Long-Term Recency in Anterograde Amnesia: Deborah Talmi, Jeremy B. Caplan, Brian Richards, Morris Moscovitch
Long-Term Recency in Anterograde Amnesia: Deborah Talmi, Jeremy B. Caplan, Brian Richards, Morris Moscovitch
* [Link]@[Link]
Abstract
Amnesia is usually described as an impairment of a long-term memory (LTM) despite an in-
tact short-term memory (STM). The intact recency effect in amnesia had supported this
view. Although dual-store models of memory have been challenged by single-store models
based on interference theory, this had relatively little influence on our understanding and
treatment of amnesia, perhaps because the debate has centred on experiments in the neu-
OPEN ACCESS
rologically intact population. Here we tested a key prediction of single-store models for free
Citation: Talmi D, Caplan JB, Richards B, recall in amnesia: that people with amnesia will exhibit a memory advantage for the most re-
Moscovitch M (2015) Long-Term Recency in
Anterograde Amnesia. PLoS ONE 10(6): e0124084.
cent items even when all items are stored in and retrieved from LTM, an effect called long-
doi:10.1371/[Link].0124084 term recency. People with amnesia and matched controls studied, and then free-recalled,
Academic Editor: Efthimios M. C. Skoulakis,
word lists with a distractor task following each word, including the last (continual distractor
Alexander Fleming Biomedical Sciences Research task, CDFR). This condition was compared to an Immediate Free Recall (IFR, no distrac-
Center, GREECE tors) and a Delayed Free Recall (DFR, end-of-list distractor only) condition. People with am-
Received: September 15, 2014 nesia demonstrated the full long-term recency pattern: the recency effect was attenuated in
Accepted: March 8, 2015
DFR and returned in CDFR. The advantage of recency over midlist items in CDFR was
comparable to that of controls, confirming a key prediction of single-store models. Memory
Published: June 5, 2015
deficits appeared only after the first word recalled in each list, suggesting the impairment in
Copyright: © 2015 Talmi et al. This is an open amnesia may emerge only as the participant’s recall sequence develops, perhaps due to in-
access article distributed under the terms of the
Creative Commons Attribution License, which permits
creased susceptibility to output interference. Our findings suggest that interference mecha-
unrestricted use, distribution, and reproduction in any nisms are preserved in amnesia despite the overall impairment to LTM, and challenge strict
medium, provided the original author and source are dual-store models of memory and their dominance in explaining amnesia. We discuss the
credited.
implication of our findings for rehabilitation.
Data Availability Statement: Requests for data will
be received at the first author’s university article
repository, and is associated with the publications ID
number/DOI for this article at: [Link]
[Link].
Introduction
Funding: This work was supported by a Canadian
Institute of Health Research grant MOP 49566 to
Anterograde amnesia is defined as an impairment of memory retrieval from a long-term mem-
MM. The funder had no role in study design, data ory (LTM) store accompanied by intact retrieval from a short-term memory (STM) store or
collection and analysis, decision to publish, or working memory [1–3], a definition expressed in many modern textbooks [4, 5]. This view of
preparation of the manuscript. amnesia assumes a dual-store model of memory [6], and has persisted despite an ongoing de-
Competing Interests: The authors have declared bate between dual-store and single-store models on explaining memory behaviour in healthy
that no competing interests exist. participants [7–13] and a variety of findings from neuropsychology, neuroimaging and animal
models of memory [14]. Provocatively, even Crowder, who argues against dual-store models,
pointed out that his own textbook expressed the dual-store view [15, 16]. Here we focus on sin-
gle-store models and a key prediction they make for amnesia: that people with amnesia would
exhibit an intact long-term recency effect. As we discuss below, this prediction also has impor-
tant value for rehabilitation. Before we turn to this specific prediction, however, we first pro-
vide some background for this debate to clarify why this prediction is important.
theory models of memory, which only posited a single memory store. Therefore, the long-term
recency effect was a cornerstone in their ascendance over early dual-store models [7–12].
Single store models could also predict the pattern of deficits in amnesia [11, 28, 29], and
claim, in the interest of parsimony, that the debate is settled in favour of the single store model.
Because this claim rests primarily on evidence of long-term recency effects in healthy controls,
and on only one study in amnesia [22], the dominant view of amnesia is still firmly grounded
in the classical dual store model.
