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Standard Consolidation Theory versus Multiple Trace Theory:
recent findings in retrograde amnesia
Erica Neutel, studnr. 5992028
Abstract
Theories on the mechanisms of memory benefit from research on the memory of amnesic
patients. The relationship between areas of brain damage and patterns of memory loss yield
insight into the storage and retrieval of memories. Here the two main theories of
consolidation, Standard Consolidation Theory and Multiple Trace Theory, are considered and
evidence from amnesia research, both for and against these theories, is evaluated. The number
of studies on the memory of amnesiacs is limited, as is the number of subjects in such studies.
Results do yield valuable information, though, confirming and contradicting some of the
predictions of both Standard Consolidation Theory and Multiple Trace Theory.
Contents
Introduction ………. ………………………………………………………………………………..2
A steep Ribot gradient for episodic memory: evidence for Standard Consolidation Theory ………4
A shallow Ribot gradient or none at all: evidence for Multiple Trace Theory.……………………..5
The various tests of episodic memory ………………………………………………………………7
Conclusion…………………………………………………………………………………………..10
References…………………………………………………………………………………………..11
Introduction
My eyes, switched on at last, saw the following: a nurse reaching out to take me from the
doctor; my mother’s triumphant face, as big as Mount Rushmore, as she watched me heading
for my first bath. (I said it was impossible, but still I remember it.) Jeffrey Eugenides,
Middlesex, 2002, p. 215.
This description of the first moments after birth caught in a memory is poetic precisely
because it is impossible: however much we would wish to, we do not remember those first
few days. But from about our fourth year of life, we all, gradually, do become able to save
things in our memory and keep them there, forever. Places, houses, situations, feelings,
people, will live in our minds, ready to be pondered upon, whenever we want to. But where
do they ‘live’? How are they stored? What ís a memory? These questions have fascinated
philosophers since ancient times, and from the 19th century on, starting with Hermann
Ebbinghaus, memory has been the subject of psychological, experimental study.
As is the case with many brain functions, in addition to behavioral studies of healthy
subjects, a significant source of knowledge has been the behavior of people with dysfunction,
in this case, amnesia. By studying the memories of amnesiacs, we can learn about the
processes of memory. A loss of memories of events before the onset of amnesia is called
‘retrograde’ amnesia and the inability to form new memories since the onset of amnesia is
called ‘anterograde’ amnesia. One important discovery has been that, in retrograde amnesia,
memories from long ago are often better preserved than recent memories. This pattern was
described by the French scientist Theodule Ribot (1883) and has subsequently become known
as the ‘Ribot gradient’. The phenomenon of the Ribot gradient has led to theories of memoryconsolidation. Because damage to the hippocampal system often leads to amnesia (e.g.
Penfield & Milner, 1958), and because in this amnesia, remote memories are often better
preserved than recent memories, it is proposed that memories first ‘reside’ in the hippocampal
system, i.e. the hippocampal system is needed to retrieve them, and then, over the course of
several years, are ‘transferred’ to the neocortex. So, finally, after several years, memories are
stored in the neocortex and their retrieval is independent from the hippocampal system. This
would explain why, after damage to the hippocampal system, remote memories can still be
retrieved whereas recent memories cannot. The recent memory has not been consolidated and
would need the (damaged) hippocampus for retrieval.
This consolidation should not be viewed as a transfer from one brain area to another,
though, but rather as a binding of neocortical traces by the hippocampus. By way of the
binding activity of the hippocampus, the memory becomes connected and anchored in the
neocortex. This process is described by connectionist models such as TraceLink (Murre,
1996). Without going into the technical details, I will describe this model here, to show how
the binding role of the hippocampus might work. In TraceLink, there are three subsystems:
(1) a trace system (neocortex), (2) a link system (hippocampus) and (3) a modulatory system
(representing areas in the brain that modulate learning). The trace system consists of many
modules, containing nodes. There is a limited connectivity between these nodes. The link
system has many connections with the trace system.
