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The Journal of Neuroscience, May 15, 1999, 19(10):3962-3972
Recollection and Familiarity in Recognition Memory: An
Event-Related Functional Magnetic Resonance Imaging Study
R. N. A.
Henson1, 2,
M.
D.
Rugg2,
T.
Shallice2,
O.
Josephs1, and
R. J.
Dolan1, 3
1 Wellcome Department of Cognitive Neurology, Institute
of Neurology, University College London, London WC1N 3BG, United
Kingdom, 2 Institute of Cognitive Neuroscience and
Department of Psychology, University College London, London, WC1N 3BG,
United Kingdom, and 3 Royal Free Hospital School of
Medicine, London NW2, United Kingdom
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ABSTRACT |
The question of whether recognition memory judgments with and
without recollection reflect dissociable patterns of brain activity is
unresolved. We used event-related, functional magnetic resonance imaging (fMRI) of 12 healthy volunteers to measure hemodynamic responses associated with both studying and recognizing words. Volunteers made one of three judgments to each word during recognition: whether they recollected seeing it during study (R judgments), whether
they experienced a feeling of familiarity in the absence of
recollection (K judgments), or whether they did not remember seeing it
during study (N judgments). Both R and K judgments for studied words
were associated with enhanced responses in left prefrontal and left
parietal cortices relative to N judgments for unstudied words. The
opposite pattern was observed in bilateral temporoccipital regions and
amygdalae. R judgments for studied words were associated with enhanced
responses in anterior left prefrontal, left parietal, and posterior
cingulate regions relative to K judgments. At study, a posterior left
prefrontal region exhibited an enhanced response to words subsequently
given R versus K judgments, but the response of this region during
recognition did not differentiate R and K judgments. K judgments for
studied words were associated with enhanced responses in right lateral
and medial prefrontal cortex relative to both R judgments for studied
words and N judgments for unstudied words, a difference we attribute to
greater monitoring demands when memory judgments are less certain.
These results suggest that the responses of different brain regions do
dissociate according to the phenomenology associated with memory retrieval.
Key words:
remember; know; recollection; familiarity; episodic
memory retrieval; source; event-related fMRI
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INTRODUCTION |
The "remember-know" procedure
was introduced by Tulving (1985) to investigate the conscious
experience accompanying memory retrieval. Participants in this
procedure indicate with a remember (R) judgment those stimuli that
evoke recollection of a specific episode in which the stimuli were
experienced previously. For stimuli thought to have been experienced
previously, but which do not evoke recollection of a specific episode,
participants make a know (K) judgment. R judgments typically entail
memory for the spatiotemporal context in which stimuli occurred or the mental associations triggered by their occurrence ("source" memory) (Johnson et al., 1993). K judgments typically entail a sense of familiarity, in the absence of information about the source of that
familiarity (such as when one recognizes a face, but cannot remember to
whom it belongs).
Behavioral evidence pertaining to the remember-know distinction
includes claims that deeper encoding (Gardiner, 1988), lower normative
frequency of stimuli (Gardiner and Java, 1990), and full versus divided
attention (Gardiner and Parkin, 1990) increase R but not K judgments,
whereas repeated shallow encoding (Gardiner et al., 1994) and
subliminal priming (Rajaram, 1993) increase K but not R judgments.
These claims, however, are based on the assumption that R and K
judgments are exclusive, and different dissociations arise when R and K
judgments are assumed to be independent or redundant (Yonelinas et al.,
1996). Nonetheless, whether R and K judgments reflect qualitative or
quantitative differences (Donaldson, 1996), they remain a useful means
of operationalizing the subjective experience accompanying retrieval.
