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Mark A. Wheeler
Perhaps the most remarkable achievement of human memory is the ability
to think back and relive happenings from the past. In response to such a
simple cue as, say, high school graduation night, it is possible to
mentally transport oneself back many years or decades and to reexperience
parts of life that probably have not been considered in a long time. The
type of memory that allows people to reect upon personal experiences is
called episodic memory (Tulving, 1983, 1993).
Psychological writing on the topic of episodic memory began at least as
early as William James (1890). Because James's work was pioneering, he
had the opportunity to select and dene those psychological phenomena
that he considered to be important for the developing eld. It is interesting
to note the way that he dened memory. James took a much more
restrictive denition than do most contemporary researchers. Rather than
consider memory as encompassing such acts as motor learning, habit
formation, stimulus-response strengthening, and the acquisition and use of
knowledge, the concept to James was equivalent to what is now called
episodic memory. (These other phenomena, motor learning, etc., were all
readily apparent to James, and he devoted much discussion to them, but
they were not labeled as memory phenomena.) The conscious recollection
that accompanied memory retrieval was taken as the dening
characteristic of memory. Memory requires more than the mere dating of a
fact in the past. It must be dated in my past I must think that I directly
experienced its occurrence (p. 612).
Episodic memory also is dened by the nature of conscious awareness that
accompanies retrieval, a type of awareness now called autonoetic (self-
knowing) awareness. The retrieval of episodic information, such as the
recollection of a particular time that one drove one's rst automobile, is not
merely an objective account of what has happened or what has been seen
or heard. Its contents are infused with the idiosyncratic perspectives,
emotions, and thoughts of the person doing the remembering. It
necessarily involves the feeling that the present recollection is a
reexperience of something that has happened before.
The primary goals of this chapter are to discuss and support two theoretical
propositions about episodic memory and autonoetic awareness. Because
episodic remembering necessarily entails a conscious reexperience of the
personal past, it is possible to conclude the following:
1. Episodic memory is critically dierent from all other varieties of
memory (e.g., stimulus-response strengthening, general knowledge
acquisition), and can be dissociated from them. An experimental
dissociation occurs when one particular
back upon the instance in which the fact was originally learned. Therefore,
source amnesia is a compelling phenomenon only when it occurs after
recent learning episodes.
Brain lesions in the prefrontal cortex have been associated with source
amnesia. In the most direct demonstration, Janowsky, Shimamura, and
Squire (1989) asked both patients and control subjects to learn a series of
facts (e.g., the name of the dog on the Cracker Jack box was Bingo).
Following a delay of about one week, all participants returned and were
asked questions that were based on either the facts they had seen the
week before (e.g., What was the name of the dog on the Cracker Jack box?)
or new facts that had not been studied but were potentially known. The
patients had no trouble retrieving the learned information, as they recalled
as many facts as the control group. Where the groups diverged was on a
followup question that probed about the source of the recalled facts.
Patients were strikingly more likely to claim that the experimentally
learned facts had actually been learned at some other time, before the
experiment. They were also more likely to guess that a pre-experimentally
learned fact had been encountered during the study phase of the
experiment when in reality it had not.
The Janowsky et al. (1989) data represent an example of a dissociation
between episodic and semantic memory. Despite the presence of
pathology, patients updated their semantic knowledge at levels that, at
least in this experiment, were equivalent to that of healthy controls. On the
fact-recall measures, they showed unimpaired noetic awareness of recently
studied items. When faced with questions about source, however, there
were striking diculties. For most healthy adults, the source questions
were not dicult. To answer the question, one must simply remember
studying the fact one week before. Results imply that the prefrontal injuries
somehow prevented the episodic recollection of the study episode, even
when semantic memory was successfully updated during the episode.
Relations between frontal dysfunction and source amnesia have also been
demonstrated in elderly populations, through correlational measures.
Because the neurobiological changes that occur with aging occur primarily
in the prefrontal cortex (Haug et al., 1983), it is possible to apply ndings
from research in cognitive aging to questions about frontal-lobe
functioning, and vice versa (West, 1996). Of course, such applications must
be made carefully.
Older adults are especially prone to source amnesia (M clntyre & Craik,
1987; Schacter, Kaszniak, Kihlstrom, & Valdiserri, 1991). Even when fact
recall is equated between the two age groups, elderly subjects are much
more likely to make source errors. Also, the ability to remember the source
of learned facts is correlated with performance on other, nonmemory
measures that are especially sensitive to frontal injury, such as the
Wisconsin Card Sorting Test, and word uency tests (Craik, Morris, Morris, &
Loewen, 1990). The simple ability to recall facts was not correlated with
these measures. Similar correlations have been discovered in patients with
anterograde amnesia that had varying degrees of pathology extending into
the prefrontal cortex (Schacter et al., 1984). Across these three
populations, there is converging evidence for a dissociation between
autonoetic episodic recollection and semantic learning, with only the
former dependent upon the frontal lobes.
There is another way to assess the extent to which recalled or recognized
items are being autonoetically recollected. The logic behind the
remember/know task is relatively simpleif one wants to determine
whether research participants are retrieving episodic memories, then one
can simply ask them (see Gardiner, 1988; Gardiner, Richardson-Klavehn,
chapter 15). Following retrieval of a previously studied item, test
instructions ask subjects to respond remember, or R, for those items on
the list whose prior experience they can consciously reexperience. Know,
or K, responses represent the acknowledgment that the test item was
encountered on the specied study list, but in the absence of any conscious
recollection of its occurrence. The very fact that participants are readily
willing to make know responses is evidence that people can make
judgments about single episodes from the recent past without relying upon
episodic memory.
