 |
 Previous Article | Next Article 
The Journal of Neuroscience, March 15, 2003, 23(6):2407
What Neural Correlates Underlie Successful Encoding and
Retrieval? A Functional Magnetic Resonance Imaging Study Using a
Divided Attention Paradigm
Elizabeth A.
Kensinger1,
Richard J.
Clarke1, and
Suzanne
Corkin1, 2
1 Department of Brain and Cognitive Sciences,
Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, and 2 Athinoula A. Martinos Center for Biomedical Imaging,
Charlestown, Massachusetts 02129
 |
ABSTRACT |
If attention is divided during learning, memory suffers.
Nevertheless, individuals can learn information with divided attention. This event-related functional magnetic resonance imaging (fMRI) study
(n = 17) investigated what neural processes support
(1) learning with divided attention and (2) retrieval of information learned with divided attention. Participants encoded words (Is the word
abstract or concrete?) while performing an auditory discrimination task
(press a button whenever an auditory pattern changes). The auditory
task was easy or hard, depending on the similarity of the patterns. A
behavioral study indicated that detailed ("recollective") information was more likely to be present for words encoded with the
easy versus the hard concurrent task. Words encoded with the hard
versus the easy concurrent task, in contrast, were more likely to rely
on less detailed ("familiarity"-based) information. fMRI revealed
encoding-related activation in the left prefrontal cortex (PFC) and
left hippocampus that was linked to successful memory formation only
for items encoded with the easy task. In contrast, activation in the
right PFC and left parahippocampal gyrus was linked to successful
memory for all items. Thus, successful encoding with the hard
concurrent task was supported by a subset of the regions recruited for
successful encoding with the easy task. The neural processes recruited
for successful retrieval also depended on the encoding condition: The
left PFC was disproportionately recruited for retrieval of items
encoded with the easy task, whereas the right PFC was
disproportionately recruited for retrieval of items encoded with the
hard task. These findings may reflect left-sided specialization for
recollective memories and right-sided specialization for
familiarity-based traces.
Key words:
divided attention; explicit memory; encoding; retrieval; dual task; neuroimaging; prefrontal cortex; human
| |
Introduction |
The term "divided attention"
refers to an experimental paradigm in which participants learn
information while performing a concurrent task that is easy (taking few
resources from the encoding operation) or hard (shifting resources from
the encoding operation). [We remain neutral as to whether the
divided attention manipulation at encoding taxes a general attention
system or a working memory system (or these two systems may be
equivalent).] Participants' memory is worse for items encoded with a
hard than with an easy secondary task (Baddeley, 1984 ; Craik et al.,
1996; Naveh-Benjamin et al., 2000a,b). Positron emission
tomography (PET) studies using a divided-attention paradigm found less
activation in regions of prefrontal cortex (PFC) with performance of a
hard secondary task versus an easy one (Shallice et al., 1994;
Fletcher et al., 1995, 1998; Anderson et al., 2000; Iidaka et
al., 2000). The PFC regions in which activation was affected are those
that have been linked to episodic encoding (Fletcher et al.,
1998; Wagner et al., 1998; Kirchhoff et al., 2000; Paller and
Wagner, 2002). These regions may have shown greater activation during
encoding with the easy versus the hard task because some
encoding-related processes were not performed with concurrent
performance of a hard secondary task (Shallice et al., 1994;
Fletcher et al., 1995; Iidaka et al., 2000).
Despite evidence that encoding processes are disrupted by divided
attention, individuals can successfully encode some information while
performing a hard secondary task. This finding raises the following
question: What neural substrates support successful memory formation
when resources for encoding are reduced (i.e., during concurrent
performance of a hard task)? [The requisite blocked design of PET
prevented investigation of this issue. The event-related functional
magnetic resonance imaging (fMRI) design of this study allows
correlation of single events during encoding with later retrieval, thus
providing a way to address this question.] One possibility is that the
same regions that are usually implicated in successful memory formation
(Brewer et al., 1998; Fernandez et al., 1999; Wagner et al., 1999;
Kirchhoff et al., 2000; Fernandez and Tendolkar, 2001; Otten and Rugg,
2001; Paller and Wagner, 2002) continue to support successful encoding
during performance of a hard concurrent task. An alternate option is
that only a subset of the regions that typically support successful
encoding continue to do so during performance of a hard task.
To understand why this second option could occur, consider that
individuals can form two kinds of memories: (1) vivid, detailed memories that they can "remember" or "recollect," or (2)
memories that lack detail and provide only a feeling that the item was presented (sense of "knowing" or "familiarity") (Mandler, 1980; Tulving, 1985; Jacoby, 1991; Gardiner and Java, 1993; Yonelinas, 2002).
Formation of vivid, "recollective" memories is thought to require
more attention than formation of less detailed traces; thus, divided
attention may disproportionately affect the encoding of detailed
memories (Yonelinas, 2001, 2002). [Shallice et al. (1994) and Fletcher
et al. (1995) have proposed that divided attention may disrupt the
ability to form explicit memories, while allowing formation of implicit
memories.] Activation in the subset of brain regions that allows less
detailed memory formation may relate to successful encoding even with
divided attention, whereas activation in regions that support detailed
memory formation may not.
If divided attention qualitatively alters the memories formed, then the
divided attention manipulation could affect not only the neural
processes recruited for successful memory formation but also those
recruited for successful retrieval. Retrieval of detailed, recollective
memories may rely more on the left PFC (Johnson et al., 1997; Nolde et
al., 1998a,b; Henson et al., 1999a,b; Rugg et al., 1999) and the
hippocampus (Eldridge et al., 2000; Davachi et al., 2001), while
retrieval of familiarity-based memories may rely on the right PFC
(Henson et al., 1999a,b; Eldridge et al., 2000) and the
parahippocampal gyrus (Strange et al., 2002; Davachi et al., 2003).
Therefore, we hypothesized that the left PFC and left hippocampus would
be disproportionately recruited for retrieval of words encoded with the
easy concurrent task, whereas the right PFC and left parahippocampal
gyrus would be disproportionately recruited during retrieval of words
encoded with the hard concurrent task.
| |
Materials and Methods |
Behavioral companion study
To confirm that the difficulty of the secondary task at encoding
affected the amount of detail that could be retrieved, we conducted a
behavioral study outside of the scanning environment.
Participants. Participants in this experiment comprised 24 young adults (12 women). They were matched to participants in the imaging study by age (20-35 years of age; mean, 26.4) and education level (14-18 years; mean, 16.3).
Encoding. The stimuli were 480 words, with written
frequencies ranging from 10 to 100 (Kucera and Francis, 1967). They
were presented one at a time in Geneva 48 point font, using MacStim (David Darby, WhiteAnt Occasional Publishing, West Melbourne, Victoria,
Australia). Stimulus words were divided into four encoding runs, each
with 120 words.