Little is known about the neural substrates that mediate R and K
judgments. Knowlton and Squire (1995) found that amnesics with damage
to the hippocampal formation or diencephalon showed reduced levels of
both R and K judgments, whereas Schacter et al. (1997b) found that
amnesics showed reduced levels of R but not K judgments. These results
can be reconciled by scoring R and K judgments under an independence
assumption, for which amnesics show reduced levels of both recollection
and familiarity (Yonelinas et al., 1998). However, after reviewing the
more general pattern of recognition and recall in amnesia, Aggleton and
Brown (1998) argued that recollection depends on the hippocampus,
whereas familiarity depends on the perirhinal cortex. An additional
frontal role in recollection is suggested by studies showing that
frontal patients are disproportionately impaired at retrieval of source
information (Janowsky et al., 1989; Shimamura et al., 1990).
Distinct patterns of event-related potentials (ERPs) have been
associated with R and K judgments. Smith (1993) found enhanced positive-going ERPs for R relative to K judgments 550-700 msec after
stimulus, and Duzel et al. (1997) found that this difference was
maximal over the left parietotemporal and bilateral frontal electrode
sites. This pattern is consistent with the ERPs associated with correct
and incorrect source judgments, which also diverge at these sites
(Wilding and Rugg, 1996; Johnson et al., 1997). However, the anatomical
generators of ERPs are notoriously difficult to localize. Here we
capitalize on the high spatial resolution of event-related functional
magnetic resonance imaging (fMRI) to localize differences in the
hemodynamic response to individual R and K judgments.
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MATERIALS AND METHODS |
Participants. Twelve right-handed volunteers (six
male), aged between 22 and 34 years (with a mean age of 26 years), gave informed consent to participate in the experiment.
Cognitive tasks. Participants were scanned during four
sessions ordered as study-test-study-test conditions. Both
conditions involved sequential, visual presentation of 90 stimuli, each
stimulus prompting a manual response with the right hand. The stimuli
were presented for 1 sec, followed by 7 sec of a central fixation cross.
In the study condition, the task was to press a key with either the
index or middle finger to indicate whether the stimulus was a real word
(a "lexical decision" task). Sixty stimuli were words; 30 were
nonwords created by rearranging the letters of the remaining words
assigned to that condition. A 1 min period of backward counting
followed every study session to minimize any contribution of short-term
memory to the subsequent test condition.
In the test condition, the 60 old words from the previous study
condition were redisplayed, intermixed with 30 new words not seen
before. Participants made one of three possible key presses with their
index, middle, or ring fingers to indicate whether they consciously
recollected seeing the word in the previous study episode (an R
judgment), knew that the word was seen in the previous study episode
but could not recollect any contextual information about its previous
occurrence (a K judgment), or thought the word was new (an N judgment).
Participants were given brief practice on the study and test conditions
before scanning, and the instructions for the R/K distinction [adapted
from Rajaram (1993)] were clarified with examples. The instructions
for responding emphasized accuracy over speed, and participants were
reminded to focus on the fixation cross between stimuli.
Experimental materials and procedure. We obtained 240 five-letter nouns with a Kucera-Francis written frequency of 10-100 from the Medical Research Council Psycholinguistics database
(http://www.psy.uwa.edu.au/uwa_mrc.htm) and assigned
them randomly to each condition for each participant. The stimuli were
presented in 24-point Helvetica font on a Macintosh computer and
projected onto a screen ~300 mm above the participant in the MRI
scanner. The visual angle subtended by the stimuli was ~2°.
The stimuli were ordered such that every third stimulus in the study
condition was a nonword, and every third stimulus in the test condition
was a new word, to maximize blood oxygenation level-dependent (BOLD)
signal contrast between words and nonwords and old and new words,
respectively (R. Henson, O. Josephs, and K. Friston, unpublished
observations). To reduce the risk of participants detecting this
pattern, a random 10% of trial triplets were reordered. In fact, no
participant reported detecting any pattern in the stimuli, and the
behavioral data showed no evidence of this manipulation. The finger
assignment of word-nonword and R-K-N judgments was counterbalanced
across participants.
fMRI scanning technique. A 2T Siemens VISION system
(Siemens, Erlangen, Germany) was used to acquire both T1 anatomical
volume images (1 × 1 × 1.5 mm voxels) and T2*-weighted
echoplanar (EPI) images (64 × 64 5 × 5 mm pixels;
echo time = 40 msec) with BOLD contrast. Each echoplanar image
comprised 34 2.5 mm axial slices taken every 3 mm, positioned to cover
the cortex (the cerebellum was not imaged). Data were acquired during
four 12 min sessions, separated by a 2 min rest period. A total of 245 volume images per session were taken continuously with an effective
repetition time (TR) of 3 sec/vol, of which the first five volumes were
discarded to allow for T1 equilibration effects. The ratio of
interscan-to-interstimulus interval ensured an effective sampling rate
of the hemodynamic response of 1 Hz.