Hybrid models
Baddeley and Hitch [13] claim that interference-based models of memory fare poorly in ex-
plaining very long term recency, for instance, when recalling the results of a sport season a long
while after it is over (Baddeley & Hitch, 1977). In such situations the retrieval context is a lot
more different from the context of encoding of multiple game instances, and it is less likely that
similarity would favour memory for the most recent game. To resolve this they propose an al-
ternative model of recency, called the Activation Model. In this model recently presented items
are more strongly ‘activated’ than other items. In indirect tests of memory this activation would
yield priming effect. Recency effects in direct tests of long-term memory tests ensue when par-
ticipants adopt a strategy of retrieving more highly activated items first. The differences between
this model of long-term memory and other interference-based models still need to be worked
out. The Activation Model could be considered a ‘hybrid’ model of memory because the authors
assume that this process could occur in multiple memory stores, and do not commit to a single
store view [13]. A model that is ‘hybrid’ by design was suggested by Davelaar et al (2005). Their
model assumes two memory stores, STM and LTM, and accommodates the long-term recency
effect by assuming that LTM functions as interference-based models predict.
The performance of people with amnesia on IFR has been researched extensively, and ac-
cords with the predictions of both dual and single store models. People with amnesia exhibit an
intact recency effect in IFR accompanied by a reduced probability of recalling items from earli-
er in the list [30–35]. This pattern is compatible with the notion that final list items are re-
trieved from an intact short-term memory store, whereas earlier items are retrieved from an
impaired LTM. It is also compatible with interference-based single-store models and the acti-
vation model or recency, which assume that recent items have a retrieval advantage. To ac-
count for poorer retrieval of earlier items in amnesia, these views could refer to reduced
rehearsal [36] or increased susceptibility to interference [37–41]. The performance of people
with amnesia on CDFR has not been established.
Crucially, given the scale-invariance that interference-based single store models of memory
assume, they must predict that whatever memory is spared in amnesia must also be scale-in-
variant; hence, these models predict an intact long-term recency effect in amnesia, equivalent
in magnitude to the effect in controls. Classical dual-store models cannot account for long-
term recency in any population. Finally, hybrid models do not need to predict scale invariance
because they assume that memory operates differently at different time scales.
Taken together, a demonstration of long-term recency in amnesia is of theoretical interest
because it would only provide a strong support for single-store models. Both single-store and
hybrid models can account for the full long-term recency pattern, namely recency in IFR
which is reduced in DFR and then returns in CDFR (hybrid models do so at the cost of re-
duced parsimony); but only single-store models predict that the LTR should be unaltered in
amnesia (equivalent to controls).
The question of whether or not people with amnesia exhibit a long-term recency effect is
not only of theoretical interest. Currently, in accordance with the classical, early dual store
model definition of amnesia, patients are thought not to be able to retain any information in
LTM. Although clinical observations show that patients do sporadically report such informa-
tion, and free-recall intrusions from previous list have also been documented in the research
literature [13, 42], these reports are not thought to be governed by any known rules and are,
therefore, given little weight.
To emphasize the clinical relevance of our findings we attempted to demonstrate the eco-
logical validity of the long-term recency effect in this group. For this purpose we designed an
incidental song-recall task. Participants listened to one song after each free-recall period (fol-
lowing each of the study lists) and were asked to recall the songs freely at the end of the testing
session. The song-recall task can be viewed as a form of (incidental) continual-distractor free
recall procedure, in which the word-list task takes on the role of the distractor. If participants
with amnesia exhibit long-term recency in CDFR, they should also recall more of the songs
they studied late in the course of the experiment relative to those they studied at the beginning
of the session.
Our work follows up on a previous attempt to characterise long-term recency in amnesia.
Carlesimo and colleagues [22] first tested for long-term recency in people with amnesia. They
described their results as people with amnesia exhibiting an intact recency effect in IFR, in line
with previous work [30–35], but an impaired recency effect in CDFR compared to neurologi-
cally intact controls. This would be an important finding because it cannot be accommodated
by single-store models of memory, which predict scale invariance. However, the authors’ inter-
pretation is not the only possible view of their results. What they actually found in the CDFR
condition was an equivalent-sized reduction in probability of recall at all serial positions.
