulators. It is hypothesized that the biological
acts to reinforce or strengthen the hippocampal index of the consequences of the experiential event are capable of activat-
cortical array associated with that experiential event. ing the neuromodulatory system(s) that influences the rate of
Older memories may utilize an extension of this indexing permanence of LTP and its sequelae in the hippocampus.
process involving cortical mechanisms. The hippocampal Such processes may also affect any alteration of neocortical
memory index is hypothesized to be an active process, pro- processes involved in auto-indexing.
viding feedback to the neocortex and elsewhere regarding the
One of the current views of hippocampal functioning is
memorial saliency of patterns of neocortical activity. If a
that the hippocampus occupies a critical location mediating
pattern of neocortical activation that has been previously
information transfer between the neocortex and subcortical
experienced, and a hippocampal memory index thus estab-
structures (Swanson et al., 1982; Teyler & DiScenna, 1984b).
lished, is repeated, the neocortical-to-hippocampal pathways
Although the main thrust of the hippocampal memory index-
will impinge upon a previously potentiated array of hippo-
ing theory is the link between neocortical modules and the
campal loci. The result of this will be a facilitated hippocampal
hippocampus, it must not be overlooked that the extensive
response to this pattern of neocortical input. The facilitated
subcortical connectivity of the hippocampus also plays a role
hippocampal output will provide feedback to the neocortex
in memory modulation. We propose that the subcortical
that the pattern of neocortical activation currently being
connectivity of the hippocampus functions to integrate the
processed has occurred previously—that is, it is a memorial
homeostatic, affective, and visceral aspects of an organism's
event. The facilitated hippocampal output may also influence
response to a recalled event. Many memorial events have an
nonspecific cortical and subcortical regions to direct the or-
emotional component or have requirements for the organism
ganism's attention to this relevant experiential event. If the
to take some sort of action. In both of these cases, the
experience fails to duplicate the earlier pattern of neocortical
organism not only must prepare its cognitive and motor
activation, the event will not be recognized as a memorial
systems to interpret and react appropriately to environmental
event.
Evidence from human studies supports the idea (a) that the events but must be prepared to take homeostatic action with
hippocampus is not necessary for retrieval of older memories regard to the encoded event. It is suggested that the extensive
(Scoville & Milner, 1957) and (b) that there exists a neocortical subcortical connections that the hippocampus displays enable
mnemonic process that "takes over" from the hippocampus this homeostatic response to a recalled event to occur.
over an extremely long (3-year) time course (Squire et al., The topographic organization of the hippocampus (as re-
1984). Although a neurobiological process with such an ex- viewed by Teyler & DiScenna, 1984b) is amenable to regis-
tended time course has not been described and there is little tering the spatio-temporal sequencing of cortical modules
support from animal experiments for this concept (Harley, activated by an experiential event. The hippocampus can be
1979), it is nevertheless possible that the continual reactiva- thought of as a four-dimensional map in which several or-
tion of a particular hippocampal index would have a slowly thogonal dimensions can be displayed. The theory requires
incrementing effect on the cortical circuitry it indexes. If this the hippocampal representation of the topography of the
is the case, the hippocampal index would, with time, become neocortex. The nature of the map is at present not known,
redundant and result in the ability of the cortex alone to although evidence is accumulating (see Teyler & DiScenna,
match to the pattern of experientially activated cortical mod- 1984b). One possibility is that there is a simple one-to-one
ules. Such an "auto-indexing" mechanism might be affected isomorphic topographic representation between neocortical
by the frequency of indexing, such that an often reaccessed and hippocampal loci. Alternatively, however, it could be that
index would become cortically based at a faster rate than one a given cortical module might be represented in multiple
rarely indexed. However, until this interesting idea receives hippocampal loci. Similarly, a single hippocampal location
more direct support from the animal literature, it must remain might index multiple neocortical loci. Although technically
speculative. difficult, these relations can be empirically determined.