Participants completed two encoding tasks, each followed by a retrieval
task. In the encoding task, participants saw words for 2 sec each and
rated each word as abstract or concrete by pressing a button with their
right middle or ring finger, respectively. Because we wanted the
behavioral encoding task to be identical to that performed in the
scanner, fixation crosses were interspersed pseudorandomly between the
words. Participants made no response when fixation occurred.
In addition to making the abstract-concrete decisions, participants
simultaneously performed an auditory discrimination task. For this
task, 1.5 sec auditory patterns (created using Sound Edit; MacroMedia,
Inc., San Francisco, CA) were presented continuously as people
rated words and also when they viewed the fixation crosses. The
participants' task was to listen to these patterns and to press a
button with their left index finger every time a sound pattern changed
from pattern A to pattern B (or from B to A). The difficulty of the
auditory discrimination task was related to the similarity of auditory
patterns A and B. In the easy version of the task, the two auditory
patterns were rhythmically distinct and thus easy to discriminate. In
the hard version, the patterns were rhythmically similar and hard to
discriminate. Participants were given an instructional cue as to
whether the secondary task would be easy or hard, and that task version
continued for 30 sec, until the next instructional cue (Fig.
1).
View larger version (25K):
[in this window]
[in a new window]
|
Figure 1.
The instruction frame and first 8 sec of a
representative encoding pseudoblock. A 2 sec instruction frame
indicated the encoding task (classify words as abstract or concrete)
and difficulty of the auditory discrimination task (easy or hard).
Words were presented for 2 sec each and were pseudorandomly intermixed
with fixation crosses. Sound patterns played throughout the
pseudoblock, and participants pressed a button when they noted that the
sound pattern changed (e.g., from pattern A to pattern B).
|
|
Retrieval. After each of the encoding tasks, participants
performed a recognition task with 72 previously presented words and 48 nonpresented words. Pilot data suggested that with this breakdown,
participants responded that approximately one-half of the stimuli were
presented previously. Participants were asked to indicate via button
press whether they (1) "remembered" the word from the encoding
list, (2) "knew" the word was presented previously, or (3) thought
the word was "new" (nonpresented). A "remember" response
indicated that participants had a vivid memory of the presented item,
whereas a "know" response indicated that participants lacked a
specific memory of the presentation of the item but sensed that it had
been presented recently (Tulving, 1985; Jacoby, 1991).
Data analysis. Data were analyzed in two ways. First, we
calculated the corrected recognition scores (percentage of remember hits  percentage of remember false alarms or percentage of know hits percentage of know false alarms). Second, we computed
recollection and familiarity scores as suggested by Yonelinas et al.
(1998). These scores take into account the fact that the probability of making a know response to a presented word is constrained by the number
of remember responses made to presented words, because participants
were instructed to give a know response to items that are familiar and
not recollected. Analyses consisted of repeated-measures ANOVA with
secondary task type (easy, hard) and memory strength (remember, know;
recollection, familiarity) as within-subject factors, and subsequent
t tests. All reported p values are
two-tailed.
fMRI study
Having confirmed in the behavioral study that the manipulation
of secondary task difficulty affected overall memory as well as the
richness of the memory traces formed, we then examined what effect this
manipulation of secondary task difficulty would have on the neural
processes underlying successful encoding and retrieval.
Participants. The participants comprised 22 right-handed,
native English speakers. Five participants were excluded because of
scanner malfunction (one man, one woman), sound presentation failure
(one man), or excessive head movement (one man, one woman). The
remaining 17 participants (nine men, eight women) were 20-35 years of
age (mean age, 26.1) with 14-18 years of education (mean, 16.0 years).
Participants were screened to exclude those with any history of
neurological or psychiatric disorder, and no participants were taking
centrally acting medications.
General methods. Before entering the scanner, participants
performed a practice encoding and retrieval run. Once in the scanner, they completed an additional short practice run to allow
familiarization with the presentation of the sound patterns via
headphones. Participants were scanned during three encoding and three
retrieval runs.
Encoding. The encoding task was identical to that described
in the behavioral study. Each encoding run included 12 30 sec pseudoblocks; each pseudoblock consisted of 10 words, each presented for 2 sec. The times of the word onsets were jittered with fixation crosses to allow for optimal accuracy and efficiency of estimation of
the hemodynamic response to each stimulus (Dale et al., 1999). We used
the optseq program (part of the FS-FAST analysis tools; http://surfer.nmr.mgh.harvard.edu/optseq, written by D. Greve, Charlestown, MA), which determines stimulus optimization (i.e., the optimal word onsets) given the repetition time (TR), number of
event types, time per event type, and number of acquisitions. A
description of the calculations used in the development and implementation of this stimulus optimization program can be found in
previous publications (Burock et al., 1998; Dale, 1999).
Although task type was blocked (i.e., participants performed either the
hard distractor task or the easy distractor task for 30 sec periods),
we could still resolve the hemodynamic response associated with each
individual item because the items were jittered with fixation (Burock
et al., 1998; Dale, 1999). Therefore, the analysis of the data was
event-related.
Retrieval. A recognition run followed each encoding run.
Each recognition run included 120 words, with 60 fixation points pseudorandomly intermixed to provide jitter. Across the recognition runs, 108 words had been encoded in the easy discrimination condition (one-half retrieved in the hard condition; one-half retrieved in the
easy condition); 108 had been encoded in the hard discrimination condition (one-half retrieved in the hard condition; one-half retrieved
in the easy condition); and 144 new words were pseudorandomly intermixed (one-half in the easy condition). The order of the encoding-recognition runs was counterbalanced across the participants.
Control experiment. In a control experiment, nine young
adults (six males, 18-30 years of age) performed only the auditory discrimination task (without the encoding or retrieval tasks). As in
the main experiment, an instructional cue informed the participants whether the task would be easy or hard, and the tasks were presented in
30 sec blocks. In addition, there was a "no task" condition, which
served as the baseline. Throughout all task conditions, participants
viewed a fixation cross on the screen in addition to monitoring the
sound patterns. The critical comparison was between the hard task and
the easy task conditions.
Scanning protocols. Imaging was performed on a
Siemens (Erlangen, Germany) Allegra 3 Tesla head-only MRI
scanner with a 36 cm inner diameter asymmetric gradient coil. Head
motion was minimized using pillows and foam padding around the head.