Equality of recency slopes is the relevant prediction of interference-based single-store models
and the activation model of recency, and visual inspection of the data suggests that the slopes
of the recency effects were quite similar for patients as for controls in their CDFR condition.
More seriously, as also noted by others [11], the authors used an entirely different methodology
in the IFR and CDFR conditions; in the IFR condition, Carlesimo et al.’s participants were
given a list of words to study and recall, whereas in CDFR, participants were given the list of
words as anagrams to solve, with the unscrambled words being the target material for subse-
quent recall (a paradigm previously used by Vallar, Papagno and Baddeley, 1991). This differ-
ence in methodologies between the IFR and CDFR conditions makes it difficult to draw
inferences across the two tasks. For example, although anagram solution generally motivates
incidental study, controls may have rehearsed more than patients [7] during the distractor
tasks, which could have aided their retrieval of the final list items and artificially increased their
long-term recency. It could be that in the CDFR task, there was simply a group difference
(main effect) in overall difficulty of the task, and if they had used the same anagram task during
their IFR condition, perhaps the main effect would have been evident in that task as well.
Moreover, Carlesimo et al.’s study is made even more inconclusive because it lacked the
DFR condition, which is an essential component of the traditional long-term recency debate. It
is the flattening of the recency effect in the DFR condition that establishes that the distractor
task is effective (either in emptying STM, from the perspective of dual-store models, or in pro-
viding a sufficiently strong contextual shift, from the perspective of interference-theory based
models). Without the DFR condition, we do not know if the distractor task was equally effec-
tive across amnesic and control groups. Moreover, we don’t even know if either group exhib-
ited long-term recency by the standard definition, which demands: a) recency in the IFR
condition, plus b) a flattening of the recency effect in the DFR condition, followed by c) a re-
turn of recency in the CDFR condition, exceeding that in the DFR condition. In other words,
the basic validity tests were missing. A flattened recency effect in DFR that then returned in
CDFR would militate against the criticism above. Here we applied the full set of conditions
(IFR, DFR and CDFR) to both people with amnesia and neurologically intact controls, using
the same procedure across conditions and groups. Finally, because amnesic participants are
often found to be at a disadvantage in intentional memory tasks but unimpaired in incidental
and implicit memory tasks (e.g. [43]), we employed an intentional study test to provide a stron-
ger test of long-term recency in amnesia.
Controls Patients
Mean SD Mean SD
Age 55.33 7.06 52.56 5.13
Years of Education 16.00 2.36 16.22 3.15
Premorbid intelligence 110.47 10.07 109.89 11.23
Digits span forward 7.27 1.33 7.11 0.93
Digits span backward 5.53 1.46 5.00 1.66
Note. SD = standard deviation. Premorbid intelligence was assessed using the Wechsler Test of Adult
Reading.
doi:10.1371/[Link].0124084.t001
PR MS JSB DA MT RR KM MB KC
Male/Female M M M M M F F M M
Age 47 52 59 55 42 56 53 55 54
Aetiology Seizures Encephalitis Korsakoff Encephalitis Aneurism Cyst removal Aneurism Aneurism Head Trauma
WTAR 106 120 119 117 92 96 119 119 101
WASI
FSQ 82%ile 87%ile 92%ile 87%ile High average* 81%ile 55%ile 90%ile 47%ile
VSQ 86%ile 94%ile 96%ile 92%ile Average* 81%ile 12%ile 91%ile 47%ile
PSQ 70%ile 47%ile 77%ile 66%ile Superior* 73%ile 96%ile 86%ile 47%ile
Digit Span
Total 10 18 25 18 16 22 16 21 17
Forward 5 8 8 7 7 7 7 7 8
Back 3 5 7 5 4 7 4 7 3
CVLT
Immediate recall 4%ile 25%ile 2%ile <1%ile <1%ile 4%ile <1%ile 3%ile <1%ile
Short delay 0 1 0 0 0 0 2 4 <1%ile
Long delay 0 1 1 0 0 0 0 2 <1%ile
BVMT
Immediate recall 0%ile** <1%ile 2%ile 1%ile <1%ile <1%ile 7%ile ] 7%ile
Delayed recall 0%ile** 1%ile 4%ile <1%ile <1%ile <1%ile 7%ile 1%ile] <1%ile
Recognition <1%ile** 11–16%ile 6–10%ile <1%ile 11–16%ile 1–2%ile >16%ile ] 1–2%ile
Fluency
Phonemic (FAS) 6¼ 45%ile 63%ile 98%ile 30%ile 16%ile 16%ile <1%ile 7–13%ile
Semantic (animals) 6¼ 19%ile 37%ile 50%ile 10%ile 12%ile 99%ile <1%ile 50%ile
WCST >16%ile >16%ile >16%ile >16%ile >16%ile >16%ile _6¼ >16%ile >16%ile
Notes. WASI = Wechsler Abbreviated Test of Intelligence; FSQ = full scale quotient; VSQ = visual scale quotient; PSQ = performance scale quotient;
WTAR = Wechsler Test of Adult Reading; CVLT = California Verbal Learning Test; BVMT = Brief Visual Memory Test; FAS = Letter fluency test;
WCST = Wisconsin Card Sorting Test. The values given are the raw scores when they were available; otherwise we noted the percentile scores.