 HIPPOCAMPAL MEMORY INDEXING 151

Although it is not currently possible to do more than and that laboratory animals are capable of abstract learning
speculate regarding the detailed topological relations between (Fountain, Henne, & Hulse, 1984; Hulse, 1978; Hulse &
the hippocampus and neocortex, the essence of the model can O'Leary, 1982). Laboratory experiments have shown that
be stated simply: The output of the hippocampus is able to neocortical tissue or neocortical associations are not required
topographically reaccess the neocortical modules whose activ- for the solution for many of the standard laboratory problems
ity was initially impressed onto the hippocampus. that are utilized to study the neuronal mechanisms underlying
learning and memory (Norman, Buchwald, & Villablanca,
Associative Information Encoding 1977; O'Keefe & Nadel, 1978). There are instances in which
neocortical and hippocampal lesions or destruction of thala-
The hippocampal memory indexing theory specifies that mocortical fibers has been shown to have minimal effect on
the spatio-temporal patterning of neocortical modules acti- the acquisition of a variety of standard laboratory learning
vated by an experiential event is initially stored in the hip- tasks (Chow, 1967; Moore, Yeo, Oakley, & Russell, 1980;
pocampus by LTP. The theory proposes that only the initial Oakley & Russell, 1975, 1977; O'Keefe & Nadel, 1978).
experiential event is stored in the hippocampus. How, then, However, if the learning task is made more difficult, lesions
can this theory accommodate learned associations between that were ineffective in disrupting simpler learning tasks are
experiential events? now effective (Eichenbaum, Potter, Papsdorf, & Butter, 1974;
The hippocampal memory indexing theory asserts that such Kesner & Novak, 1982). Therefore, we argue that the critical
associations are stored by intracortical associational systems. nature of the cortical contribution to the animal's behavior
These intracortical associational systems include the ipsilat- has not been tapped in these simpler situations.
eral associational systems that serve to interrelate areas on the Because the hippocampal memory indexing theory features
ipsilateral cortex, and the commissural connectives that serve the interaction of neocortical analyzers and hippocampal
primarily to interrelate homologous hemispheric regions. It storage, it would be expected that dysfunction of either hip-
has recently been shown by Wilson and Racine (1983) that pocampus or neocortex would impair performance on suffi-
the commissural associational connectives exhibit LTP. ciently demanding behavioral problems. A bilateral lesion of
Therefore, it is proposed that the associations that are formed dorsal hippocampus does not affect simple rabbit nictitating
from the initial experiential event are mediated by LTP membrane conditioning (short-delay classical conditioning;
occurring between cortical modules. In this respect, the theory Solomon, 1977, 1980) but impairs performance in more
ascribes associative linkages to neocortical processing. The demanding situations (long-trace classical conditioning;
role of the hippocampus is to store only the event, not the Weisz, Solomon, & Thompson, 1980). Hippocampal lesions
myriad of associations an event may elicit. The question of are also quite devastating to more complex tasks involving
the ability of thalamocortical pathways to exhibit LTP is, at discrimination reversals (Orr & Berger, 1981) and other higher
present, unresolved. Lee (1982) reported that stimulation of order processes (Kettner, Clark, Berry, & Thompson, 1981).
while matter resulted in LTP recorded from intermediate Neocortical destruction does not interfere with the acquistion
layers of the neocortical slice. However, Komatsu, Toyama, of a simple classically conditioned rabbit nicitating membrane
Maeda, and Sakaguchi (1981), and we ourselves (Teyler & response (Moore et al., 1980; Oakley & Russell, 1975, 1977).
Chiaia, 1984) were unable to observe thalamocortical LTP in We know of no data with respect to neocortical lesions under
adult animals. Lee stimulated subjacent white matter and more stringent rabbit nictitating membrane conditioning par-
may have involved associational systems in the response he adigms, although the evidence from other behavioral para-
recorded. Associational systems have been shown to exhibit digms supports the contention that neocortical systems are
LTP (Wilson & Racine, 1983). This important question essential only when the task demands are greater (Chow, 1967;
clearly deserves more attention. O'Keefe & Nadel, 1978; Squire et al., 1983). These data
The memory indexing theory suggests that experiential support the contention that there may be different, perhaps
events themselves are not initially stored in cortical locations overlapping, neuronal substrates for different tasks (Chow,
but that the index of cortical locations is maintained in the 1967; Thompson, 1983; Weingartncr, Grafman, Boutelle,
hippocampus. Furthermore, the associations between exper- Kaye, & Martin, 1983).