Preprocessing. To correct for their different acquisition
times, the signal measured in each slice was shifted relative to the
acquisition of the middle slice using a sinc interpolation in time. All
volumes were then realigned to the first volume and resliced using a
sinc interpolation in space. Each volume was normalized to a standard
EPI template volume (based on the Montreal Neurological
Institute reference brain) (Cocosco et al., 1997) of 3 × 3 × 3 mm voxels in the space of Talairach and Tournoux (1988)
using nonlinear basis functions. The T1 structural volume was
coregistered with the mean realigned EPI volume and normalized with the
same deformation parameters. Finally, the EPI volumes were smoothed
with an 8 mm full-width half-maximum isotropic Gaussian kernel
to accommodate further anatomical differences across participants and
proportionally scaled to a global mean of 100.
Data analysis. Data were analyzed using Statistical
Parametric Mapping (SPM97d, Wellcome Department of Cognitive Neurology, London, UK) (Friston et al., 1995). Stimuli in the test condition were
classified according to seven event-types: correct R, K and N
judgments, incorrect R, K and N judgments, and trial failures (when no
judgment was made within 4 sec of the stimulus). Stimuli in the study
condition were classified according to three basic event types:
judgments to words, judgments to nonwords, and trial failures.
Judgments to words in the study condition were further classified as
words given an R judgment in the subsequent test condition, words given
a K judgment in the subsequent test condition, words given an N
judgment in the subsequent test condition, and trial failures in the
subsequent test condition.
By treating the volumes acquired during each session as a time series,
the hemodynamic responses to the stimulus onset for each event-type
were modelled with a canonical, synthetic hemodynamic response function
and its first-order derivative with respect to time (Josephs et al.,
1997). The inclusion of the derivative accommodates for small
deviations in the onset of the hemodynamic response (Friston et al.,
1998). These functions were used as covariates in a general linear
model, together with a constant term and a basis set of cosine
functions with a cutoff period of 90 sec to remove low-frequency drifts
in the BOLD signal (Holmes et al., 1997). The parameter estimates for
the height of the canonical response for each event-type covariate
resulting from the least mean squares fit of the model to the data were
stored as separate images, and the estimates were averaged across the
two sessions of each study and test condition.
Pairwise contrasts between the height parameter estimate for event
types comprising at least 10 events were tested by voxel-specific, repeated-measures t tests across participants (effecting a
random effects model), which were subsequently transformed to the unit normal Z-distribution to create a statistical parametric map for each
contrast. Given that differential activity in several brain regions was
predicted on the basis of previous studies of encoding and recognition
of words, the regionally specific differences reported below consisted
of four or more contiguous voxels surviving a threshold of
p < 0.001 (Z > 3.09). The maxima of
these regions were localized on the normalized structural images and
labeled using the nomenclature of Talairach and Tournoux (1988) and
Brodmann (1909) for consistency with previous studies.
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RESULTS |
Behavioral data
Performance of the lexical decision task in the study condition
was almost perfect, with 97% of words and 93% of nonwords classified
correctly (the 2% of trials in study and test conditions in which
participants failed to give a response within 4 sec of stimulus onset
were removed from subsequent analyses). The mean reaction time for
correct word classifications (M = 931 msec, SD = 145 msec)
was shorter than for correct nonword classifications (M = 998 msec, SD = 187 msec), although this difference did not reach
significance (t(12) = 1.49, p > 0.10). Mean reaction times for correct lexical decisions in the study
condition did not differ significantly for words given an R (M = 931 msec, SD = 150 msec) or K (M = 970 msec, SD = 201 msec) judgment in the subsequent test condition
(t(12) = 0.69).