In this model, forming a memory of something that happened – what is called
‘episodic learning’ – takes place in four stages. In stage 1, when something happens (the
beginning of a memory), several nodes in the trace system are activated. In stage 2 the
connections between these particular nodes and the link system are strengthened and the
elements of the link system that are connected to these nodes are activated. In stage 3 the
actual consolidation begins: whenever some of the nodes in the trace system (a part of the
representation of the event) become activated, the activation will spread to the connected
elements of the link system, so the link system will activate the remainder of the nodes
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belonging to that event. Being activated together, the nodes in the trace system will become
interconnected. With each activation these connections within the trace system will become
stronger. In stage 4 the representation in the trace system is no longer dependent on the link
system. The connections between the link system and the trace system will be used for new
representations and the representation in the link system will gradually fade out. (The
modulatory system serves to control the learning rate and can be left out in this short
description.) In short: the hippocampus (the link system) has a temporary role in connecting
the elements in the neocortex (the trace system) and causes these elements to become
interconnected, after which the representation is set permanently in the neocortex and the role
of the hippocampus is played out.
A year after the TraceLink article, the standard consolidation theory was attacked by
Nadel and Moscovitch (1997). One of the arguments they used was the lack of evidence for
the Ribot gradient: sometimes, in amnesia following a lesion in the hippocampal area, a
temporal gradient in autobiographical memory is shallow or even absent. They introduced an
alternative theory, the ‘Multiple Trace Theory’. The main new aspect that distinguishes
Multiple Trace Theory from the Standard Consolidation Theory is that at every re-activation
of a memory trace, a new hippocampal trace is created, so of one memory, a multiple trace is
formed. In Multiple Trace Theory, memories are not transferred from the hippocampal system
to the neocortex; rather, autobiographical memory always depends on the hippocampal
system, which provides the necessary contextual information.
It is important here to make a distinction between ‘episodic’ and ‘semantic’ memory.
This is a widely used distinction, introduced by Tulving (1972). ‘Episodic memory’ is the
term used for the memory of information about temporally dated episodes or events (things
that happened, e.g. one’s wedding), whereas ‘semantic memory’ is used for the memory of
facts (things we know, e.g. Paris is the capital of France). According to the Multiple Trace
Theory only semantic memories become independent of the hippocampus; episodic
memories, also very remote ones, will always involve the hippocampus. In most standard
theories of consolidation, such as the TraceLink model, the neocortex is the store of both
episodic and semantic memory (but see McClelland, McNaughton & O’Reilly, 1995, and
Hasselmo & McClelland, 1999, for accounts of models of consolidation that do distinguish
the storage of episodic and semantic information).
In the past decade, these two conflicting theories – Standard Consolidation Theory and
Multiple Trace Theory –, and their predictions considering amnesia, have both stood their
ground and are often referred to as the main theories of consolidation of memory (e.g. Bright,
Buckman, Fradera, Yoshimasu, Colchester & Kopelman, 2006; Bayley, Hopkins & Squire,
2006; Hepner, Mohamed, Fulham & Miller, 2007; Noulhiane, Piolino, Hasboun, Clemenceau,
Baulac & Samson, 2007; Rosenbaum, Moscovitch, Foster, Schnyer, Gao, Kovacevic et al.,
2008). Wishing to resolve the conflict, Meeter and Murre (2004) have evaluated evidence
from several areas of research: fMRI studies (which measure activity in different brain
structures of healthy subjects during the retrieval of memories), animal experiments (which
study behavior after e.g. hippocampal lesions) and amnesia research (which studies the
relationship between brain damage and patterns of amnesia). Their conclusion is ambiguous
and the controversy remains: they have found evidence both for Standard Consolidation
Theory and for Multiple Trace Theory. The authors also criticize the vagueness of the
theories: clearer definitions are needed, as well as a more developed description of the
mechanisms suggested and the time frames involved.