For each participant, 2 magnetization-prepared rapid acquisition
gradient echo structural scans optimized for gray/white contrast
were collected to provide detailed anatomical information. After the
structural scans, a series of echoplanar functional scans was collected
to provide images sensitive to blood oxygen level-dependent
(BOLD) contrast. Functional T2*-weighted images were acquired
using a single-shot echoplanar sequence (tau, 25 msec; echo
time, 30 msec; TR, 2000 msec; 3.13 mm in-plane resolution; 5 mm
slice thickness; no skip). Slices were aligned along the anterior
commisure/ posterior commisure line. Each scan lasted 6 min and 24 sec, during which 92 images were acquired in an interleaved
manner for each of 22 axial slices.
Data analysis. Data were motion corrected using the Analysis
of Functional Neuroimages motion correction algorithm (Cox and Jesmanowicz, 1999). We excluded participants whose motion exceeded two
functional voxels. We conducted analyses both with and without global
signal intensity normalization. The results did not differ qualitatively; we therefore report the normalized data here.
We used selective averaging and deconvolution of the BOLD signal. The
BOLD signal was modeled as a linear combination of hemodynamic responses, offset, and trend embedded in Gaussian nose (Boynton et al.,
1996; Dale and Buckner, 1997; Dale, 1999). The hemodynamic response to
a particular stimulus type was modeled as a sum of  functions
over a fixed time window phase-locked to the presentation of the
stimulus. No response shape for this function was assumed, but it was
assumed that the response to a particular stimulus type was the same
for every presentation of that stimulus type, and that the overlap of
temporally adjacent responses was linear. This signal model was
inverted to obtain the average hemodynamic response to each stimulus as
if that stimulus were presented in isolation, allowing for the
resolution of individual events (Boynton et al., 1996; Dale et al.,
1997; Dale, 1999).
Effects for each condition were estimated using a participant-specific,
fixed-effects model. The participant-specific effects from each of
these contrasts were entered into a second-level group analysis
treating participants as a random effect. Regions were considered
reliable if they consisted of at least five contiguous voxels that
exceeded a threshold of p < 0.001 (uncorrected).
Regions of interest (ROI) were defined functionally based on the
contrasts of all encoding versus baseline or all retrieval versus
baseline. The defined ROIs were therefore unbiased with respect to the
contrast of interest (easy vs hard concurrent task; remembered vs
forgotten). ROI analyses examined whether there was a reliable
condition (e.g., words remembered, words forgotten) by time (0-14 sec)
interaction. Time represented the time course of the signal change;
thus, an interaction between condition and time indicated that the
signal change differed based on condition during a specific part of the
time course (i.e., the interaction indicated that the condition effect
was not related to a nonspecific elevated signal change). Planned
contrasts also examined whether the peak percentage signal change
(across 2 sec time points, compared with the fixation-sound baseline)
differed for two conditions (e.g., remembered, forgotten or easy, hard).
We resampled the functional data into standardized space (Spherical,
Talairach) to allow averaging of group data. Automatic spherical
resampling (Dale et al., 1999; Fischl et al., 1999, 2001) examined the
effect of condition on cortical activation for the group. Automatic
Talairach resampling using the Montreal Neurological Institute
atlas (Mazziotta et al., 1995) examined the effect of condition (e.g.,
hard versus easy encoding) on subcortical activation for the group of
participants. All group data were analyzed using random-effects
analyses (Friston et al., 1999).
| |
Results |
Behavioral companion study
Table 1 shows remember scores and
know scores for each of the conditions. All scores were corrected for
false alarm rate (percentage of hits percentage of false
alarms). Repeated-measures ANOVA, calculated either on the raw remember
and know scores or on the computed recollection and familiarity scores
(Yonelinas et al., 1998), indicated a significant effect of encoding
difficulty (F(1,23) = 6.4;
p < 0.01) and an interaction between memory strength (remember vs know or recollection vs familiarity) and encoding difficulty (F(1,23) = 6.4;
p < 0.01).
View this table:
[in this window]
[in a new window]
|
Table 1.
Corrected recognition performance as a function of encoding
condition in the behavioral companion study (mean, SD)
|
|
The results of this behavioral companion study confirmed that the hard
auditory task at encoding altered the type of memory trace formed.
Items encoded with the hard auditory task were recognized by only a
sense of previous encounter (know response) more frequently than items
encoded with the easy auditory task. Items encoded with the easy
auditory task, in contrast, were recognized based on detailed
information about the presentation of the item (remember response) more
frequently than were items encoded with the hard auditory task.
fMRI study
Behavioral performance
Accuracy. The presence of the hard secondary task at
encoding led to poorer memory than did the presence of the easy
secondary task (t = 5.1; p < 0.01). In
contrast, the difficulty of the secondary task at retrieval did not
affect memory performance (p > 0.1). Repeated-measures ANOVA indicated no effect of memory process (encoding, retrieval) (F(1,16) = 0.10;
p > 0.3), a significant effect of task difficulty
(F(1,16) = 4.42; p < 0.01) on memory performance, and a significant task difficulty by
memory process interaction (F(1,16) = 5.25; p < 0.01), indicating that the difficulty manipulation had a greater effect at encoding than at retrieval (Table
2). These results are consistent with the
findings of numerous behavioral studies (Craik et al., 1996, 2000;
Naveh-Benjamin et al., 1998; Naveh-Benjamin and Guez, 2000) and are
consistent with the performance we found on this task in a behavioral
pilot study.
View this table:
[in this window]
[in a new window]
|
Table 2.
Mean corrected (percentage of hits percentage of
false alarms) recognition performance (SD) as a function of secondary
task difficulty and memory process
|
|
Reaction times for noting sound pattern changes. A
comparison of reaction times for the two auditory discrimination
conditions indicated that participants were slower to respond to
auditory pattern changes when the discrimination was hard than when it was easy (Table 3)
(F(1,16) = 733.32; p < 0.0001). Participants were slower at indicating the sound pattern
change (regardless of auditory task difficulty) when it occurred at
retrieval than at encoding (F(1,16) = 6.64; p < 0.01), but there was no interaction between
task difficulty and memory process
(F(1,16) = 0.91; p > 0.2), indicating that the increased time to respond to the hard versus
the easy auditory pattern changes was similar at encoding and
retrieval. These results are also consistent with those of previous
behavioral studies, as well as the performance of participants on this
task when assessed outside of the scanner.
View this table:
[in this window]
[in a new window]
|
Table 3.
Reaction times (in milliseconds) to the change in sound
patterns as a function of secondary task difficulty and memory process
(mean, SD)
|
|
Reaction times for rating words as abstract/concrete or
old/new. Participants' reaction times for rating the words as
abstract or concrete were not affected by the difficulty of the
auditory discrimination task at encoding, nor were the reaction times
for making old or new decisions at retrieval affected by secondary task
difficulty (Table 4). Repeated-measures
ANOVA revealed no effect of task difficulty at encoding or at retrieval
and no interaction between encoding difficulty and retrieval
difficulty.