The mean proportions and reaction times for each judgment type in the
test condition are shown in Table 1.
Collapsing across R and K judgments, overall memory performance was
reasonable, as indexed by a hit-false alarm rate of 0.78  0.16 = 0.62. Although the difference was small (when scored under
an exclusivity assumption), the hit rate (0.26) for K judgments was
significantly greater than the false alarm rate (0.14),
t(12) = 4.09, p < .01, confirming that K judgments were more than guesses. (When scored under
an independence or redundancy assumption, the difference between hit,
0.26/(1 0.51) = 0.53, and false alarm, 0.14/(1 0.02) = 0.14, rates for K judgments was even more noticeable.)
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Table 1.
Proportions of old and new words and reaction times (RT)
for R, K, and N judgments in the test condition
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R judgments were almost twice as common as K judgments on average,
although the range of R and K judgments was large, with one participant
failing to give >10 R judgments and two participants failing to give
>10 K judgments. These participants were removed from the relevant
image contrasts below (their removal did not have any appreciable
effect on the means and SDs reported in Table 1 or on the significance
of tests performed on the behavioral data). The mean correct reaction
times were longer for K judgments than R or N judgments;
t(12) > 3.53, p < 0.01 in both
cases. Mean correct reaction times did not differ significantly for R
and N judgments (t(12) = 1.51, p > 0.10). The numbers of incorrect R, K, and N judgments were deemed
insufficient to analyze these event-types further. Subsequent analyses
are therefore restricted to correct judgments.
Imaging data
The maxima of all brain regions showing differential event-related
responses to correct R, K, and N judgments are shown in Tables 2-4.
Below we discuss the responses of selected regions that were predicted
on the basis of previous findings.
Correct R versus correct N judgments at test
The regions exhibiting greater event-related responses to R than N
judgments were strikingly left-lateralized, probably reflecting the
verbal nature of the stimuli. The top panel of Figure
1 shows a transverse slice through the
left prefrontal, left parietal, posterior cingulate, and precuneus
regions reported in Table 2. The left
midlateral prefrontal region (BA 9/46) showed similar responses to R
and K judgments, but less response to N judgments. Activation of nearby
regions in comparison of old versus new stimuli was observed by Tulving
et al. (1996). The left lateral superior parietal region (BA 7) showed
a more graded pattern of responses, with the greatest to R judgments
and the least to N judgments. Activity in this area may underlie the
left parietal ERP difference observed between correct responses to old
and new words (Rugg, 1995). The posterior cingulate region (BA 31)
showed a decreased response relative to baseline fixation, with the
least deactivation for R judgments. Given that deactivations may be a
consequence of the global normalization of the BOLD signal (Aguirre et
al., 1998), we emphasize only the differential nature of the response as a function of judgment type. The precuneus region (BA 7/31) showed a
small activation for R judgments and small deactivations for K and N
judgments. This region is consistently activated during episodic
retrieval and may reflect reinstatement of visual images associated
with words during study [Fletcher et al. (1996); although see Buckner
and Peterson (1996)].
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Figure 1.
Regions showing enhanced event-related responses
to correct R versus correct N judgments (top
panel) and correct N versus correct R judgments
(bottom panel). The anatomical slices are taken
through a normalized T1 structural image of one participant's brain.
The activations reflect t tests on the height of the
best-fitting canonical hemodynamic response function (HRF) across
participants, thresholded at p < 0.01 for the
purpose of illustration. The event-related plots are the sum of the
best-fitting canonical HRF and its derivative (see Materials and
Methods) from the voxel in the maxima of the activations, for the nine
participants who made sufficient numbers of correct R, K, and N
judgments. The error bars show the SE of the mean fitted HRF height
across the nine participants (not the SE of the mean difference in
fitted HRF heights for R and N judgments, which forms the error term in
the repeated-measures t tests).