Since 2004, the year Meeter and Murre’s review was published, there has been new
research that can shed light on the theories of consolidation. The three fields studied by
Meeter and Murre – fMRI studies, animal experiments and amnesia research – all have their
own possibilities and limitations. Studies of healthy individuals yield insight into normal
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memory processes, yet activity in certain brain areas during retrieval of memories does not
directly imply a crucial role for those brain areas. In order to obtain evidence for that crucial
role, we would have to lesion them. Lesions can be made in animals – at a certain moment, in
a certain limited brain area – but animals are not humans and animal research, as valuable as
it is, cannot tell us everything about human functioning. Amnesiacs are human and have real
brain damage, so their behavior tells us something about the crucial role of certain brain areas
for retrieval of memories, yet lesions are often diffuse and affect several brain regions (partly)
and, furthermore, there are not many amnesiacs, so these patient studies will always have a
relatively small group of subjects. All in all, each of these three fields of research yields a
valuable contribution; they complement each other. For now, I will confine myself to research
on amnesia and the Ribot gradient and ask the following question: which evidence for
Standard Consolidation Theory and for Multiple Trace Theory can be derived from studies of
remote and recent memories in amnesiacs, since 2004? First I will consider results yielding
evidence for Standard Consolidation Theory and then results yielding evidence for Multiple
Trace Theory. Subsequently, I will try to explain the discrepancy in the evidence by
examining the different memory tests that are used. Finally I will evaluate the two theories,
with the studied research in mind, and I will propose some directions for further research.
A steep Ribot gradient for episodic memory: evidence for Standard
Consolidation Theory
Multiple Trace Theory predicts a shallow Ribot gradient in the case of limited damage to the
hippocampal system. Remote memories are expected to withstand the loss of hippocampal
tissue better than recent memories, because of the multiple trace: remote memories have more
traces. In the case of a complete loss of the hippocampus, Multiple Trace Theory predicts a
complete loss of episodic memories. Hence, a steep Ribot gradient yields evidence against
Multiple Trace Theory, and, furthermore, results of patients whose hippocampus is
completely lost, but who nevertheless demonstrate intact remote episodic memory, are totally
incompatible with Multiple Trace Theory. In this section I will discuss five studies that refute
Multiple Trace Theory.
Three studies (Bayley, Gold, Hopkins & Squire, 2005; Bayley, Hopkins & Squire,
2006; Kirwan, Bayley, Galván & Squire, 2008) report results on varying, but overlapping
groups of eleven patients in total. The fact that in some cases the same patients are used for
different studies does not yield superfluous results on those patients. Because different
memory tests were used in the different studies, the results complement each other. Estimates
of the patients’ brain damage were based on MRI. The damage was either limited to the
hippocampal region, or covering a greater part of the temporal lobe, or temporal ánd
neocortical. The autobiographical memory of these patients was tested. Those patients with
hippocampal damage had retrograde amnesia of approximately 5 years, those with more
extensive temporal damage had retrograde amnesia of several decades and those patients with
temporal and neocortical damage had extensive memory loss, also for remote events. Remote
memory in patients with temporal damage was close to normal, i.e. a steep Ribot gradient.
The most remarkable result of these studies, however, is the fact that two of the
subjects, who were examined in all three of the studies, had a nearly complete loss of
hippocampal tissue (a reduction in volume of 98% (left) and 97% (right), resp. 100% (left)
and 93% (right)). Yet, the remote episodic memory of both of these patients was intact.
Despite the fact that this evidence is ‘small’ in the sense that it concerns only two patients, it
is strong nevertheless, because these results are simply incompatible with Multiple Trace
Theory.
4
A similar pattern was observed in a study by Hepner, Mohamed, Fulham and Miller
(2007), who examined a single patient with damage in the temporal lobe. This patient had a
normal remote autobiographic memory but his score in recent memory was low. Despite some
ambiguous results in other tests, this clear temporal gradient, together with the severity of the
brain damage – the MRI indicated an infarct involving all of the hippocampus – yields
evidence for Standard Consolidation Theory.