View this table:
[in this window]
[in a new window]
|
Table 4.
Reaction times (in milliseconds) to retrieve words as a
function of secondary task difficulty at encoding and retrieval (mean,
SD)
|
|
fMRI results: encoding
We first conducted voxel-based statistical analyses, which
revealed the voxels of the brain that showed condition-related activity
above a threshold of p < 0.001. These analyses
revealed that encoding with either the easy or the hard distractor task (compared with baseline) elicited activation in occipital, parietal, and frontal regions bilaterally, and in the left medial temporal lobe
(MTL). Interestingly, the regions recruited were similar regardless of
the difficulty of the secondary task: In a direct contrast of encoding
with the hard distractor task versus encoding with the easy distractor
task, we found no evidence of additional neural circuits that were
recruited to coordinate performance of the encoding task with
performance of the more difficult auditory task. Even with the
threshold dropped to p < 0.05, the same occipital, parietal, and frontal regions were
recruited in both tasks (Tables 5 and 6).
These results are in contrast to the view that increasing task
coordination demands require bringing on-line additional neural
resources (D'Esposito et al., 1995) and instead suggest that the
demands required for a more difficult task coordination can be met by
the same regions active during a less demanding task coordination
condition (see also Adcock et al., 2000; Bunge et al., 2001).
View this table:
[in this window]
[in a new window]
|
Table 5.
Brain regions showing significantly more activation during
encoding with the easy task than during baseline
|
|
View this table:
[in this window]
[in a new window]
|
Table 6.
Brain regions showing significantly more activation during
encoding with the hard task than during baseline
|
|
We then conducted ROI analyses that further examined activation related
to task difficulty (within regions active during encoding with
both tasks). These analyses indicated that the magnitude of responses
(maximum signal change) in the left inferior and left superior frontal
regions were greater during encoding with the easy compared with the hard auditory task (Table 7, Fig. 2).
View this table:
[in this window]
[in a new window]
|
Table 7.
Brain regions showing significantly more activation during
encoding with the easy task than during encoding with the hard task
|
|
View larger version (132K):
[in this window]
[in a new window]
|
Figure 2.
Effect of auditory task difficulty on activation
at encoding. A region of left ventrolateral PFC (BA 44) showed a
smaller peak percentage signal change during encoding with the hard
task (2.1) than with the easy task (2.5; p < 0.001).
|
|
These results indicate that regions associated with encoding, including
a region of the left ventrolateral PFC [Brodmann area (BA) 44;
Talairach coordinate: 48, 19, 25], showed less activation during
concurrent performance of the hard task than during concurrent performance of the easy task. These data are in general agreement with
the results of previous PET studies of divided attention (Shallice et al., 1994; Fletcher et al., 1995, 1998; Anderson et
al., 2000; Iidaka et al., 2000), and suggest that some encoding processes were not being performed effectively during encoding with the
hard auditory task.
To assure that this difference was attributable to differences in the
encoding processes rather than to differences in the neural processes
recruited for the auditory discrimination task, we conducted a control
experiment in which nine participants performed only the auditory
discrimination tasks. Voxel-based and ROI analyses indicated no
modulation in the PFC or the MTL as a function of the difficulty of the
secondary task. The only regions that showed significant modulation
(p < 0.01, uncorrected) were the anterior cingulate gyrus (BA 31) and primary auditory cortex (BA 41, 42); these
regions showed greater activation during performance of the hard task
than the easy task.
The finding that the PFC reductions in activation were not related
solely to the difficulty of the secondary task supports our hypothesis,
and that proposed by previous researchers (Shallice et al., 1994;
Fletcher et al., 1995; Iidaka et al., 2000), that the reductions in
activation stem from differences in encoding processes performed with
the two secondary tasks. What, then, are the neural processes that
support successful encoding with the hard task and the easy task?
Functional MRI results: subsequent memory
To address this question, we conducted analyses of subsequent
memory (as in Brewer et al., 1998; Fernandez et al., 1999; Wagner et
al., 1999; Kirchhoff et al., 2000; Otten and Donchin, 2000; Davachi et
al., 2001; Otten and Rugg, 2001). ROIs defined from the contrast of all
encoding trials versus baseline indicated four regions that showed
subsequent memory effects (i.e., greater signal change for subsequently
remembered items than for subsequently forgotten items): two areas in
the PFC [one in the left inferior PFC (BA 45/47) (Fig.
3A), and one in the right
inferior PFC (BA 45) (Fig. 3B)] and two regions of the MTL
[the anterior left hippocampus (Fig.
4A) and the left
inferior middle parahippocampal gyrus (Fig. 4B)]. In
previous studies, activation in these regions, particularly the left
PFC and MTL areas, also predicted subsequent memory (Wagner et al.,
1999; Kirchhoff et al., 2000; Otten and Rugg, 2001; Davachi and Wagner,
2002; for review, see Paller and Wagner, 2002).
View larger version (77K):
[in this window]
[in a new window]
|
Figure 3.
PFC activation at encoding related to
retrieval success: Two regions showed activation related to subsequent
memory. The left inferior PFC (BA 45/47; A) showed this
effect only for items encoded with the easy task; the right inferior
PFC (BA 45; B) showed the relationship for items encoded
with either the easy or the hard task.
|
|
View larger version (84K):
[in this window]
[in a new window]
|
Figure 4.
MTL activation at encoding relative to retrieval
success. Two regions showed activation related to subsequent memory
retrieval. The left anterior hippocampus (A)
showed the effect only for items encoded with the easy task, whereas
the left parahippocampal gyrus (B) showed the
relationship for items encoded with either task. R,
Right; L, left.
|
|
We then analyzed the activation in these ROIs to examine whether it was
related to successful encoding (i.e., subsequent correct recognition)
for items encoded with the easy and the hard auditory task, or only for
items encoded in one of these conditions. The peak percentage of signal
change (relative to baseline) in the left inferior PFC region (BA 45 and 47) predicted successful retrieval only for items encoded with the
easy auditory task (Fig. 3A). Activation in this region did
not differ for subsequently remembered versus forgotten items encoded
with the hard auditory task. The findings were different for the area
in the right inferior PFC (BA 45) (Fig. 3B). Here,
activation predicted subsequent memory for items encoded with the easy
task as well as for items encoded with the hard task.
Within the MTL, left anterior hippocampal activation (Fig.
4A) correlated with subsequent retrieval success only
for items encoded with the easy task. In contrast, activation in
the left inferior middle parahippocampal gyrus (Fig.
4B) predicted retrieval success for items encoded
with either the easy or the hard task.