In one comparison, Parkin and Walter (1992) required both elderly and
young adults to study a list of items before taking a recognition test,
followed by remember/know instructions. More recently, Wheeler and Stuss
(unpublished) had both patients with focal prefrontal injuries and also
healthy controls make living/ nonliving decisions about study words before
giving similar tests. In all of these experiments, there was some relatively
minor eect of prefrontal pathology (or age) on the recognition tests. The
eect reached statistical signicance in the Parkin and Walter (1992)
studies. There was a much larger discrepancy between
has identied a few patients with anterograde amnesia; the patients had
anoxic episodes as children (one virtually at birth, another at age 4, and
the other at age 9), and have bilateral pathology that is restricted almost
completely to the hippocampus. All suered their trauma over 10 years
prior to the study. They were brought to the attention of the researchers
because of their severe problems whenever they attempt to remember
events. None of the three was capable of taking on the types of
responsibilities that are commensurate with other young adults. Formal
neuropsychological testing was consistent with these observations, as all
three were found to be severely impaired whenever they attempted to
recall information that had been presented more than a few minutes
earlier.
From the description so far, the patients' proles match those of typical
anterograde amnesics: profound losses in the ability to remember things
that have occurred since the traumatic episode. But these three share one
capability that sets them apart from the majority of patients with damage
in the medial temporal regions: all of them have fared very well in
mainstream education. Despite a seemingly complete loss of the ability to
remember posttraumatic events, they are fully competent in speech and
language, and have acquired seemingly normal levels of factual knowledge
about the world. All three are within the normal range on the vocabulary,
information, and comprehension subtests of the Intelligence Quotient scale
(Vargha-Khadem et al., 1997). These retained bits of knowledge are
expressed condently and exibly, with noetic awareness only; both
anecdotal reports and formal testing strongly imply that the patients know
many things and remember nothing.
These patients show a dierent pattern of learning and memory decits
than previously reported amnesics. The classic patient HM, for example,
who had bilateral surgical excision of much of his medial temporal cortex
(Scoville & Milner, 1957), exhibits clear losses in the learning of both new
semantic knowledge (Cohen & Eichenbaum, 1994; Gabrieli, Cohen, &
Corkin, 1988) and the recollection of postsurgical episodes (Milner, Corkin,
& Teuber, 1968). Ostergaard (1987) studied a patient who, like the Vargha-
Khadem et al. patients, became amnesic during childhood; after assessing
the patient's progression for the next several years, the conclusion was that
both episodic and semantic memory were severely disrupted.
Discrepancies between dierent outcomes are probably related to the
specics of the underlying pathology. A recent magnetic resonance imaging
study with patient HM showed that the surgical excision had removed the
rostral portion of both hippocampi, and also much of the surrounding
entorhinal and perirhinal cortices (Corkin, Amaral, Gonzalez, Johnson, &
Hyman, 1997). Similarly, Ostergaard's patient's lesion included the entire
left hippocampus as well as the parahippocampal cortical areas. By
contrast, the Vargha-Khadem patients all had bilateral lesions in the
hippocampus proper with very little or no damage to the surrounding
cortices. It was suggested that the integrity of these surrounding cortices is
sucient to allow for the entry of information into semantic memory, while
additional processing from the hippocampus is necessary for episodic
encoding (Mishkin, Suzuki, Gadian, & Vargha-Khadem, 1997).
Because these ndings have been reported so recently, many questions
remain unanswered. For example, although the patients clearly fail to show
autonoetic awareness of the past, there is currently no way to know about
their ability to reect upon the personal present and future through such
acts as introspection, planning, and anticipation. Therefore, it remains a
possibility that the relation between these acts and episodic remembering
is not evident in all populations. The further examination of these three
patients and other similar patients is sure to provide new information about
the neural substrates of the dierent varieties of memory and conscious
awareness.
Conclusions
Episodic memory is the system of memory that allows us to experience the
world autonoetically. It is this dimensionthe ability to mentally travel
through timethat is not shared by any other system or variety of memory.
Other kinds of memory (semantic knowledge, stimulus-response
strengthening, perceptual priming) are tied to the present momentthat
is, one need not have any conscious awareness of the past or future to
utilize these nonepisodic varieties of memory. Episodic memory and
autonoetic awareness are not obligatory for an organism to recall,
recognize, report, or otherwise use information that was acquired in a
recent, single episode. Indeed, the evidence reported in this
chapter implies this point more strongly than any other. Although the
verbal recall or recognition of a recently studied fact, or the deferred
imitation of witnessed behaviors, may appear to an observer to be
compelling evidence for an operational episodic memory system, a number
of clever experiments have suggested otherwise. Individuals may know
many things about the world, including the personal past, but be unable to
mentally travel back in time to recollect the experiences upon which the
knowledge is based.
Episodic remembering bears a close family resemblance to other higher
order mental achievements (e.g., introspecting, daydreaming, anticipating)
that are not typically considered to be acts of memory. The patients with
large prefrontal lesions show these relations the most clearly, although
children between the ages of about 1 and 5 years demonstrate many
analogous symptoms. While neither population is amnesic, several dierent
researchers have independently remarked that both groups do not seem to
have the same kind of mental life as healthy, adult humans. They do not
merely show a dissociation between semantic and episodic memory of the
past; they appear to be more generally unable or unwilling to reect upon
their subjective experiences in the past, present, or future (see Wheeler et
al., 1997, for a longer discussion of these populations). It is too early to
know whether or not these relations will be evident in the amnesic patients
reported by Vargha-Khadem and colleagues (1997).