*This description was the only "score" provided for us.
**The complex figure of the Kaplan Baycrest Neuropsychological Assessment (KBNA) was administered instead of the BVMT.
6¼
Not tested in this patient.
]
The Rey-Osterrieth Complex Figure Test was administered instead of the BVMT.
doi:10.1371/[Link].0124084.t002
Control participants were recruited from the University of Toronto and the Rotman Re-
search Institute volunteer pool. The study received the approval of the Toronto Academic
Health Sciences Network ethics review board.
Materials
Word stimuli. Nine word lists were constructed, and three lists were used in each one of
three experimental tasks: IFR, DFR, and Each word lists consisted of 9 words. Six of the words
in each list were randomly sampled without replacement for each participant from the same
pool of 78 words. In addition, to these six words, three ‘target’ words in each list were sampled
without replacement from a separate pool of 27 words and placed randomly in serial positions
1, 5, and 9. The 3-letter stem of target words had between 4 and 9 accessible completions
(M = 5.78, SD = 1.7%) and the average probability of each word to be given as a first response
to the stem ranged from 2% to 9.3% (M = 4.1%, SD = 2.2% according to published norms
[45]). None of the target words had the same stem as another word in the experiment. All
experimental words were nouns, had 5–6 letters, mean frequency of 41.62, SD = 54.68 [46],
mean concreteness of 553, SD = 67.37 [47], and all were neutral in valence. To reduce proactive
interference, words for practice trials were all proper names, sampled from a pool of 30 male
and female first names. Words were presented in lowercase, black 72-point Times New Roman
font on a yellow background.
Distractor task stimuli. The stimuli for the distractor task were simple yet cognitively de-
manding arithmetic problems. Each included three randomly sampled single digits and a solution
which could be correct or incorrect. Two of the digits had values between 1–5 and one had values
between 1–9. Incorrect solutions were larger or smaller than the correct one by 1 (for example, 9
+4+2 = 16 or 3+8+1 = 12). The problems were presented on a grey background in the center of to
the left or the right of the center of a grey screen, in black 28-point Times New Roman font.
Song excerpts. All songs used in the song-recall task were highly familiar, uplifting, popu-
lar American songs, such as ‘Rock around the Clock’ or ‘Singing in the Rain.’ To increase the
chances that most participants, even those with retrograde amnesia, would be familiar with
most of the songs, we selected songs which were mostly released in the fifties and sixties; the
most recent song used was ‘American Pie,’ released in 1971. One-minute excerpts from each
song, which included the most familiar part (e.g. the chorus), were converted to 22050 samples,
8-bit stereo files. One song was played after each list for a total of nine songs in all. Song order
was randomized for each participant.
Procedure
Prior to the experiment itself, participants received initial practice which included studying
and recalling three 4-word lists, and performing the distractor task three times. Following ini-
tial practice, all participants were able to answer at least one distractor question and recall at
least one word. The order of the three experimental tasks was counterbalanced across partici-
pants. Each task began with instructions and one practice list, and included three word lists.
Fig 1 depicts the encoding and testing procedure for each list. Participants were reminded of
the instructions before each list. The experimenter recorded all words participants recalled. A
five-minute break followed each task. During the first break, participants completed the
WTAR. There was no task during the second break. The digit span task (forward and back-
ward) was administered after the last task. Finally participants were reminded that some songs
were played during the course of the experiment and were invited to take as much time as they
needed to recall freely the names of these songs.