The results of the subsequent memory analyses indicated that the locus
of signal change at encoding that predicted retrieval success for items
encoded with the hard task comprised a subset of the areas in which
activation changes predicted retrieval success for items encoded with
the easy task. These data, together with the finding from the
behavioral study that participants did not encode as much detailed
information with the hard task, suggest that the formation of detailed,
recollective memories depends on the left inferior PFC and left
anterior hippocampus.
fMRI results: effects of encoding condition on regions recruited
during successful retrieval
If, as the behavioral companion study and subsequent memory
analyses suggested, participants formed qualitatively different types
of memories for items encoded with the hard compared with the easy
auditory task, it is possible that different brain regions were brought
on-line during the retrieval of these traces.
Successful retrieval: ROI analyses
To address this issue, we defined ROIs based on the contrast of
all retrieval (easy and hard) versus baseline. We then examined which
of those regions showed greater activation during correct retrieval
compared with incorrect retrieval. Four brain regions met this
criterion. One region in the right inferior PFC (BA 44) (Fig.
5A) showed greater activation
during retrieval of words encoded with the hard task compared with
retrieval of words encoded with the easy task. This finding, together
with the behavioral companion study data showing that memory traces
lacking in detail occurred more frequently for items encoded with the
hard versus the easy task, implicates the right inferior PFC as a
component of the substrate for the sense of knowing or familiarity.
View larger version (97K):
[in this window]
[in a new window]
|
Figure 5.
Prefrontal activation during successful retrieval
related to encoding difficulty: A right inferior PFC region (BA 44;
Talairach coordinate: 43, 17, 24; A) showed greater
activation during correct retrieval of words encoded with the hard task
(1.5) compared with the easy task (1.2). In contrast, two regions of
the left PFC (BA 45; Talairach coordinate: 38, 28, 2;
B) and BA 9/44; Talairach coordinate: 41, 13, 25;
C) showed a greater percentage of signal change
during retrieval of items encoded with the easy versus the hard task
(1.0 and 0.75, respectively, for region B, and 1.6 and 1.3, respectively, for region C; p < 0.001).
|
|
Two regions in the left PFC (BA 45 and BA 9 and 44) (Fig.
5B,C) showed the opposite pattern: greater activation during
retrieval of words encoded with the easy task. This result, together
with the behavioral result that participants retrieved detailed
memories more frequently for items encoded with the easy versus the
hard task, identifies left PFC regions as part of the circuit
underlying retrieval of detailed, recollective memories.
We also found one region in the left anterior hippocampus that showed
greater activation during the retrieval of words encoded with the easy
versus the hard task (Fig. 6). This
finding is consistent with recent literature (Aggleton and Brown, 1999;
Eldridge et al., 2000; Brown and Aggleton, 2001; Davachi et al.,
2001; Strange et al., 2002) indicating that the hippocampus
specifically supports in the retrieval of recollective, but not
familiarity-based, memories. Despite recent claims that the
parahippocampal gyrus is activated above baseline during retrieval of
familiarity-based memories (Davachi et al., 2001; Yonelinas et al.,
2001; Strange et al., 2002), we found no parahippocampal activation
during retrieval.
View larger version (181K):
[in this window]
[in a new window]
|
Figure 6.
MTL activation during successful retrieval related
to encoding difficulty. The left anterior hippocampus showed modulation
similar to that seen for the left prefrontal regions: a greater
percentage of signal change during retrieval of items encoded with the
easy (0.57) than with the hard (0.17) task
(p < 0.001). R, Right;
L, left.
|
|
| |
Discussion |
The motivation for this study was the finding that although neural
activation during encoding was reduced by divided attention (Shallice
et al., 1994; Fletcher et al., 1995; Iidaka et al., 2000), individuals
can, nevertheless, learn information when their attention is divided.
The event-related design of this study allowed us to assess which brain
regions support successful memory formation (i.e., successful encoding)
when participants performed a hard or an easy secondary task. We also
investigated whether the regions recruited for successful retrieval of
information differed depending on whether that information had been
learned with the hard task (favoring familiarity) or with the easy task
(favoring recollection) at encoding.
Before addressing these two questions, we asked whether our
divided-attention manipulation, like those used in previous PET studies
(Shallice et al., 1994; Fletcher et al., 1995; Anderson et al., 2000;
Iidaka et al., 2000), resulted in reductions in activation in regions
implicated in episodic encoding. Consistent with previous PET studies,
we found that encoding with the hard versus the easy distractor task
reduced the activation in various PFC regions, including a region in
the left ventrolateral PFC believed to play a role in maintenance of
verbal information (Poldrack et al., 1999).
Like previous researchers (Shallice et al., 1994; Fletcher et al.,
1995; Iidaka et al., 2000), we interpreted this reduction in activation
as reflecting a degradation of encoding processes when participants
performed the hard concurrent task. This view is consistent with the
behavioral companion study reported here, and with extensive behavioral
evidence that divided attention at encoding reduces the probability of
successful retrieval (Craik et al., 1996; Naveh-Benjamin et al.,
2000a,b), and in particular, reduces the ability to form rich,
recollective memories (Yonelinas, 2001). It is also possible that
encoding items with a hard secondary task reduces the explicit memory
traces formed, forcing increased reliance on neural substrates
supporting implicit memory formation (Shallice et al., 1994; Fletcher
et al., 1995).
The convergence of our results using a constrained encoding task (i.e.,
"Decide whether each word is abstract or concrete") with those of
previous PET studies using unconstrained encoding tasks (e.g., "Learn
these word pairs") and cued recall (e.g., providing the first word of
a word pair), suggests that the functional neuroimaging results
generalize to a range of intentional encoding tasks. It will be worth
examining in future studies whether this effect also generalizes to
incidental encoding tasks (i.e., when participants are not aware that a
memory task will follow).
What brain regions support successful memory formation?
We then investigated what brain regions supported successful
encoding (i.e., encoding of items that participants later recognized correctly) in the hard task and the easy task. Previous research on
encoding with full attention showed a relationship between successful
encoding and magnitude of activation in the left PFC (Johnson et al.,
1997; Wagner et al., 1999), hippocampus, and parahippocampal gyrus
(Brewer et al., 1998; Fernandez et al., 1999; Wagner et al., 1999;
Kirchhoff et al., 2000). Our results converge with these findings: The
bilateral inferior PFC (left BA 45/47, right BA 45), the left anterior
hippocampus, and the left inferior middle parahippocampal gyrus all
showed subsequent memory effects for items encoded with the easy task.
Only a subset of these regions (right inferior PFC and left
parahippocampal gyrus), however, related to subsequent memory for items
encoded with the hard task. The regions that no longer supported
successful encoding are regions that appear to be tied to the formation
of detailed, recollective memories (Davachi et al., 2001; Strange et
al., 2002), whereas the regions that continued to support successful encoding even with the concurrent hard secondary task are those that
have been linked to formation of less detailed memories that evoke a
"sense of knowing" or familiarity (Davachi et al., 2001; Strange et
al., 2002). Our fMRI results, therefore, are consistent with the
behavioral evidence presented here: Participants are more likely to
form detailed memories for items encoded with the easy task than with
the hard task.
