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The Journal of Neuroscience, August 15, 2000, 20(16):6173-6180
Prefrontal-Temporal Circuitry for Episodic Encoding and
Subsequent Memory
Brenda A.
Kirchhoff1,
Anthony D.
Wagner2, 3,
Anat
Maril4, and
Chantal E.
Stern1, 3
1 Department of Psychology, Boston University, Boston,
Massachusetts 02215, 2 Department of Brain and Cognitive
Sciences, Massachusetts Institute of Technology, Cambridge,
Massachusetts 02139, 3 Massachusetts General Hospital
Nuclear Magnetic Resonance Center, Charlestown, Massachusetts
02129, and 4 Department of Psychology, Harvard University,
Cambridge, Massachusetts 02138
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ABSTRACT |
Humans encounter and form memories for multiple types of
experiences that differ in content, novelty, and memorability. Critical for understanding memory is determining (1) how the brain
supports the encoding of events with differing content and (2) whether neural regions that are sensitive to novelty also influence whether stimuli will be subsequently remembered. This event-related functional magnetic resonance imaging (fMRI) study crossed content
(picture/word), novelty (novel/repeated), and subsequent memory
(remembered/forgotten) to examine prefrontal and temporal lobe
contributions to encoding. Results revealed three patterns of
encoding-related activation in anatomically connected inferior
prefrontal and lateral temporal structures that appeared to vary
depending on whether visuospatial/visuo-object, phonological/lexical,
or semantic attributes were processed. Event content also modulated
medial temporal lobe activity; word encoding predominately activated
the left hemisphere, whereas picture encoding activated both
hemispheres. Critically, in prefrontal and temporal regions that were
modulated by novelty, the magnitude of encoding activation also
predicted whether an event would be subsequently remembered. These
results suggest that (1) regions that demonstrate a sensitivity to
novelty may actively support encoding processes that impact subsequent
explicit memory and (2) multiple content-dependent prefrontal-temporal
circuits support event encoding. The similarities between prefrontal
and lateral temporal encoding responses raise the possibility that
prefrontal modulation of posterior cortical representations is central
to encoding.
Key words:
declarative memory; explicit memory; fMRI; neuroimaging; human memory; prefrontal cortex; medial temporal lobe; parahippocampal
gyrus; hippocampus
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INTRODUCTION |
Recent neuroimaging studies have
consistently demonstrated that the prefrontal cortices and medial
temporal lobes (MTLs) are active during episodic encoding (Nyberg et
al., 1996 ; Lepage et al., 1998; Buckner et al., 1999; Schacter
and Wagner, 1999; Wagner, 1999). One factor affecting the nature
of prefrontal encoding may be the content of the to-be-encoded
information. Encoding verbal information preferentially activates the
left inferior prefrontal cortex (LIPC), whereas encoding nonverbal
information preferentially activates the right inferior prefrontal
cortex (RIPC) (Kelley et al., 1998; Wagner et al., 1998a).
Dissociations within the LIPC suggest that semantic and phonological
feature processing activates the anterior LIPC [Brodmann's area (BA)
45/47] and the posterior LIPC (BA 44/6), respectively (Buckner et al., 1995; Fiez, 1997; Poldrack et al., 1999).
The content of experiences also appears to affect the nature of MTL
encoding-related activation. Word encoding predominately activates the
left MTL, scene and object encoding activate the MTL bilaterally, and
unfamiliar face encoding predominately activates the right MTL (Stern
et al., 1996; Gabrieli et al., 1997; Martin et al., 1997; Brewer et
al., 1998; Kelley et al., 1998; Wagner et al., 1998b).
As in inferior prefrontal cortex (Raichle et al., 1994; Demb et al.,
1995; Gabrieli et al., 1996; Wagner et al., 1997; Schacter and Buckner,
1998), the relative novelty of the experience modulates the magnitude
of MTL activation. Activation is greater when stimuli are viewed for
the first time relative to when they have been seen multiple times
(Stern et al., 1996; Gabrieli et al., 1997). Interpretations of these
differential MTL responses across relative novelty include that they
reflect responses to novelty detection or stimulus priming. However,
recent functional magnetic resonance imaging (fMRI) findings indicate
that the magnitude of MTL and prefrontal activation during the encoding
of an experience predicts subsequent memory for that experience, even
when the novelty of the subsequently remembered and forgotten stimuli
is held constant (Brewer et al., 1998; Fernandez et al., 1998; Wagner
et al., 1998b).