Immediate free recall (IFR). Words were presented for 3 seconds each. The orienting task
for encoding required participants to rate each word as either ‘pleasant’ or ‘unpleasant’. They
rated the words by pressing one of two marked keys on a computer keyboard; the rest of the
keyboard was covered with cardboard in order to make it easier for patients to switch back to
the orienting task in CDFR. A blank inter-stimulus interval (ISI) of 500 ms followed each
word. The instruction ‘Recall words’ was presented after the final ISI and participants were
given 45 seconds to recall studied words in any order.
Delayed free recall (DFR). The procedure was almost identical to IFR, except that follow-
ing the last ISI participants performed the distractor task for 30 seconds.
Continual-distractor free recall (CDFR). The procedure was almost identical to that of
the IFR task, but instead of the blank ISI which followed each word, participants performed the
distractor task for 15 seconds. They also performed the distractor task for 15 seconds once be-
fore the first word, and for 30 seconds after the last studied word.
Distractor task. The computer monitor changed colour to grey when the task began. A
single arithmetic problem was presented, and participants read it out loud, and say ‘yes’ if the
Fig 1. Task structure. Participants saw 9 word lists, 3 in each of 3 conditions—IFR, DFR, and CDFR. After
each list a song was played for 1 minute, and participants’ familiarity with the song was assessed. The CDFR
condition is illustrated in more detail on the right with timing information shown under the timeline arrow. This
condition included the presentation of three 9-word lists (grey screens). An inter-word interval preceded each
of the 9 words (white screens with grey frames) and was filled with an arithmetic task. A longer interval was
inserted after the last word, just before the recall test. At the end of that final interval participants saw the word
‘Recall’ and invited to freely recall the words they remembered (white screen with black frame). They were
then given a cued recall for three of the words (black screens).
doi:10.1371/[Link].0124084.g001
solution was correct, and ‘no’ if it was incorrect. The experimenter keyed in their response,
which triggered the next problem.
Cued recall. This test provides more support during retrieval than free recall and was in-
cluded to allow even the most densely amnesic participants to experience some success in re-
trieving studied words so as to motivate them during the course of this challenging experiment.
The instructions encouraged participants to first think back about the studied list and attempt
to retrieve a studied word, but if they could recall no appropriate completion, to complete the
stem with the first word that came to mind [48]. The cued recall test began as soon as partici-
pants completed each free-recall test and consisted of a presentation of the stems for each one
of the three target words (serial positions 1, 5 and 9) in a random order. Participants verbally
completed each presented stem before the next stem appeared. Results from this test are re-
ported in Table 3 but because of potentially differential reliance on implicit memory in the pa-
tient and control groups they are not analysed further.
Song encoding. Immediately following each cued recall test, participants were instructed
to relax and listen to a single song excerpt. They then answered the following questions about
it: (1) Is the song familiar to you? (2) What is the name of the song? (3) Do you know all, some,
Note. The average number (and SD) of words participants provided in a cued recall test after IFR, DFR and CDFR tests. The numbers (1, 5, and 9) refer
to the serial positions of the studied words to which the cues referred. For example, patients given a cue for the first word they studied in IFR retrieved, on
average, 0.63 of a word, compared to controls, who retrieved 0.87 of a word.
doi:10.1371/[Link].0124084.t003
or none of the words? (4) Can you hum all, some, or none of the tune? All participants enjoyed
the song task and experienced success in it, which helped motivate those who found recalling
the words particularly challenging.
Adapting the recall task to people with amnesia. Task switching between word study
and the distractor task was more difficult for patients than controls, because they did not al-
ways remember the complete set of instructions. When patients failed to rate a word, or did
not immediately begin reading the arithmetic problems, the experimenter gave short remind-
ers, either pointing at the keyboard or at the screen, or providing short verbal cues (‘read the
exercise’, ‘rate the word’). Following the practice list, patients were able to perform the tasks ad-
equately with minimum reminders. The necessity of these reminders for patients but not con-
trols was the only difference in procedure between the two groups.
Results
All data is freely available to download from the first author’s university article repository
([Link]
Fig 2. Number of words recalled as a function of group and serial position. (a) IFR (b) DFR (c) CDFR.