What brain regions support successful retrieval?
We hypothesized that brain activation at retrieval could differ
when retrieving qualitatively different memory traces (i.e., for
detailed memories encoded with the easy task vs less detailed memories
encoded with the hard task). Consistent with this hypothesis, we found
a dissociation between the regions used to retrieve items encoded with
the easy and with the hard task. In particular, we found greater
activation in left PFC regions (BA 45; BA 9/44) for correctly retrieved
items that had been encoded with the easy compared with the hard task,
and greater activation in a right PFC (BA 44) region for items that had
been encoded with the hard compared with the easy task. These
laterality effects are consistent with recent neuroimaging studies
suggesting that right-sided regions may be recruited when individuals
are asked to make recognition judgments based on familiarity (Henson et
al., 1999a,b, 2000; Dobbins et al., 2003), as may occur when
memory traces are not detailed and include only familiarity
information. In contrast, left-sided regions appear more important for
retrieval of memories with rich detail (Johnson et al., 1997; Nolde et
al., 1998a,b; Rugg et al., 1999; Ranganath et al., 2000).
A question has remained about whether these laterality effects
represent differences in retrieval orientation (i.e., whether participants are attempting to retrieve or to monitor for detailed information or familiarity information) or differences in retrieval success (i.e., whether the products of the retrieval effort include recollective information or familiarity information). Our data support
the interpretation that the laterality effects are based on differences
in retrieval success. The retrieval scans intermixed items that had
been encoded with the easy and hard tasks; thus, participants did not
know the condition under which specific items had been encoded.
Therefore, it is difficult to imagine that participants adopted
different retrieval strategies for words encoded with the different
tasks. It seems more plausible that the observed laterality effects
were based on the qualitative nature of the memory trace that was
retrieved (i.e., the amount of detail present). In other words, these
results suggest that when different types of memory traces are formed
at encoding [e.g., recollective vs familiarity-based or explicit vs
implicit, as proposed by Fletcher et al. (1995) and Shallice et al.
(1994)], different brain regions may be brought on-line later to allow
the successful retrieval of those items.
It is unclear why these laterality effects occur: It is possible that
right PFC regions are used during postretrieval monitoring, and thus
are more critical for items with weaker traces, where they are closer
to the boundary between what a person will accept as old versus assign
as new (Henson et al., 2001; Yonelinas, 2002). Right prefrontal
specialization is also found in studies of novelty (Menon et al.,
2000), and a familiarity-based signal may be similar to that required
for determining whether an object is novel. The left-sided activation
found in the present study could result from semantic processing of the
words; however, even studies with nonverbal stimuli have found
left-sided prefrontal activation during retrieval of detailed
information (Ranganath et al., 2000).
Conclusion
Using a divided-attention paradigm, we found that participants'
memories of words encoded with a easy secondary task were more detailed
(recollective) than those encoded with a hard task. A greater
proportion of the words encoded with the hard task than the easy task
relied on a less detailed sense of knowing or familiarity. fMRI
indicated that encoding with the hard task showed less activation in
PFC regions associated with episodic memory formation than encoding
with the easy task. Only a subset of the brain regions that supported
successful encoding with an easy secondary task continued to do so when
encoding occurred with a hard secondary task. Activation in the left
inferior PFC and the left anterior hippocampus predicted retrieval
success only for items encoded with the easy task, whereas activation
in the right inferior PFC and left inferior middle parahippocampal
region predicted retrieval success for all items. Divided attention at
encoding also affected the neural processes recruited for successful
retrieval: We found a dissociation between brain regions preferentially
used to retrieve items encoded with the easy task (left PFC and left
anterior hippocampus) and those encoded with the hard task (right PFC).
These results suggest that the brain regions that support successful
encoding and successful retrieval vary depending on the detail of the
memory trace. Familiarity-based traces lacking in detail may rely on right-sided PFC, whereas recollective traces that are rich in detail
may rely more on left-sided PFC and the hippocampus.
| |
FOOTNOTES |
Received Sept. 4, 2002; revised Dec. 3, 2002; accepted Dec. 27, 2002.
This work was supported by National Institutes of Health Grant AG14432,
the National Science Foundation, and a Howard Hughes Medical Institute
Predoctoral Fellowship (E.A.K.)
Correspondence should be addressed to Elizabeth A. Kensinger, NE20-392,
77 Massachusetts Avenue, Cambridge, MA 02139. E-mail: ekensing{at}mit.edu.
| |
References |
-
Adcock R,
Constable R,
Gore J,
Goldman-Rakic P
(2000)
Functional neuroanatomy of executive processes involved in dual-task performance.
Proc Natl Acad Sci USA
97:3567-3572[Abstract/Free Full Text].
-
Aggleton JP,
Brown MW
(1999)
Episodic memory, amnesia, and the hippocampal-anterior thalamic axis.
Behav Brain Sci
22:425-489[Web of Science][Medline].
-
Anderson ND,
Iidaka T,
Cabeza R,
Kapur S,
McIntosh AR,
Craik FI
(2000)
The effects of divided attention on encoding- and retrieval-related brain activity: a PET study of younger and older adults.
J Cogn Neurosci
12:775-792[Web of Science][Medline].
-
Baddeley A
(1984)
Attention and retrieval from long-term memory.
J Exp Psychol Gen
113:518-540[Web of Science].
-
Boynton GM,
Engel SA,
Glover GH,
Heeger DJ
(1996)
Linear systems analysis of functional magnetic resonance imaging in human V1.
J Neurosci
16:4207-4221[Abstract/Free Full Text].
-
Brewer JB,
Zhao Z,
Desmond JE,
Glover GH,
Gabrieli JD
(1998)
Making memories: brain activity that predicts how well visual experience will be remembered.
Science
281:1185-1187[Abstract/Free Full Text].
-
Brown MW,
Aggleton JP
(2001)
Recognition memory: what are the roles of the perirhinal cortex and hippocampus?
Nat Rev Neurosci
2:51-61[Web of Science][Medline].
-
Bunge SA,
Ochsner KN,
Desmond JE,
Glover GH,
Gabrieli JD
(2001)
Prefrontal regions involved in keeping information in and out of mind.
Brain
124:2074-2086[Abstract/Free Full Text].
-
Burock MA,
Buckner RL,
Woldorff MG,
Rosen BR,
Dale AM
(1998)
Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI.
NeuroReport
9:3735-3739[Web of Science][Medline].