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Table 2.
Maxima within regions showing significant BOLD signal
changes in the comparisons between correct R and correct N judgments
(excluding one participant who made insufficient numbers of R
judgments)
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Other notable regions exhibiting greater responses to R than N
judgments included a ventral region in left inferior frontal gyrus (BA
47), a more anterior region in left superior frontal gyrus (BA 10), and
a posterior medial temporal region in the left hippocampus, close to
the fornix. The left prefrontal regions have been associated with
reflective processes by Nolde et al. (1999), and the posterior medial
temporal region has been associated with episodic retrieval in a
meta-analysis by LePage et al. (1998) (although see Schacter and
Wagner, 1998) and in our own studies (Strange et al., 1999).
Several regions showed greater responses to N than R judgments. These
included a large region in right parietal cortex, extending from
precuneus to superior and inferior parietal gyri (BA 7/40), and large
regions of temporoccipital cortex, particularly on the left and
extending along the lingual, parahippocampal, and middle temporal gyri
(BA 19/37). The reduced response elicited by R and K judgments relative
to N judgments in the temporoccipital regions (Fig. 1, bottom
panel) is consistent with the relative deactivations for
familiar versus novel stimuli that have been attributed to perceptual
priming (Blaxton et al., 1996; Buckner et al., 1996; Schacter and
Buckner, 1998).
Correct K versus correct N judgments at test
The regions exhibiting greater responses to K than N judgments
were confined mainly to left and right prefrontal cortices (Table
3; Fig. 2,
top panel) and included bilateral middle frontal gyri
(BA 9), bilateral medial frontal gyri, centred in the cingulate sulci (BA 9/32), bilateral posterior inferior frontal gyri (BA 47), and
a more anterior region of right midlateral prefrontal cortex (BA 46).
The left prefrontal regions generally showed greater responses to R and
K judgments than N judgments, whereas the right prefrontal regions
generally showed greater responses to K judgments than R and N
judgments. One or more of these regions are usually activated during
episodic retrieval (for review, see Cabeza and Nyberg, 1997; Desgranges
et al., 1998), particularly when retrieval is effortful (Schacter et
al., 1996; Rugg et al., 1997; Buckner et al., 1998b). A small region of
left lateral precuneus (BA 19) also exhibited greater responses to K
than N judgments, but the spatial extent of left parietal activation
was noticeably smaller than in the comparison of R and N judgments.
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Table 3.
Maxima of regions showing significant BOLD signal changes
in the comparisons between correct K and correct N judgments (excluding
two participants who made insufficient numbers of K judgments)
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Figure 2.
Regions showing enhanced event-related responses
to correct K versus correct N judgments (top
panel) and correct N versus correct K judgments
(bottom panel). For details, see Figure 1.
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Many regions that showed reduced responses for R relative to N
judgments also showed reduced responses to K judgments, notably bilateral posterior middle temporal gyri (BA 37/39), bilateral insular
cortex, and bilateral anterior medial temporal cortex. Although the
spatial smoothing and averaging entailed by our statistical inference
across participants makes precise localization difficult, the group
maxima of the medial temporal regions was located just anterior to the
temporal horn of the lateral ventricle in each participant's
normalized structural image, making the amygdala the most likely
candidate. The response of these regions was a deactivation relative to
baseline (Fig. 2, bottom panel), but with less
deactivation for N than R or K judgments. This differential sensitivity
to new versus old words is consistent with the proposal that anterior
regions of the amygdala-hippocampal complex are sensitive to stimulus
novelty (Tulving et al., 1996; Dolan and Fletcher, 1997; LePage et al.,
1998; Strange et al., 1999), in this case the contextual novelty of the
new words.