Although previous reports suggest that the encoding of different
stimulus features depends on distinct MTL and prefrontal regions,
critical questions remain. First, do these regions interact with
additional posterior brain structures representing the specific features being encoded into memory? Second, to the extent that novelty-related activity may reveal regions contributing to encoding (Knight, 1996; Tulving et al., 1996), do regions demonstrating a
differential response during the encoding of novel stimuli also predict
subsequent memory? To address these questions, an event-related fMRI
study of the encoding of pictures and words was conducted. Stimulus
type (picture/word) was crossed with novelty (novel/repeated) and
subsequent memory (remembered/forgotten). Novelty has been defined
previously in a number of ways (Martin et al., 1997). Here novel
encoding consisted of studying items not encountered previously in the
experimental context, whereas repeated encoding consisted of repeatedly
studying the same two pictures or words during the experiment [similar
to Stern et al. (1996); Gabrieli et al. (1997)]. As in previous
studies, novelty was held constant when considering regions that
predict subsequent memory (Brewer et al., 1998; Fernandez et al., 1998;
Wagner et al., 1998b).
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MATERIALS AND METHODS |
Subjects. Nine right-handed native English-speaking
volunteers participated in this study (seven men; two women; age range, 18-34 years). All subjects had normal or corrected-to-normal vision. Informed consent was obtained in a manner approved by the Human Studies
Committee of Massachusetts General Hospital.
Tasks. Stimuli were complex color pictures of indoor or
outdoor scenes, four- to eight-letter words naming indoor or outdoor objects, and fixation crosses. There were five trial types: novel pictures, repeated pictures, novel words, repeated words, and fixation.
Each of 10 functional scans consisted of 100 stimulus presentations (20 presentations of each of the five trial types), for a total of 1000 stimulus presentations per subject. Participants saw a unique picture
or word during each novel stimulus trial. In the repeated stimulus
trials, the subjects saw one of two repeating pictures or one of two
repeating words (each of these exemplars was seen 100 times across the
10 functional scanning runs). A new trial occurred every 2 sec. The
five trial types were pseudorandomly intermixed with counterbalancing
such that each trial type followed every other trial type equally
often. For picture and word trials, subjects performed an incidental
encoding task in which they made one of two left-handed key press
responses to indicate whether the item represented an indoor or outdoor
entity. Before the first functional run, participants made indoor or
outdoor decisions for each of the repeated picture and word stimuli a
total of 10 times during two practice sequences to ensure that these
stimuli were familiar and that the participants understood task
requirements. This design results in the novel and the repeated
conditions for each stimulus class (picture/word) differing in
situational novelty (novel vs repeated) as well as in the number of
unique items contributing to the condition (200 vs 2).
A surprise recognition memory test was administered outside of the
scanner 15-20 min after the scanning session. During this test, a
random sequence of 400 pictures and 400 words was presented; half were
the novel items seen during the functional encoding scans, and half
were new, unstudied items. Subjects indicated whether they recognized
the test item as having been studied as well as their confidence by
manually responding "high-confidence studied," "low-confidence
studied," or "new."
Data acquisition. Anatomical and functional data were
acquired on a 3.0T GE Signa scanner with an ANMR upgrade.
Structural data were acquired using a T1-weighted
rf-spoiled GRASS sequence (60 sagittal slices; 2.8 mm slice thickness).
Functional data were acquired using a whole-brain echoplanar
T2*-weighted gradient echo sequence
(TR = 2 sec; TE = 30 msec; flip angle = 60°; 16 AC-PC axial slices with a 1 mm skip between slices; 3.125 × 3.125 × 7 mm resolution; 108 images per slice). The duration
of each functional run was 3 min and 44 sec. Ten runs were acquired per subject.
Data analysis. Only trials in which the subjects made the
correct indoor or outdoor designation (96.9%) were analyzed.
Functional data were selectively averaged within subjects (data from
one run for one subject were not included because of scanner
malfunction). Data were then transformed into Talairach space
(Talairach and Tournoux, 1988) and averaged across subjects. The
procedures for selective averaging and statistical map generation are
described elsewhere (Dale and Buckner, 1997; Buckner et al., 1998).
Briefly, voxel-based statistical activation maps were constructed on
the basis of the differences between trial types using a t
statistic. Clusters of five or more voxels exceeding a statistical
threshold of p < 0.001 were considered significant
foci of activation.
Repeated-measures mixed-effect ANOVAs, which treated subjects as a
random effect, were conducted to further examine the effects of
novelty, stimulus type, hemisphere, and subsequent memory on the
percent signal change relative to the fixation baseline in frontal,
lateral temporal, and medial temporal regions of interest (ROIs). ROIs
were identified using an automated algorithm that identified all
contiguous voxels within 10 mm of a peak activation (Buckner et al.,
1998; Wagner et al., 1998b). ROIs were identified from the novel
stimulus comparison (all novel > all repeated) if possible when
effects of novelty were examined because this contrast is unbiased with
respect to examining the effects of stimulus type (picture/word),
hemisphere (left/right), and subsequent memory (high-confidence
remembered/forgotten) (Fig.