-
Cox RW,
Jesmanowicz A
(1999)
Real-time 3D image registration for functional MRI.
Magn Reson Med
42:1014-1018[Web of Science][Medline].
-
Craik FI,
Govoni R,
Naveh-Benjamin M,
Anderson ND
(1996)
The effects of divided attention on encoding and retrieval processes in human memory.
J Exp Psychol Gen
125:159-180[Web of Science][Medline].
-
Craik FI,
Naveh-Benjamin M,
Ishaik G,
Anderson ND
(2000)
Divided attention during encoding and retrieval: differential control effects?
J Exp Psychol Learn Mem Cogn
26:1744-1749[Web of Science][Medline].
-
Dale AM
(1999)
Optimal experimental design for event-related fMRI.
Hum Brain Mapp
8:109-114[Web of Science][Medline].
-
Dale AM,
Buckner RL
(1997)
Selective averaging of rapidly presented individual trials using fMRI.
Hum Brain Mapp
5:329-340[Web of Science].
-
Dale A,
Greve D,
Burock M
(1999)
Optimal stimulus sequences for event-related fMRI.
Hum Brain Mapp
5:329-340.
-
Davachi L,
Wagner AD
(2002)
Hippocampal contributions to episodic encoding: insights from relational and item-based learning.
J Neurophysiol
88:982-990[Abstract/Free Full Text].
-
Davachi L,
Maril A,
Wagner AD
(2001)
When keeping in mind supports later bringing to mind: neural markers of phonological rehearsal predict subsequent remembering.
J Cogn Neurosci
13:1059-1070[Web of Science][Medline].
-
Davachi L,
Mitchell JP,
Wagner AD
(2003)
Multiple routes to memory: distinct medial temporal lobe processes build item and source memories.
Proc Natl Acad Sci USA
100:2157-2162[Abstract/Free Full Text].
-
D'Esposito M,
Detre JA,
Alsop DC,
Shin RK,
Atlas S,
Grossman M
(1995)
The neural basis of the central executive system of working memory.
Nature
378:279-281[Medline].
-
Dobbins IG,
Rice HJ,
Wagner AD,
Schacter DL
(2003)
Retrieval orientation and success: separable neurocognitive components underlying episodic recognition.
Neuropsychologia
41:318-333[Web of Science][Medline].
-
Eldridge LL,
Knowlton BJ,
Furmanski CS,
Bookheimer SY,
Engel SA
(2000)
Remembering episodes: a selective role for the hippocampus during retrieval.
Nat Neurosci
3:1149-1152[Web of Science][Medline].
-
Fernandez G,
Tendolkar I
(2001)
Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level.
Brain Res Bull
55:1-9[Web of Science][Medline].
-
Fernandez G,
Effern A,
Grunwald T,
Pezer N,
Lehnertz K,
Dumpelmann M,
Van Roost D,
Elger CE
(1999)
Real-time tracking of memory formation in the human rhinal cortex and hippocampus.
Science
285:1582-1585[Abstract/Free Full Text].
-
Fischl B,
Sereno MI,
Dale AM
(1999)
Cortical surface-based analysis. II. Inflation, flattening, and a surface-based coordinate system.
NeuroImage
9:195-207[Web of Science][Medline].
-
Fischl B,
Liu A,
Dale AM
(2001)
Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex.
IEEE Trans Med Imaging
20:70-80[Web of Science][Medline].
-
Fletcher PC,
Frith CD,
Grasby PM,
Shallice T,
Frackowiak RS,
Dolan RJ
(1995)
Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans.
Brain
118:401-416[Abstract/Free Full Text].
-
Fletcher PC,
Shallice T,
Dolan RJ
(1998)
The functional roles of prefrontal cortex in episodic memory. I. Encoding.
Brain
121:1239-1248[Abstract/Free Full Text].
-
Friston KJ,
Zarahn E,
Josephs O,
Henson RN,
Dale AM
(1999)
Stochastic designs in event-related fMRI.
NeuroImage
10:607-619[Web of Science][Medline].
-
Gardiner JM,
Java R
(1993)
Recognizing and remembering.
In: Theories of memory (Collins AF,
Gathercole SE,
Conway MA,
Morris PE,
eds), pp 163-188. Hove, UK: Erlbaum.
-
Henson R,
Rugg M,
Shallice T,
Josephs O,
Dolan R
(1999a)
Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study.
J Neurosci
19:3962-3972[Abstract/Free Full Text].
-
Henson R,
Shallice T,
Dolan RJ
(1999b)
Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis.
Brain
122:1367-1381[Abstract/Free Full Text].
-
Henson R,
Rugg MD,
Shallice T,
Dolan RJ
(2000)
Confidence in recognition memory for words: dissociating right prefrontal roles in episodic retrieval.
J Cogn Neurosci
12:913-923[Web of Science][Medline].
-
Henson R,
Shallice T,
Rugg M,
Fletcher P,
Dolan R
(2001)
Functional imaging dissociations within right prefrontal cortex during episodic memory retrieval.
Brain Cogn
47:79-81[Web of Science].
-
Iidaka T,
Anderson ND,
Kapur S,
Cabeza R,
Craik FI
(2000)
The effect of divided attention on encoding and retrieval in episodic memory revealed by positron emission tomography.
J Cogn Neurosci
12:267-280[Web of Science][Medline].
-
Jacoby L
(1991)
A process dissociation framework? Separating automatic from intentional uses of memory.
J Mem Language
30:513-541.
-
Johnson MK,
Kounios J,
Nolde SF
(1997)
Electrophysiological brain activity and memory source monitoring.
NeuroReport
8:1317-1320[Web of Science][Medline].
-
Kirchhoff BA,
Wagner AD,
Maril A,
Stern CE
(2000)
Prefrontal-temporal circuitry for episodic encoding and subsequent memory.
J Neurosci
20:6173-6180[Abstract/Free Full Text].
-
Kucera H,
Francis W
(1967)
In: Computational analysis of present-day American English. Providence, RI: Brown UP.
-
Mandler G
(1980)
Recognizing: the judgment of prior occurrence.
Psychol Rev
87:252-271[Web of Science].
-
Mazziotta JC,
Toga AW,
Evans A,
Fox P,
Lancaster JA
(1995)
Probabilistic atlas of the human brain: theory and rationale for its development.
NeuroImage
2:89-101[Web of Science][Medline].
-
Menon V,
White CD,
Eliez S,
Glover GH,
Reiss AL
(2000)
Analysis of a distributed neural system involved in spatial information, novelty, and memory processing.
Hum Brain Mapp
11:117-129[Web of Science][Medline].
-
Naveh-Benjamin M,
Guez J
(2000)
Effects of divided attention on encoding and retrieval processes: assessment of attentional costs and a componential analysis.