In the studies discussed so far, brain damage was assessed using MRI. Combinations
of neuropsychological tests and post-mortem neurohistological analysis are rare, but the
detailed information such studies yield, do make them very useful. Gold and Squire (2006)
performed such a study, on three memory-impaired patients. Although the results are that all
three patients show a definite temporally graded amnesia, contradicting Multiple Trace
Theory, the evidence is not as strong as in other studies. One patient had medial temporal lobe
damage, the other two patients had damage in the diencephalon. The diencephalon and the
hippocampus are connected and the authors suggest that diencephalic and medial temporal
lobe lesions can cause a similar memory impairment. However, one of the patients had
Korsakoff’s syndrome. She is said to have had heavy alcohol abuse of unknown duration, so
the memory loss might have been caused by the alcohol abuse. This makes the implications
for the functioning of normal memory less clear.
All of the evidence discussed here is limited: the first three studies concern eleven
patients, in the last two there was one patient with temporal damage. These small numbers are
inherent to this kind of patient research. Nevertheless, for gaining insight in the main question
of this paper, the evidence is valuable. In several cases a steep Ribot gradient is observed.
These results still hold when different methods of memory testing are used, as in the first
three studies. Perhaps the most convincing evidence is that of the two patients whose
hippocampus is completely destroyed, yet who still have an intact remote memory. This
means that the Multiple Trace Theory, as it is formulated by Nadel and Moscovitch (1997),
cannot hold. It would have to be adapted to incorporate the evidence discussed here. Evidence
against Standard Consolidation Theory can also be found. This evidence will be discussed in
the next section.
A shallow Ribot gradient or none at all: evidence for Multiple Trace Theory
No steep Ribot gradients were found in amnesia in three studies: Rosenbaum et al. (2008),
Steinvorth, Levine and Corkin (2005) and Rosenbaum, McKinnon, Levine and Moscovitch
(2004). In these studies, seven patients – four, two and one, respectively –, who all had medial
temporal damage, were examined. All patients had extensive memory loss with no or only a
shallow temporal gradient. In the first of these studies (Rosenbaum et al., 2008), it is argued
that episodic memory relies on the hippocampus because the patient with the most extensive
memory loss also had the highest degree of hippocampal damage. All four patients in this
study have diffuse damage, though, in many (cortical) regions besides the hippocampal area.
As memory loss can be caused by damage in other regions than the hippocampal area, and as
four patients is a small number, a relation between hippocampal damage and memory loss can
only lead to very tentative conclusions, so the evidence for Multiple Trace Theory might not
be as strong as the authors claim.
The other two studies are of special historic interest because two famous patients,
H.M. and K.C., are examined. Both studies used new methods of testing that were claimed to
be more sensitive to the episodic character of memories than the older tests. The studies
obtained results that confirm the predictions of Multiple Trace Theory, i.e. severe impairment
of autobiographical memory throughout the entire life span. The authors stress the importance
5
of the testing methods: old methods might have led to more positive results about episodic
memory than were warranted.
All three of the above studies have one disadvantage, though. In most of these
patients, damage was caused by a traffic accident, an infection, an infarct, or herpes
encephalitis. The resulting brain damage was very diffuse in every case. This makes it
relatively tricky to derive implications for the theories of memory processes and thus weakens
the evidence for Multiple Trace Theory. The only patient that had a lesion in a specific limited
area, is H.M., in the second study. He underwent a bilateral medial temporal lobe resection,
and hence his brain damage was limited to the medial temporal lobe. The same limited
damage was found in twelve of 21 subjects examined in a study by Bright et al. (2006). The
results seem to support Multiple Trace Theory, in that there was no steep Ribot gradient.