Correct R versus correct K judgments at test
The direct contrast of R against K judgments revealed a subset of
the regions identified in the R versus N contrast, namely left inferior
parietal (BA 40), left superior parietal (BA 7), and posterior
cingulate (BA 24/31) regions, in addition to a region of left anterior
superior frontal gyrus (BA 8/9; Table 4,
Test). For the prefrontal and left parietal regions, this
difference reflected greater deactivation for K (and N) judgments
relative to R judgments (Fig. 3,
top panel). For the posterior cingulate region, the
difference reflected an activation for R judgments and deactivations
for K (and N) judgments. The left superior parietal maximum is very
close to that previously associated with retrieval of contextual
information (Henson et al., 1999) and may underlie the left parietal
ERP differences attributed to source retrieval (Wilding and Rugg, 1996;
Allan et al., 1998). Anterior left prefrontal regions have also been
associated with source retrieval by Nolde et al. (1998a), although the
anterior region identified in the present study is more superior (BA
8/9 rather than BA 10).
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Table 4.
Maxima of regions showing significant BOLD signal changes
in the comparisons between correct R and correct K judgments at study
and at test (excluding three participants who made insufficient numbers
of R or K judgments)
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Figure 3.
Regions showing enhanced event-related responses
to correct R versus correct K judgments (top
panel) and correct K versus correct R judgments
(bottom panel). For details, see Figure 1.
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The reverse contrast of K against R judgments implicated three of
the regions associated with the K versus N contrast, namely left and
right cingulate sulci (BA 9/32) and right midlateral prefrontal cortex
(BA 46). All three regions showed greater responses to K judgments than
either R or N judgments (Fig. 3, bottom panel). These
differences may reflect greater retrieval monitoring associated with K
judgments (see Discussion), reflected by the longer reaction times for
K than R or N judgments. The responses of the more posterior inferior
and middle frontal regions did not appear to differentiate R and K judgments.
Correct R versus correct K judgments at study
Figure 4 shows a region in left
posterior middle frontal gyrus (BA 9/44) that exhibited a greater
response to words at study that were subsequently given an R judgment
at test than words that were subsequently given a K judgment. Because
every event in this comparison was associated with a correct lexical
decision, the response times of which did not differ significantly as a function of the later recognition judgment, this subsequent
memory effect is unlikely to reflect simple perceptual differences.
Rather, it is likely to reflect differences in semantic elaborative or organizational processes that aid memory encoding (Fletcher et al.,
1998). A similar finding was reported recently by Wagner et al.
(1998b).
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Figure 4.
Regions showing enhanced event-related responses
at study to words given correct R versus correct K judgments in the
subsequent recognition test. The event-related plot on the
left shows the fitted response at study; the plot on the
right shows the fitted response of the same voxel at
test. For details, see Figure 1.
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Responses measured at the same voxel, however, did not differentiate R
and K judgments at test (although they did differentiate R and K
judgments from N judgments). Similar response profiles, which
distinguished R and K judgments at study but not at test, were also
seen for a more ventral region of left inferior frontal gyrus (BA 47)
and a lateral region of left precuneus (BA 7; Table 4, Study).
Thus the brain regions in which activity during study predicted
subsequent recollective experience did not necessarily reflect that
experience during test. A right hippocampal-parahippocampal region
showed greater response to words at study that were subsequently given
K rather than R judgments, but given that this pattern was not
parallelled at test, and that no predictions were made for this
opposite pattern (cf. Brewer et al., 1998; Wagner et al., 1998b), we do
not offer any explanation for responses in this or the precuneus
regions in Table 4, Study.
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DISCUSSION |
The present study represents one of the first event-related fMRI
experiments to identify brain regions that exhibit differential hemodynamic responses according to whether participants recognize stimuli from a previous study episode (cf. Schacter et al., 1997a; Buckner et al., 1998a). Moreover, it provides evidence that several brain regions exhibit differential responses as a function of whether
correct recognition is associated with recollection, as operationalized
by the remember-know procedure (Tulving, 1985). This combination of
event-related fMRI with a subjective classification of events heralds
an exciting future for the neuroimaging of human memory.