J Exp Psychol Learn Mem Cogn
26:1461-1482[Web of Science][Medline].
-
Naveh-Benjamin M,
Craik FI,
Guez J,
Dori H
(1998)
Effects of divided attention on encoding and retrieval processes in human memory: further support for an asymmetry.
J Exp Psychol Learn Mem Cogn
24:1091-1104[Web of Science][Medline].
-
Naveh-Benjamin M,
Craik FI,
Perretta JG,
Tonev ST
(2000a)
The effects of divided attention on encoding and retrieval processes: the resiliency of retrieval processes.
Q J Exp Psychol A
53:609-625[Web of Science][Medline].
-
Naveh-Benjamin M,
Craik FI,
Gavrilescu D,
Anderson ND
(2000b)
Asymmetry between encoding and retrieval processes: evidence from divided attention and a calibration analysis.
Mem Cognit
28:965-976[Web of Science][Medline].
-
Nolde S,
Johnson M,
Raye C
(1998a)
The role of prefrontal cortex during tests of episodic memory.
Trends Cogn Sci
2:399-405[Web of Science].
-
Nolde S,
Johnson MK,
D'Esposito M
(1998b)
Left prefrontal activation during episodic remembering: an event-related fMRI study.
NeuroReport
9:3509-3514[Web of Science][Medline].
-
Otten LJ,
Donchin E
(2000)
Relationship between P300 amplitude and subsequent recall for distinctive events: dependence on type of distinctiveness attribute.
Psychophysiology
37:644-661[Web of Science][Medline].
-
Otten LJ,
Rugg MD
(2001)
When more means less: neural activity related to unsuccessful memory encoding.
Curr Biol
11:1528-1530[Web of Science][Medline].
-
Paller KA,
Wagner AD
(2002)
Observing the transformation of experience into memory.
Trends Cogn Sci
6:93-102.
-
Poldrack RA,
Wagner AD,
Prull MW,
Desmond JE,
Glover GH,
Gabrieli JD
(1999)
Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex.
NeuroImage
10:15-35[Web of Science][Medline].
-
Ranganath C,
Johnson MK,
D'Esposito M
(2000)
. Left anterior prefrontal activation increases with demands to recall specific perceptual information.
J Neurosci
20:RC108(1-5).
-
Rugg MD,
Fletcher PC,
Chua PM,
Dolan RJ
(1999)
The role of the prefrontal cortex in recognition memory and memory for source: an fMRI study.
NeuroImage
10:520-529[Web of Science][Medline].
-
Shallice T,
Fletcher P,
Frith CD,
Grasby P,
Frackowiak RS,
Dolan RJ
(1994)
Brain regions associated with acquisition and retrieval of verbal episodic memory.
Nature
368:633-635[Medline].
-
Strange BA,
Otten LJ,
Josephs O,
Rugg MD,
Dolan RJ
(2002)
Dissociable human perirhinal, hippocampal, and parahippocampal roles during verbal encoding.
J Neurosci
22:523-528[Abstract/Free Full Text].
-
Tulving E
(1985)
Memory and consciousness.
Can Psychol
26:1-12.
-
Wagner AD,
Schacter DL,
Rotte M,
Koutstaal W,
Maril A,
Dale A,
Rosen BR,
Buckner RL
(1998)
Building memories: remembering and forgetting verbal experiences as predicted by brain activity.
Science
281:1188-1191[Abstract/Free Full Text].
-
Wagner AD,
Koutstaal W,
Schacter DL
(1999)
When encoding yields remembering: insights from event-related neuroimaging.
Philos Trans R Soc Lond B Biol Sci
354:1307-1324[Abstract/Free Full Text].
-
Yonelinas AP
(2001)
Consciousness, control, and confidence: the 3 Cs of recognition memory.
J Exp Psychol Gen
130:361-379[Web of Science][Medline].
-
Yonelinas AP
(2002)
The nature of recollection and familiarity: a review of 30 years of research.
J Mem Language
46:441-517.
-
Yonelinas AP,
Kroll NEA,
Dobbins IG,
Lazzara M,
Knight RT
(1998)
Recollection and familiarity deficits in amnesia: convergence of remember/know, process dissociation, and receiver operating characteristic data.
Neuropsychology
12:1-17.
-
Yonelinas AP,
Hopfinger JB,
Buonocore MH,
Kroll NEA,
Baynes K
(2001)
Hippocampal, parahippocampal, and occipital-temporal contributions to associative and item recognition memory: an fMRI study.
NeuroReport
12:359-363[Web of Science][Medline].
Copyright © 2003 Society for Neuroscience 0270-6474/03/2362407-09$05.00/0
This article has been cited by other articles:
|
|
|
|
 
N. M. Dudukovic, S. DuBrow, and A. D. Wagner
Attention during memory retrieval enhances future remembering
Mem Cognit,
October 1, 2009;
37(7):
953 - 961.
[Abstract]
[PDF]
|
|
|
|
|
|
|
K. R. MICKLEY and E. A. KENSINGER
Emotional valence influences the neural correlates associated with remembering and knowing
Cogn Affect Behav Neurosci,
June 1, 2008;
8(2):
143 - 152.
[Abstract]
[PDF]
|
|
|
|
|
|
|
N. De Pisapia, J. A. Slomski, and T. S. Braver
Functional Specializations in Lateral Prefrontal Cortex Associated with the Integration and Segregation of Information in Working Memory
Cereb Cortex,
May 1, 2007;
17(5):
993 - 1006.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Iidaka, A. Matsumoto, J. Nogawa, Y. Yamamoto, and N. Sadato
Frontoparietal Network Involved in Successful Retrieval from Episodic Memory. Spatial and Temporal Analyses Using fMRI and ERP
Cereb Cortex,
September 1, 2006;
16(9):
1349 - 1360.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Kensinger and D. L. Schacter
Neural Processes Underlying Memory Attribution on a Reality-monitoring Task
Cereb Cortex,
August 1, 2006;
16(8):
1126 - 1133.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Duarte, C. Ranganath, and R. T. Knight
Effects of Unilateral Prefrontal Lesions on Familiarity, Recollection, and Source Memory
J. Neurosci.,
September 7, 2005;
25(36):
8333 - 8337.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-P. Royet and J. Plailly
Lateralization of Olfactory Processes
Chem Senses,
October 1, 2004;
29(8):
731 - 745.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Kahn, L. Davachi, and A. D. Wagner
Functional-Neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory
J. Neurosci.,
April 28, 2004;
24(17):
4172 - 4180.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Kensinger and S. Corkin
Two routes to emotional memory: Distinct neural processes for valence and arousal
PNAS,
March 2, 2004;
101(9):
3310 - 3315.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
TOP
ABSTRACT
Introduction