Error bars represent standard error.
doi:10.1371/[Link].0124084.g002
Fig 3. Number of words recalled as a function of group and serial position. Here the data are re-plotted
from Fig 2 with all conditions (IFR, DFR and CDFR) plotted for Controls (a) and Amnesia (b) separately. Note
that both groups show a reduction of recency in DFR compared to IFR, and a return of recency in CDFR
compared to DFR.
doi:10.1371/[Link].0124084.g003
p<.01, partial η2 = .37] and Group interacted with Serial Position [F(8,176) = 3.25, p<.01, par-
tial η2 = .13]. To explore this interaction we carried out a series of Bonferroni-corrected one-
tailed t-tests on recall from primacy, midlist and recency positions, computed as described
above. These revealed that this interaction was due to the fact that relative to patients, controls
recalled more primacy [t(22) = 4.35, p<.005] and midlist [t(22) = 2.69, p<.01] items, but there
was no significant difference between the groups in recall of recency items (t<1). As expected,
both controls [t(14) = 5.12 p<005] and patients [t(8) = 6.61, p<.005] recalled more recency
than midlist items. In CDFR, Serial Position had a significant effect on probability of recall [F
(8,176) = 1.99, p = .05, partial η2 = .08], an effect which exhibited a quadratic trend [F(1,22) =
6.50, p<.05, partial η2 = .23]. The main effect of Group was significant [F(1,22) = 20.23,
p<.001, partial η2 = .48] but Group did not interact with Serial Position [F<1]. Recency items
were recalled more often than midlist items when both groups were considered together [t(23)
= 2.53, p<01, one-tailed]. Although the interaction with Group was not significant, for com-
pletion we report that one-tailed t-tests confirmed that this effect remained significant when
each group was examined separately [controls: t(14) = 1.93, p<.05; patients: t(8) = 2.29,
p<.05]. Serial Position did not have a significant effect on DFR, [F(8,176) = 1.07, p>.10, partial
η2 = .05]. The main effect of Group was significant [F(1,22) = 30.86, p<.001, partial η2 = .58]
but Group did not interact significantly with Serial Position [F<1].
Fig 4. Number of words recalled at the first recall attempt as a function of group and serial position.
(a) IFR. (b) DFR. (c) CDFR.
doi:10.1371/[Link].0124084.g004
Fig 5. Song recall as a function of group and serial position. Error bars represent standard error.
doi:10.1371/[Link].0124084.g005
(11,242) = 2.74, p<.01, partial η2 = .11], and exhibited linear [F(1,22) = 20.11, p<.001, partial
η2 = .48] and quadratic [F(1,22) = 7.22, p<.05, partial η2 = .25] trends consistent with the pres-
ence of both recency and primacy effects. Patients recalled fewer songs than controls [F(1,22) =
10.85, p<.01, partial η2 = .33] but Group did not interact with Serial Position, F<1.
Distractor task
The effect of Task (DFR, CDFR) on the number of exercises attempted and on solution accura-
cy during the distractor task was analysed with two repeated measures ANOVAs with Group
as a between-subject factor. The results indicate that patients found the distractor task more
difficult than controls in both DFR and CDFR. Patients attempted to solve fewer exercises than
controls F(1,22) = 5.44, p<.05, partial η2 = .20, and their accuracy was overall lower than that
of controls, F(1,22) = 5.21, p<.05, partial η2 = .19. All participants attempted more exercises in
CDFR than DFR task [F(1,22) = 45.05, p<.001, partial η2 = .67; the interaction with Group was
non-significant, F(1,22) = 3.68, p = .07]. Accuracy was higher in DFR [F(1,22) = 19.41, p<.001,
partial η2 = .47].
Discussion
Our chief finding was an intact long-term recency effect in participants with amnesia, as indi-
cated by their having a memory advantage equivalent to that of controls for recent, as com-
pared to other items. Indeed, patients exhibited intact recency effects in CDFR and in an
analogous task, recall of interspersed songs, confirming a key prediction of single-store models.
The intact recency effects in the patient group contrasted with their reduced probability of re-
call across all serial positions, apart from the recency portion of the IFR condition where their
free recall was as good as that of controls.
These patient data alone already exhibit all the crucial features of the standard argument
against strict dual-store models and in favour of the single-store, interference-theory account.