The striking left-lateralization of regions associated with
recollection of old words (R judgments) relative to rejection of new
words (N judgments) is surprising in light of numerous studies that
have associated episodic retrieval with right prefrontal cortex
(Shallice et al., 1994; Tulving et al., 1994; Buckner and Peterson,
1996; Nyberg et al., 1996; Fletcher et al., 1997). Most of these
studies have used blocked rather than event-related designs and
compared an episodic retrieval task with a comparable control task. One
possibility is that the right prefrontal activations in these
comparisons reflect the adoption of a retrieval mode (Kapur et al.,
1995; Nyberg et al., 1995), the cognitive state arising whenever one
attempts to refer to past experiences (Tulving, 1983). Because
participants in the present study were attempting retrieval throughout
the experiment, differential responses in right prefrontal cortex
therefore might not be expected. Other studies (Rugg et al., 1996;
Buckner et al., 1998b) have found right prefrontal activation when
comparing blocks of a retrieval task in which only the ratio of old to
new words varied. These activations tend to cluster in anterior regions
of prefrontal cortex, and we may have failed to detect differential
responses in these regions by virtue of diminished sensitivity owing to fMRI susceptibility artifacts in frontopolar regions.
Nonetheless, we did find differential responses in right posterior
prefrontal cortex associated with old relative to new words when
recognition was based on familiarity in the absence of recollection (i.e., K judgments). These regions included ventral and dorsal regions
of posterior prefrontal cortex, medial frontal/anterior cingulate
cortex, and dorsal midlateral prefrontal cortex. We attribute these
differences to postretrieval processing (Shallice et al., 1994; Rugg et
al., 1996). The right dorsolateral activation in particular we
attribute to monitoring (cf. Nolde et al., 1999): processes that verify
whether the products of retrieval attempts are sufficient for the
current task (Burgess and Shallice, 1996). When these products include
the spatiotemporal context of a word's previous occurrence, an R
judgment can follow immediately. When no such spatiotemporal
information is forthcoming, yet the products of retrieval are
associated with a feeling of familiarity, further retrieval attempts
may ensue before a judgment is made (explaining why reaction times were
longer for K judgments than R or N judgments). When repeated retrieval
attempts fail to reinstate any contextual information, the decision
remains whether to attribute the familiarity to a word's previous
occurrence (i.e., give a K or an N judgment). The relatively high
proportion of misses in the present experiment suggests that many K
judgments to old words were close to the K-N criterion (Donaldson,
1996; Yonelinas et al., 1996). In other words, we suggest that
monitoring requirements during recognition are highest when familiarity
levels are close to a response criterion. The right prefrontal
activations associated with higher old/new word ratios in the studies
of Rugg et al. (1996) and Buckner et al. (1998b) may therefore not
reflect retrieval success per se but rather differing degrees of
monitoring resulting from shifting response criteria, particularly
given that these activations are sensitive to changes in task
instructions (Wagner et al., 1998a).
Unlike their homologs in right prefrontal cortex, ventral and dorsal
regions of left posterior prefrontal cortex exhibited greater responses
to both R and K judgments relative to N judgments. Thus, although these
regions indexed successful retrieval, they did not appear to
distinguish recollection and familiarity or the degree of monitoring.
They may subserve other postretrieval processes such as maintaining or
manipulating retrieval products in working memory (Petrides et al.,
1995). The left prefrontal region that did exhibit greater responses to
R than K judgments was in anterior prefrontal cortex. Nolde et al.
(1998) found that nearby, although generally inferior, regions of
anterior left prefrontal cortex exhibited greater event-related
responses to words in a source retrieval task than in a simple yes-no
recognition task. Comparable results were observed in a recent blocked
fMRI study (M. Rugg, P. Fletcher, P. Chua, and R. Dolan, unpublished observations). Anterior left prefrontal cortex therefore may be specialized for the reflective processes associated with source retrieval (Nolde et al., 1999), and damage to nearby regions may contribute to the source retrieval impairment observed in frontal patients (Janowsky et al., 1989; Shimamura et al., 1990).