Autobiographical memory shows a shallow Ribot gradient for those with lateral temporal
damage and ambiguous ‘gradient’ (loss of recent and childhood memories, with relatively
spared memory for the years between) for those with medial temporal damage. The pattern of
memory loss in individual patients cannot be derived because only data for the entire groups
are given. A correlation between episodic recall and left lateral temporal and parahippocampal
volume was found. This result suggests a role for the hippocampal region in episodic
retrieval. Nine of 21 patients had frontal damage, but no correlations with frontal volume
were found. Since these correlations were computed over the (large) group of 21 subjects,
these results do give some evidence for the role of the temporal lobe in episodic memory and
hence for Multiple Trace Theory. Implications could have been made stronger if only remote
autobiographical recall would have been taken into account, though.
Clearly, patients who have had tissue removed in surgery, as in the case of H.M., yield
the most valuable results because their brain damage is limited and well described. A similar
patient is examined in the next two studies. Poreh et al. (2006) and Gilboa et al. (2006) study
one and the same patient, whose fornix had been lesioned. Because the fornix is part of the
‘extended’ hippocampal system (Gilboa et al., 2006), and damage to the fornix deprives the
hippocampal system of some of its crucial input, these two studies can inform us about the
role of the hippocampal system in memory. In both studies – using partly overlapping
memory tests – no Ribot gradient was found, again yielding evidence for Multiple Trace
Theory.
In most studies considered until now, evidence has been limited because of the small
number of patients that were examined and/or the diffuse brain damage. The next study has
neither of these two drawbacks. Noulhiane et al. (2007) examined the autobiographical
memory of 22 patients, who all had had a medial temporal lobe resection. Using yet another
memory test, they found that the patients’ episodic memory was impaired across the entire life
span. Given the large number of subjects and the limited temporal lobe damage, this does
indeed give evidence for the dependence of episodic memory on the hippocampal system, and
thus for Multiple Trace Theory.
The evidence discussed in this section is varied. Most studies concern only small
numbers of patients. Sometimes the brain damage is diffuse, making it difficult to interpret
results. Still, especially the relatively large number of different studies and the last study by
Noulhiane et al. (2007) seem convincing: the results indicate evidence against Standard
Consolidation Theory and for Multiple Trace Theory. Taking the evidence of this section and
the last section together, though, there is a discrepancy: on the one hand, steep Ribot gradients
are observed, on the other hand, shallow gradients or no gradients at all. This shows that
either, both theories are partly wrong, or the methods used in both groups of study are
different enough to cause such a difference in results. If there would have been a great
difference in memory tests, this would explain the discrepancy. Hence, it is worthwhile to
look more closely at the various memory tests that were used.
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The various tests of episodic memory
To achieve insight in how the several tests that are used, influenced the results, I will first give
a historical overview of the memory tests in question. I will describe any deviations from the
standard procedure of the tests. Subsequently, I will examine how the tests are divided among
the two groups of studies discussed in the previous sections.
The oldest test that was used, albeit in various modified versions, was the Crovitz Cue
Technique (Crovitz & Schiffman, 1974). In the Crovitz Cue Technique subjects are given a
list of twenty common, picturable nouns, such as ‘nail’ or ‘book’. They are told to inspect
each word until an episodic memory associated with that word comes to mind. They are asked
to write down a few words to identify that memory. After finishing the list, they are asked to
date the memories. A modification of the Crovitz Cue Technique is used in three of the
studies. Gold and Squire (2006) and Gilboa et al. (2006) used ten cue words instead of twenty
and rated each memory on specificity. Gold and Squire (2006) reported that the patients drew
a disproportionate number of memories from the very remote past. The subject in the study of
Gilboa et al. (2006) drew three of ten memories from the previous five years, which is similar
to controls. This test might give some information on patients’ memory, but as a means of
measuring memory loss for different periods of life, this method does not seem valid. A
tendency to come up with remote memories does not mean there are no recent memories. The
modification Hepner, Mohamed, Fulham and Miller (2007) made, was a great improvement.
They used only four cue words (happy, afraid, angry, surprised), but asked the patient to recall
incidents from four different time periods (childhood, young adult, adult, recent). Specificity
was rated here as well. This version of the test clearly gives more valuable information about
memory loss for different time periods than the former version.