iential events—the multiple linkages available to the human
brain—are stored not primarily by intrahippocampal linkages The Hippocampus as a Cognitive Map
but rather by means of the rich interrelations extant between
cortical modules that communicate via associational fiber O'Keefe and Nadel (1978, 1979) proposed that the hippo-
systems. Therefore, we have a dichotomy wherein the associ- campus operates as a device for constructing and storing
ational linkages between experiential events are stored at the cognitive maps—"representations which capture the spatial
cortical level and the event itself is represented in the hippo- layout of an animal's experienced environment" (O'Keefe &
campus by means of the hippocampal index. Nadel, 1979, p. 494). They considered the evidence from
single-unit studies of animals operating in a spatial environ-
Neocortico-Limbic Interactions ment and the effects of lesions on spatial behavior. An im-
portant alternative theory of hippocampal function is the
It can be argued that many of the learning and memory working memory theory developed by Olton and co-workers
tasks commonly employed in the laboratory do not make (Becker & Olton, 1982; Olton, Becker, &Handelmann, 1980).
very strong demands on the associative abilities of the animal In this conceptualization the primary function of the hippo-
152 TIMOTHY J. TEYLER AND PASCAL DiSCENNA

campus "is to form the temporal/personal associations needed Consequently, it is not necessary that there exist a single
for accurate working memory" (Walker & Olton, 1984, p.240). point-to-point representation, as is the rule in sensory systems.
The hippocampal memory indexing theory does not con- This aspect of the model is amenable to study with the use of
tradict the theory proposed by O'Keefe and Nadel. Virtually contemporary anatomical tracing techniques such as horse-
all the features of O'Keefe and Nadel's model can be accom- radish peroxidase histochemistry (Wilhite & Teyler, 1985) as
modated by the hippocampal memory indexing theory. In well as the spatially less specific techniques of 2-deoxy-D-
essence, O'Keefe and Nadcl proposed that the hippocampus glucose autoradiography (Teyler & DiScenna, 1984b). As a
is a map of the spatial or cognitive world. The hippocampal cautionary note, if the hippocampal representation of a cor-
memory indexing theory asserts that the hippocampus is tical module is confirmed to a limited extent of the dendritic
indeed a map, but not a direct transform of the spatial zone of a few hippocampal cells, the demonstration of topol-
environment of the organism. Rather the hippocampal mem- ogy at the level of individual neocortical modules will be
ory indexing theory maintains that the hippocampus repre- difficult with present techniques. Given more specific infor-
sents a transform of the cortical space of the organism, on mation about the topological relations between the two struc-
which is represented Euclidean and cognitive space as well. tures, electrophysiological stimulation and recording will be
The hippocampal memory indexing theory asserts that necessary to describe the nature of the neural interaction
learned associations between experiential events are stored by between these regions.
intracortical association systems interacting with the hippo- 3. The hippocampal indexing theory asserts that cortical
campal memory index. Thus the neurobiological require- activation by experiential events can induce LTP in corre-
ments of Olton's working memory theory may be partially sponding hippocampal loci. It follows that activation of se-
satisifed by the features of this model. lected cortical regions by other means (electrical, chemical)
should similarly result in discrete patterns of hippocampal
Predictions LTP. Although this question has received little experimental
study, it has been reported that tetanization of the claustrum
Several predictions that are testable with current techniques leads to LTP in the hippocampus (Wilhite, Teyler, & Hen-
follow from a consideration of the memory indexing theory. dricks, in press). The theory suggests that the plastic properties
Limiting consideration to the hippocampal-neocortical as- of the hippocampal-neocortical connection are such that LTP
pects of the model, these predictions are the following. will not result from brief episodes of hippocampal activity.
1. A functional relation exists between hippocampus and More prolonged forms of hippocampal activity, spanning
neocortex. Although considerable literature exists document- longer time frames and perhaps coupled with other neuro-
ing anatomical neocortical-limbic and hippocampal connec- modulatory activity, are required to alter the cortical module
tivity (see Teyler & DiScenna, 1984b, for a review), much as a result of hippocampal activity.
remains to be elucidated with respect to the functional aspects 4. Given the hypothesized interrelation between hippo-
of neocortical-hippocampal connections. Anatomical studies campus and neocortex, it is predicted that equivalent forms
have demonstrated that several parallel multisynaptic routes of impairment should result from appropriate hippocampal
(via claustrum, cingulum, perirhinal cortex) exist between and neocortical lesions. The demonstration of such equiva-
neocortex and hippocampus, many of which also possess lencies depends upon the inactivation of topologically equiv-
reciprocal hippocampal-neocortical projections. Other, more alent projection areas in the two structures and upon the
direct (monosynaptic) pathways have been demonstrated be- selection of behavioral tasks that require neocortical process-
tween neocortex and hippocampus (Swanson, 1981; Wilhite ing for their successful execution. It is clear that experiments
& Teyler, 1985). The functional nature and importance of directed specifically at this question are needed to test this
most of these pathways have received little study to date. The prediction.