1a-e). Left lateral temporal
and left anterior fusiform ROIs were defined from the novel word
encoding (novel > repeated words) and word versus picture
encoding (novel word > novel picture) comparisons, respectively,
because these contrasts revealed that these regions are separable (Fig.
1f,g). ROIs were also derived from a picture subsequent
memory comparison (high-confidence remembered > forgotten picture
trials) to explore subsequent memory effects in the word condition and
the relation of these effects to novelty effects. The peak of the
hemodynamic response (typically occurring between 4 and 8 sec after
stimulus onset) was identified for each ROI in which the effects of
novelty, stimulus type, and hemisphere were examined. The peak was
identified when collapsing across subjects and trial types, and the
percent signal change at the peak for each trial type (relative to the
fixation baseline) was determined on a subject-by-subject basis and
submitted to a mixed-effect ANOVA (the significance criterion was
p < 0.05, Bonferroni corrected). For subsequent memory
ROI analyses, this procedure was modified slightly because only a
modest number of word trials were subsequently forgotten (see Results),
resulting in more variability in the peak of the hemodynamic response
for this condition across subjects. Thus, for ROI-based investigations
of subsequent memory, the summed percent signal change across the time
window corresponding to 4-8 sec after stimulus onset was determined
for each trial type and subjected to a mixed-effect ANOVA.
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Figure 1.
Inferior prefrontal, fusiform, and left lateral
temporal encoding responses. Columns A-E, Activity
during novel stimulus (novel > repeated pictures + words), novel
picture (novel > repeated), picture versus word (novel
picture > novel word), novel word (novel > repeated), and
word versus picture (novel word > novel picture) encoding,
respectively. Regions of interest were defined from the novel stimulus
(a-e), novel word (f), and word
versus picture (g) comparisons. a,
Anterior LIPC:  37, 25, 3; BA 45/47. b,
Posterior LIPC: 34, 6, 34; BA 6/44. c, Posterior RIPC:
43, 3, 37; BA 6/44. d, Left posterior fusiform: 28,
55, 9; BA 37. e, Right posterior fusiform: 34, 49,
12; BA 37. f, Left lateral temporal cortex: 56,
43, 3; BA 21/22. g, Left anterior fusiform: 40,
43, 6; BA 37. L, Left; R,
right.
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RESULTS |
Behavioral results
Classification accuracy on the indoor or outdoor discrimination
during scanning was similar for novel pictures (95.2%) and words
(95.5%; F < 1). However, participants took longer to
make the indoor or outdoor judgment for novel words (878 msec) than for
novel pictures [811 msec; F(1,8) = 8.11; p < 0.05]. Behavioral performance on the
postscan memory test revealed that corrected recognition memory (hits false alarms) was better for the words (58.2%) than for the
pictures [30.7%; F(1,8) = 27.58;
p < 0.05]. Using participants' responses on this
postscan memory test, the encoding trials were then sorted on the basis
of subsequent memory into those that were later remembered with high
confidence and those that were later forgotten. Participants remembered
an average of 70 pictures and 139 words with high confidence and forgot
an average of 78 pictures and 40 words out of 200 words and 200 pictures. The reaction times to make the indoor or outdoor decision did not differ between high-confidence remembered (797 msec) and forgotten (816 msec) pictures (F < 1) or between high-confidence
remembered (846 msec) and forgotten (837 msec) words (F < 1). Thus, any observed neural subsequent memory effects likely do
not reflect differences in stimulus processing time during encoding.
Novelty analyses
A series of voxel-based analyses was conducted on the fMRI
encoding data that consisted of the following comparisons: (1) novel stimulus encoding (novel pictures and words > repeated
pictures and words), (2) novel picture encoding (novel > repeated), and (3) novel word encoding (novel > repeated).
Repeated-measures mixed-effect ANOVAs were then conducted to examine
further the effects of novelty, stimulus type, and hemisphere on the
percent signal change in frontal, lateral temporal, and medial temporal ROIs.