Recency was present in IFR, flattened in DFR, and then returned in CDFR despite the end-of-
list distractor being the same in the CDFR and DFR conditions. This already supports single
store models, and shows that their argument against dual-store models generalizes to people
with amnesia. This is arguably a more direct test than comparisons between groups, because
not only are conditions within a group matched on a whole set of variables, but we can also be
more certain that a participant’s experience during study was well equated across conditions.
The comparison between groups is informative, nonetheless. Specifically, because the full long-
term recency pattern was observed in both groups, we can conclude not only that people with
amnesia exhibit long-term recency, but that they can do so under conditions in which control
participants also exhibit long-term recency.
Our findings qualitatively replicate those of Carlesimo et al. (1996) for the conditions com-
mon to both. Comparing their Figs 1 and 3 suggests that the serial position curve in CDFR is
steeper in Carlesimo et al.’s study. This could be due to controls in that study rehearsing the
first and last few anagrams throughout the distractor task, because they, unlike patients, could
remember that a memory test was coming up. Because we included a DFR condition and used
the same procedure across IFR, DFR and CDFR we can be more confident than Carlesimo et al.
in comparing across conditions and groups. Had controls used such a strategy in our study they
would have also exhibited a recency effect in the DFR condition. Proponents of dual-store mod-
els can be reassured, as a consequence of our additional DFR condition, that both groups of par-
ticipants must have retrieved the recency items in CDFR from long-term memory.
Because the patient groups in the two studies produced quantitatively very similar serial po-
sition curves but our controls produced a flatter serial position curve, it may be tempting to at-
tribute the difference between our conclusions and those of Carlesimo et al. to differences
between the two control groups. However, clearly, while cross-experiment comparison is typi-
cally frowned upon even when experimental conditions are identical, it is not valid here, when
the methodologies were different. What is most relevant to our inference is that the full pattern
is present in both groups, and that in CDFR the magnitude of the long-term recency effect in
patients was similar to that exhibited by their own, matched controls. Crucially, those authors
interpreted the reduced levels of free recall in the recency portion of the CDFR task as evidence
for a deficient long-term recency effect in amnesia. We were able to show that although pa-
tients had poorer memory for words from all serial positions in that task, there was no interac-
tion between serial position and group, suggesting that the long-term recency effect in amnesia
was equivalent to that of controls, concluding that this aspect of long-term memory was there-
fore intact in the patient group.
One potential caveat for the comparison between patients and controls in DFR and CDFR
was that patients performed more poorly on the distractor task than controls. This may have
influenced the amount of interference the two groups experienced, but from these data we can-
not tell whether patients suffered more interference (because they found the distractor task
more difficult) or less interference (because they solved fewer arithmetic problems). Notably,
the time both patients and controls invested in the distractor task was equivalent.
Clearly, the long-term recency effect in amnesia further discredits classical ‘strict’ dual-store
models, suggesting that arguments against these models can be made within the amnesic popu-
lation as well as in healthy participants. Both single-store and hybrid dual-store models can ac-
count for the long-term recency we observed here in both patients and neurologically intact
controls, and use interference-based mechanisms to do so. However, this finding has greater
theoretical significance for single- than dual- store and hybrid models of memory. Because re-
cency in IFR in amnesia is intact, single-store models are forced to predict intact recency in
CDFR in that group as well, namely, predict scale invariance of the recency effect. The intact
long-term recency that we demonstrated in amnesia therefore strongly supports these models.
By contrast, hybrid dual-store accounts assume memory operates differently in IFR and CDFR,
so our finding, while compatible with these models, does not challenge these models, nor does
it support them.
