Behavioural Brain Research 110 (2000) 97–108
The hippocampus and contextual memory retrieval in Pavlovian
conditioning
Stephen Maren *, William Holt
Department of Psychology and Neuroscience Program, Uni6ersity of Michigan,
525
E. Uni6ersity A6enue, Ann Arbor, MI
48109
-
1109
, USA
Accepted 25 November 1999
Abstract
Several theories of hippocampal function have suggested a role for the hippocampus in contextual memory retrieval. However,
these theories are based on studies using permanent pretraining lesions, which confound the role of the hippocampus in learning
with its role in retrieval. We argue that an alternative methodology is required to assess the role of the hippocampus in memory
retrieval processes. This alternative methodology involves temporary inactivation of the hippocampus in Pavlovian paradigms that
lend themselves to an examination of retrieval. An example of this approach is considered in a Pavlovian fear-conditioning
paradigm. We examined the influence of hippocampal inactivation on the context-specific expression of latent inhibition, a
response decrement displayed when excitatory conditioning is preceded by non-reinforced presentations of a to-be-conditioned
stimulus. Reversible inactivation of the dorsal hippocampus prior to retrieval testing eliminated the context-specific expression of
latent inhibition. The nature of the hippocampal role in retrieval processes is discussed in the light of these data. © 2000 Elsevier
Science B.V. All rights reserved.
Keywords
:
Hippocampus; Context; Muscimol; Retrieval; Fear; Interference; Latent inhibition; Freezing
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1. Introduction
It has been recognized for decades that the expres-
sion of memory depends importantly on the context in
which memory is retrieved [69]. For instance, it has
been established that memory retrieval is facilitated to
the degree that the context of memory retrieval is
similar to the context of learning [68]. In many ways,
our own day-to-day experiences reinforce this notion.
For example, we all know that it is generally much
easier to remember the name of a person that you meet
while dining at a luxurious restaurant if you re-encoun-
ter that individual at the restaurant, as opposed to at
the neighborhood grocery. Indeed, it is common to
suffer memory lapses when people, places, or things are
experienced ‘out of context’. This process by which
context facilitates memory retrieval is termed contextual
memory retrie6al. Contextual memory retrieval operates
on many forms of learning and memory, including
complex declarative memory in humans (as illustrated
above) and simple forms of learning and memory in
animals, including Pavlovian conditioning [4,5]. The
present review will focus on the latter form of learning
and memory.
Recent work in Pavlovian conditioning paradigms
has demonstrated that environmental stimuli not only
elicit learned behavioral responses (as in the sound of a
metronome eliciting salivation), but also serve as the set
of conditions under which certain associative contin-
gencies are valid [68]. A process called occasion setting
demonstrates this latter phenomenon [6,54,61]. For ex-
ample, in a serial feature-positive discrimination (a
form of positi6e occasion setting), a ‘feature’ stimulus,
such as a tone, precedes a ‘target’ stimulus (the condi-
tional stimulus or CS), such as a light, only when the
target signals an unconditional stimulus (US), such as
food or electric shock. Importantly, the feature is not
presented on trials in which the US does not follow the
target. Hence, the presence or absence of the feature-
* Corresponding author. Tel.: + 1-734-9366532; fax: + 1-734-
7637480.
E-mail address
:
maren@umich.edu (S. Maren)
0166-4328/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved.
PII: S0166-4328(99)00188-6