To overcome some of the difficulties in the (original) Crovitz task Kopelman, Wilson
and Baddeley developed the Autobiographical Memory Interview (AMI) in the late eighties
(Kopelman, 1994). The AMI is a semi-structured interview schedule, containing 58 questions
of two different kinds, for semantic and episodic memory. Questions of the first kind are, e.g.
‘What was the name of the primary school you went to?’ and of the second kind, e.g. ‘Do you
remember something that happened to you in primary school?’ Childhood, early and later
adult life and recent events are covered, using ‘standard’ life events, like school, work,
weddings and children, ending with questions about the present time. All in all nine incidents
are to be recalled, from different time periods. The richness of the description and the
specificity in time and place are scored. This test clearly gives a better assessment of memory
for different time periods than the standard Crovitz task. The AMI is often used in the studies
discussed in this paper. Bright et al. (2006) modified the AMI, to achieve a more similar test
structure for all subjects. As in the AMI, subjects were asked to recall events from different
time periods, but they were provided with a three category cues: one event in the home, one at
school/college/hospital and one on a journey or holiday. As in the AMI, answers were scored
for richness and specificity, but also the number of prompts was recorded, to gain insight in
the ability to recall events.
Several authors (Kirwan, Bayley, Galván & Squire, 2008; Steinvorth, Levine &
Corkin, 2005; Rosenbaum, McKinnon, Levine & Moscovitch, 2004) are concerned that the
AMI is not sensitive enough to impairment and does not sufficiently measure richness of
detail, i.e. episodic character of the memories. The test they developed, a test with the perhaps
confusing name ‘The Autobiographical Interview’, is claimed to give a better assessment of
that episodic character. The Autobiographical Interview was originally designed for a study
comparing the episodic/semantic nature of recall of young people with that of older people
(Levine, Svoboda, Hay, Winocur, & Moscovitch, 2002). In this test, subjects are asked to
7
choose events from five life periods, aided by a list of 100 life events (e.g. seeing someone
famous in person). The difference between the Autobiographical Interview and the AMI lies
in the fact that the AMI has two kinds of questions, for semantic and episodic memory. In the
Autobiographical Interview, however, semantic and episodic autobiographical information is
extracted from within a single narrative. The Autobiographical Interview has several probing
procedures and an elaborate scoring procedure, that distinguishes between ‘internal’ and
‘external’ details: internal details pertain to the event described and reflect episodic
reexperiencing; external details are semantic, unspecific or factual. In one of the studies, a
modified version of the Autobiographical Interview was used: instead of the list of cue words,
family photos were used as cues (Gilboa et al., 2006). Kirwan, Bayley, Galván and Squire
(2008) and Steinvorth, Levine and Corkin (2005) explicitly avoided memories that were
thought of often, to make sure the memory was not part of what they called ‘personal
folklore’. Furthermore, Steinvorth, Levine and Corkin (2005), Rosenbaum, McKinnon,
Levine and Moscovitch (2004) and Rosenbaum et al. (2008) used two separate blind raters,
even though the Autobiographical Interview already has a high interrater reliability (Levine,
Svoboda, Hay, Winocur, & Moscovitch, 2002).
In the studies that were discussed, the Remember/Know procedure (Hirano, Noguchi,
Hosokawa & Takayama, 2002) and the TEMPau task (Piolino et al., 2003) were used only
once. In the Remember/Know procedure 55 questions were asked in three categories: personal
semantics (e.g. how old are your children?), autobiographical incidents (e.g. do you remember
your first child’s birth?) and public events (e.g. who was the president assassinated in Dallas,
U.S.A.?) The subjects are asked to recall correct information in response to each question.