indexing theory requires a two-way conversation between 5. Pretrial electrical stimulation of neocortical regions, suf-
neocortex and hippocampus which must be demonstrable by ficient to induce localized hippocampal LTP, should interact
anatomy and physiology. with behavioral learning processes in a manner similar to that
2. The model requires a topological representation of neo- shown for stimulation of hippocampus alone (see Teyler &
cortical modules in the hippocampus; therefore, the nature of DiScenna, 1984a, for review).
the functional connectivity between the regions must preserve
topography. Although there is some evidence for preserved Conclusions
topography in several of the neocortical-hippocampal systems
(see Teyler & DiScenna, 1984b), the level of topographic This article presents a theoretical account of how the hip-
specificity and resolution required has not yet been addressed. pocampus, LTP, and neocortex may interact in memory
Because the model asserts a high degree of specificity (to the functions of the mammalian brain. The hippocampal mem-
level of the neocortical module) between neocortex and hip- ory indexing theory asserts that the hippocampus stores an
pocampus, we predict that the functional activation of regions index of recently activated cortical loci by the mechanism of
of the neocortex would result in topologically specific patterns LTP. This stored hippocampal index permits the operation
of activation in the hippocampus. Similarly, activation of of recognition and recall memory through its subsequent
discrete hippocampal loci would be associated with activation interaction with the neocortex.
of specific neocortical modules. The hippocampal indexing theory makes a number of
The theory does not specify the nature of the topological specific predictions. There must exist a neocortical-to-hippo-
representation but merely asserts that a representation exists. campal topological specificity of connections. The theory
 HIPPOCAMPAL MEMORY INDEXING 153

demands that an enduring representation of neocortical activ- Teaching an alphabet to rats. Journal of Experimental Psychology:
ity be impressed on the hippocampus in the form of LTP. Animal Behavior Processes, 8, 260-273.
The theory predicts similarities between hippocampal and Kesner, R. P., & Novak, J. M. (1982). Serial position curve in rats:
neocortical damage, inasmuch as the two structures are hy- Role of the dorsal hippocampus. Science, 218, 174-175.
Kettner, R. E., Clark, G. A., Berry, S. D., & Thompson, R. F. (1981).
pothesized to work in a cooperative manner.
Hippocampal, medial scptal and entorhinal responses during au-
If the hippocampus is storing an index of cortical modules
ditory signal detection behavior in the rabbit. Society for Neurosci-
activated by experiential events and is doing so over periods
ence Abstracts, 7, 358.
of time, one must resolve the question of the permanence of Komatsu, Y., Toyama, K., Maeda,;., & Sakaguchi, H. (1981). Long-
LTP. Present evidence suggests that the half-time decay of term potentiation investigated in a slice preparation of striate cortex
long-term potentiation is something less than 2 weeks. We in young kittens. Neuroscience Letters, 26, 269-274.
must then be prepared to search for phenomena capable of Lee, K. S. (1982). Sustained enhancement of evoked potentials fol-
storing information for long periods of time. Hippocampal lowing brief, high frequency stimulation of the cerebral cortex in
LTP and hippocampal memory indexing may be only the vitro. Brain Research, 239, 617-623.
instigating events for these phenomena of unknown mech- Marr, D. (1971). Simple memory: A theory for archicortex. Philo-
sophical Transactions of the Royal Society London, Series B, 262,
anism.
23-81.
Moore, J. W., Yeo, C. H., Oakley, D. A., & Russell, I. S. (1980).
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Correction to DeVietti et al.

In the article "Previous Experience Disrupts Atropine-Induced Stereotyped 'Trapping*

in Rats" by Terry L. DeVietti, Sergio M. Pellis, Vivien C. Pellis, and Philip Teitelbaum
(Behavioral Neurosdence, 1985, Vol. 99, No. 6, pp. 1128-1141), three lines were
erroneously repeated. In the first paragraph on p. 1138, the third sentence should read
as follows: Further, at the high doses that result in stereotypic trapping there are
reliable changes in both cortical and hippocampal activity (Schallert et al., 1980;
Shoham, Chen, DeVietti, & Teitelbaum, 1985; Vanderwolf, 1975).