Single-store and hybrid dual-store models offer different accounts for the finding that pa-
tients’ memory levels only matched that of controls in IFR but not in CDFR. According to hy-
brid models [4, 18], in IFR, patients utilize their intact STM to recall late list items as effectively
as controls. Our analysis of the probability of first recall [25, 26, 30] helps single-store models
account for this finding. Strikingly, the qualitative difference in memory between patients and
controls across all serial positions in CDFR, apparent when all recall output was considered,
was eliminated when analysis was limited to the first recall attempt. We found that at the end of
the IFR and CDFR lists, the very last studied item was equally accessible for both patients and
controls despite the fact that in CDFR, an effective 30-second distractor interval preceded the
cue to begin recall. The impairment patients exhibited in recalling late serial positions in CDFR
was not present at the start of recall but emerged later in retrieval. We interpret these results ac-
cording to Sederberg et al.'s (2008) single-store, interference-theory model, an extension of the
Temporal Context Model [27]. It uses a specific representation of context as a retrieval cue, and
assumes that when an item is retrieved, its context is retrieved along with it, and that this re-
trieved context then becomes part of the next retrieval cue. Thus, at the start of free recall, the
only cue available is the current context. Current context would be quite similar to the context
learned along with list items in IFR, slightly less similar to studied items in CDFR, and least sim-
ilar to studied list items in DFR (all based on the ratio-rule-like assumption that the distractor
task simply acts to accelerate contextual drift). They then propose that amnesia might be under-
stood as impaired learning of new context-item associations, with an intact ability to use current
context as a retrieval cue. This kind of mechanism might explain the effects we observed: If cue-
ing with current list context is intact, then this should produce intact retrieval of the most recent
items in IFR, and an impairment for all earlier serial positions and for all serial positions in
both DFR and CDFR, since those conditions rely more on the use of retrieved context (via
item-context associations) as a retrieval cue. However, for the very first recall (corresponding to
our probability of first recall measure), current context is the only retrieval route available to
controls as well as to patients, so differences should not yet be apparent. For all subsequent out-
put positions, however, retrieved context would be expected to enhance control participants’
ability to retrieve additional items, a mechanism unavailable in amnesia.
The pattern of intact recency in probability of first recall and impaired recency in subse-
quent recalls is also compatible with the idea that differences in free recall in amnesia might be
largely accounted for by output interference effects. Numerous studies have suggested that peo-
ple with amnesia are more susceptible to various forms of interference than neurologically-in-
tact controls [37, 38, 41], and recent work suggests that cognitive tasks may produce more
retroactive interference in amnesia than in controls [39, 40]. It may be that our patients were
more distracted by their own responses than controls, and thus, their memory impairment was
not evident in the first recall, but was revealed as the recall phase unfolded. This kind of ac-
count could be integrated into a broad range of models of free recall, including both single-
and dual-store models.
One feature of our data was that people with amnesia had impaired primacy effects (i.e., a
reduced advantage in memory for the first few presented items), both when all recall positions
were considered and in the analysis of the first recalled position. Brown, Neath & Chater
(2007) argued that a reduced primacy effect in IFR in amnesia could be explained as resulting
from a failure to rehearse during presentation of the list. As this was not the focus of our study,
we do not comment further on this finding.
A caveat in interpreting the results presented here is that people with amnesia recalled very
few items in DFR and CDFR. This would not surprise any clinician working with these
patients; indeed, clinicians are more likely to be surprised by their intact first recall. However,
it is important to bear this floor effect in mind when examining our statistical findings.
We could not obtain proper structural neuroimaging data on many of the patients. For
those for whom such data were available, the lesions were not circumscribed to a single struc-
ture such as the hippocampus, consistent with the varied aetiologies of their disorder. Our find-
ings, therefore, speak only to the functional consequences of amnesia and not to its structural
correlates. The procedure we developed, however, can be used in the future to study a larger
sample of patients whose lesions are well documented and determine, thereby, whether the pat-
tern of preserved and deficient performance is associated with any particular lesion or is com-
mon across all amnesic syndromes.
Conclusion
People with amnesia clearly have some preserved ability to retrieve items from the long-term
store, as Warrington and Weiskrantz (1968) argued when they found that while the patients
were recalling the current list, there were intrusions from previous lists. This finding is impor-
tant because it suggests avenues to pursue in rehabilitation. Our finding suggests that this pre-
served ability likely obeys the rules described by single-store interference-based models, such
as the ratio rule, and confirms a key prediction of single-store models or memory, although it
does not contradict hybrid ‘modern’ dual-store models. The finding of intact recency and long-
term recency for the first item recalled on each list provides an important constraint on possi-
ble accounts of the memory deficit in amnesia.
Acknowledgments
We thank the participants who took part in this study for their effort and dedication and the
Memory Link programme at Baycrest.
Author Contributions
Conceived and designed the experiments: DT JC. Performed the experiments: DT. Analyzed
the data: DT JC MM BR. Wrote the paper: DT JC MM. Supported the adjusting of the method-
ology to the patient population: BR.
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