Furthermore, for each response, the subject is asked to provide a remember/know response:
‘R’ if the response was accompanied by subjective feelings of his own experience and ‘K’ if it
was not. Apart from this Remember/Know procedure, Bayley, Gold, Hopkins and Squire also
asked their subjects to rate the vividness of the visual imagery in their recollection and to state
the viewpoint from which that imagery was seen, first-person or third-person viewpoint,
where first-person viewpoint would indicate the ‘remember’ character of the memory. The
TEMPau task uses the same Remember/Know procedure, and a semi-structured interview
similar to the modification of the AMI that Bright et al. (2006) used, i.e. asking for events
from different periods of life, in several categories (event linked to a person, school, work,
journey, family) and scoring the memories on specificity. Again, the subjects are asked to
give a subjective report of their state of consciousness (‘remember’ or ‘know’).
The methods that were used are quite varied. This might also explain why some
authors employ several methods of assessing autobiographical memory in one study (Hepner,
Mohamed, Fulham & Miller, 2007; Gilboa et al., 2006). The table on the next page yields, in
chronological order per group, an overview of the use of the different methods in the two
groups of studies.
8
results supporting Standard Consolidation Theory
study
test that was used
Bayley, Gold, 24 cue words, specificity rating,
Hopkins &
Remember/Know procedure
Squire, 2005. (Hirano, Noguchi, Hosokawa &
Takayama, 2002) vividness
rating, viewpoint.
Bayley,
AMI (Kopelman, 1994)
Hopkins &
Squire, 2006.
Gold &
Squire, 2006.
Hepner,
Mohamed,
Fulham &
Miller, 2007.
Kirwan,
Bayley,
Galván &
Squire, 2008.
results supporting Multiple Trace Theory
study
test that was used
Rosenbaum,
Autobiographical Interview
(Levine, Svoboda, Hay,
McKinnon,
Winocur & Moscovitch,
Levine &
2002)
Moscovitch,
2004.
Steinvorth,
Autobiographical Interview
(elaborate blind scoring)
Levine &
(Levine, Svoboda, Hay,
Corkin, 2005.
Winocur & Moscovitch,
2002)
Bright et al.,
new test, based on AMI
2006.
(Kopelman, 1994)
Crovitz Cue Technique,
specificity rating (Crovitz &
Schiffman, 1974)
AMI (Kopelman, 1994)
Crovitz Cue Technique (a
modified version) (Crovitz &
Schiffman, 1974)
Autobiographical Interview
(Levine, Svoboda, Hay, Winocur
& Moscovitch, 2002)
Poreh et al.,
2006.
AMI (Kopelman, 1994)
Gilboa et al.,
2006.
Crovitz Cue Technique (a
modified version) (Crovitz &
Schiffman, 1974)
AMI (Kopelman, 1994)
family photos
Autobiographical Interview
(a modified version) (Levine,
Svoboda, Hay, Winocur &
Moscovitch, 2002)
TEMPau task (a shortened
version) (Piolino et al., 2003)
Autobiographical Interview
(Levine, Svoboda, Hay,
Winocur & Moscovitch,
2002)
Noulhiane et
al., 2007.
Rosenbaum et
al., 2008.
Clearly, the division among the two groups is quite even: all types of methods are used
in both groups. (Here, the TEMPau task and the Remember/Know procedure are considered
to be similar tests.) Hence, even though some of the methods might be questionable, the
difference between methods does not explain the discrepancy in the results.
9
Conclusion
Recent studies on brain damage and episodic memory in amnesiacs have not led to a
definitive answer in the debate between Standard Consolidation Theory and Multiple Trace
Theory. Results have been found in favour of both of the two theories. The role of the
hippocampus in remote episodic memory is still a matter of controversy. Episodic memory is
not the only topic in this controversy, however: the brain areas needed for the memory for
spatial orientation, which is considered an important function of the hippocampus, is similarly
unclear. Research has been done on navigation in old environments. Both Maguire, Nannery
and Spiers (2006) and Rosenbaum, Gao, Richards, Black and Moscovitch (2005) tested a
former taxi driver with hippocampal damage. Whereas Maguire, Nannery and Spiers (2006)
find that in their patient navigation in old environments is highly impaired and restricted to
main roads, Rosenbaum, Gao, Richards, Black and Moscovitch (2005) conclude that their
patient’s ability to navigate was unimpaired. The former result indicates a reliance on the
hippocampus for remote spatial memory, the latter indicates retrieval independent of the
hippocampus. This is a discrepancy similar to that in episodic memory.