A left posterior prefrontal region, close to that identified by Wagner
et al. (1998b), exhibited a greater response to words at study that
were subsequently given an R as opposed to a K judgment. However, no
brain region in the present study showed a significantly greater
response to R than K judgments at both study and test. This finding is
troublesome for at least one interpretation of transfer-appropriate
processing theory (Morris et al., 1977; Kolers and Roediger, 1984),
which according to Blaxton et al. (1996) holds that the same brain
regions differentiate memory performance at both study and test. An
alternative proposal (Brewer et al., 1998; Wagner et al., 1998b) is
that the results of processes performed in prefrontal cortex during
encoding (such as semantic elaboration and organization) comprise the
input to a medial temporal memory system. Such processes are less
important when the words are seen again during test, when performance
is assumed to be driven mainly by episodic retrieval from medial
temporal structures.
Several regions within left parietal cortex also showed greater
responses to R than K judgments. At least one of these regions, in left
precuneus, also showed greater responses to K than N judgments, suggesting that some left parietal regions show a graded response to R,
K, and N judgments. This accords with several studies in which the
magnitude of the left parietal ERP old/new effect increases with the
amount of contextual information retrieved (Allan et al., 1998),
suggesting that the difference between R and K judgments may be
quantitative rather than qualitative (Johnson et al., 1993; Donaldson,
1996). More generally, our findings of both left parietal and bilateral
prefrontal differences between R and K judgments are highly consistent
with ERP findings (Smith, 1993; Wilding and Rugg, 1996; Duzel et al.,
1997; Johnson et al., 1997; Rugg et al., 1998). Furthermore, our data
suggest a dissociation between the responses of parietal and prefrontal
cortices, with the former showing a greater hemodynamic response to R
judgments and the latter showing a greater hemodynamic response to K judgments.
Our findings are moot with respect to the neuropsychological findings
of Knowlton and Squire (1995), who suggested that medial temporal
structures are important for both R and K judgments. We identified a
medial posterior region of left hippocampus that exhibited greater
response to R than N judgments, but any difference between K and N
judgments in this region failed to reach significance. This finding is
more consistent with the suggestion of Aggleton and Brown (1998) that
recollection requires hippocampal involvement. Nonetheless, no medial
temporal structure showed a differential response in a direct
comparison of R and K judgments. Indeed, whether one regards
recollection as indexed by the R versus N comparison or by the R versus
K comparison depends on whether one regards recollection and
familiarity as independent, redundant, or exclusive (Knowlton and
Squire, 1995; Yonelinas et al., 1996).
One medial temporal structure that did exhibit differential responses
to both R and K judgments relative to N judgments was the amygdala,
which showed less deactivation relative to baseline in response to N
judgments than R or K judgments. The amygdala has previously been
associated with novelty detection (Wilson and Rolls, 1993) and the
encoding of emotionally salient stimuli (Babinsky et al., 1993; Cahill
et al., 1996). The word stimuli used in the present study are unlikely
to have much emotional significance, however, and other studies have
shown that the amygdala is not necessary for episodic memory (Bechara
et al., 1995; Parker et al., 1998). One possibility is that amygdala
activity reflects an obligatory orienting or arousal response to novel
stimuli, with the translation of novelty into effective memory encoding depending on other medial temporal structures.
Previous neuroimaging studies have provided good evidence for
dissociable brain systems underlying, for example, episodic, semantic,
and implicit memory (Gabrieli, 1998). In the present study, we have
shown further that the subjective classification of stimuli afforded by
event-related techniques allows neuroscientists to begin to address
Tulving's (1983) call for a scientific approach to the conscious
experience accompanying memory retrieval.
| |
FOOTNOTES |
Received Dec. 18, 1998; revised Feb. 16, 1999; accepted March 2, 1999.
This work was supported by Wellcome Trust Grant 051028/Z.
Correspondence should be addressed to Dr. Richard Henson, Wellcome
Department of Cognitive Neurology, 12 Queen Square, London WC1N 3BG, UK.
| |
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TOP
ABSTRACT
INTRODUCTION