One important feature of this research and of the research discussed earlier is the very
small number of subjects in the studies. This makes the results difficult to interpret. Perhaps
individual differences in brain structure, in brain damage and in the development of the
dysfunction might account for some of the differences found in results. These small numbers
will always be an aspect of this kind of patient research. That makes it all the more important
to agree on the methods of research that are used. In this kind of research memory tests play
an important role. Many authors (e.g. Ivanoiu, Cooper, Shanks & Venneri, 2006; Steinvorth,
Levine & Corkin, 2005) criticize traditional methods like the AMI or the Crovitz Cue
Technique and in many studies new tests of memory are developed especially for that
particular study, often partly based on existing methods (e.g. Ivanoiu, Cooper, Shanks &
Venneri, 2006; Bright et al., 2006; Hepner, Mohamed, Fulham & Milner, 2007; Gilboa et al.,
2006). This leads to a great variety of methods, which makes an interpretation of the results,
and a comparison of studies, quite difficult. More agreement among researchers on the tests
that are suitable for such research would be valuable, also considering the small number of
studies.
For the main question of this paper, though, the variation in methods has not been a
disadvantage, because all methods are found in both groups of studies: the studies with results
supporting Standard Consolidation Theory and those with results supporting Multiple Trace
Theory. One could argue that the studies complement each other and strengthen each other’s
evidence. This leaves the controversy undecided. Meeter and Murre (2004) state that they
hope that more research will enable the scientific community to choose between the theories. I
argue that it is not a matter of choosing, but rather a matter of adjusting the theories to this
new evidence. Neither of these theories can explain all of the evidence. Some of it simply
contradicts the predictions made by the theory. According to Multiple Trace Theory there is a
continuing involvement of the hippocampal complex in episodic memory, even in remote
episodic memory (Nadel & Moscovitch, 1997). The first three studies that were discussed,
however, report two patients with a complete loss of hippocampal tissue but with intact
remote episodic memory (Bayley, Gold, Hopkins & Squire, 2005; Bayley, Hopkins & Squire,
2006; Kirwan, Bayley, Galván & Squire, 2008). These results should somehow be
incorporated in Multiple Trace Theory. On the other hand, within Standard Consolidation
Theory results of a shallow or no Ribot gradient should be explained. Furthermore, any theory
of memory should pay attention to episodic versus semantic memory, because studies often
report a difference in the retrieval of episodic and semantic memory. So also Standard
Consolidation Theory does not satisfy in its present form. Thus, rather than a choice between
10
theories, adaptation of the theories is required. This adaptation might also reduce the
vagueness in definitions that Meeter and Murre (2004) criticized, and perhaps specify the
mechanisms and time frames.
To obtain adaptations, or perhaps come to a unifying theory that incorporates elements
of both theories, research in remote memory of amnesiacs will continue to be valuable. The
development of theory and the research should complement each other, in the sense that
requirements of the memory tests should be derived from the mechanisms proposed in the
theories. There need not be a consensus on memory theories, but there should be a consensus
on the definitions of episodic and semantic memory and on the interpretations of the results
on tests of memory. Furthermore, there should be a consensus on which tests of memory are
appropriate, so that a plethora of different tests, like the one observed in the studies that were
discussed here, can be avoided. Conversely, of course, results from amnesia studies should
continue to inform theorists and influence theories. With the help of studies like these, within
a clear framework and with a consensus on tests, theorizing and modeling might result in a
unifying theory, incorporating several aspects of Standard Consolidation Theory as well as of
Multiple Trace Theory.
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