The voxel-based analyses revealed effects of novelty in multiple neural
regions. Novel stimulus encoding (collapsed across words and pictures)
was associated with activation in the anterior and ventral extent of
the left inferior prefrontal cortex (anterior LIPC) and bilateral
activation in several regions, including the posterior and dorsal
extent of the left and right inferior prefrontal cortex (posterior LIPC
and RIPC, extending into the corresponding premotor cortex),
dorsolateral prefrontal cortex (DLPC), posterior hippocampus, posterior
parahippocampal gyrus, fusiform gyrus, lingual gyrus, posterior
cingulate, and intraparietal sulcus. Novel picture encoding was
associated with activation in these same regions, with the exception of
the anterior LIPC. Novel word encoding was associated with activation
in the anterior LIPC, posterior LIPC and RIPC, bilateral DLPC,
bilateral supplementary motor area, bilateral posterior hippocampus,
bilateral posterior parahippocampal gyrus, left lateral temporal
cortex, bilateral fusiform gyrus, bilateral posterior cingulate, left
intraparietal sulcus, and right cerebellum (a complete list of
Talairach coordinates is available on request).
Hypothesis-driven ROI analyses were conducted on prefrontal, lateral
temporal, and medial temporal regions observed to be associated with
novel stimulus encoding in the voxel-based comparison. These analyses
revealed three encoding-related patterns of activity in inferior
prefrontal and lateral temporal regions: the posterior RIPC and
bilateral posterior fusiform demonstrated picture preferential encoding
effects, the posterior LIPC and left anterior fusiform demonstrated
word preferential encoding effects, and the anterior LIPC and left
lateral temporal cortex demonstrated word specific encoding effects
(see Table 1). Content sensitive
encoding activity was also observed in the medial temporal lobe.
Picture and word preferential encoding patterns:
prefrontal-fusiform cortices
Figure 1 illustrates the posterior LIPC, posterior RIPC, and
fusiform regions that were engaged during novel stimulus encoding, and
Figure 2 reveals the percent signal
change time courses from these regions. Both the posterior LIPC and
posterior RIPC (Figs. 1, 2, regions b,
c) demonstrated significant novelty responses [LIPC,
F(1,8) = 16.51; RIPC,
F(1,8) = 16.80] and novelty effects for both pictures [LIPC, F(1,8) = 27.78; RIPC, F(1,8) = 68.53] and
words [LIPC, F(1,8) = 73.77; RIPC,
F(1,8) = 16.30]. There were trends
for a main effect of stimulus type [LIPC,
F(1,8) = 9.07; p < 0.02 uncorrected; RIPC, F(1,8) = 6.60;
p < 0.04 uncorrected], with words eliciting a greater
response in the posterior LIPC and pictures eliciting a greater
response in the posterior RIPC. There also were trends for a
stimulus × novelty interaction in both the posterior LIPC
[F(1,8) = 5.51; p < 0.05 uncorrected] and posterior RIPC
[F(1,8) = 9.00; p < 0.02 uncorrected], revealing a greater novelty effect for words in the
posterior LIPC and a greater novelty effect for pictures in the
posterior RIPC.
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Figure 2.
Percent signal change time courses from the
inferior prefrontal, fusiform, and left lateral temporal regions of
interest shown in Figure 1 and labeled a-g. The
posterior RIPC (c) and bilateral posterior
fusiform regions (d, e) demonstrated picture
preferential encoding responses, the posterior LIPC
(b) and left anterior fusiform
(g) demonstrated word preferential encoding
responses, and the anterior LIPC (a) and left
lateral temporal cortex (f) demonstrated word
specific encoding responses.
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To examine the effect of hemisphere, an additional analysis including
hemisphere as a factor was conducted on the posterior LIPC and RIPC
regions of interest. A hemisphere × stimulus interaction [F(1,8) = 18.51] revealed that
although activation in the posterior LIPC was greater for words than
for pictures [F(1,8) = 13.92], activation in the posterior RIPC was greater for pictures than for
words [F(1,8) = 5.54]. Moreover, the
posterior LIPC demonstrated a greater response than did the posterior
RIPC during word encoding [F(1,8) = 19.87], whereas both regions were similarly active during picture
encoding [F(1,8) = 2.65; NS].
The hemisphere × stimulus × novelty interaction was
significant [F(1,8) = 12.46].
Comparing the difference in the percent signal change between novel and repeated pictures and words indicated a greater word novelty response in the posterior LIPC [F(1,8) = 8.26] and a trend for a greater picture novelty response in the
posterior RIPC [F(1,8) = 4.43; p < 0.07].
Three regions in the fusiform cortex were also influenced by novelty
and stimulus type. Bilateral posterior fusiform regions (Figs. 1, 2,
regions d, e) revealed novelty
responses [left, F(1,8) = 31.86;
right, F(1,8) = 26.44], with greater
responses to novel stimuli being observed both for pictures [left,
F(1,8) = 70.76; right,
F(1,8) = 60.83] and words [left,
F(1,8) = 5.83; right, F(1,8) = 4.42; p < 0.07]. Both regions demonstrated a main effect of stimulus type
[left, F(1,8) = 18.65; right,
F(1,8) = 48.72]. As was observed in
the posterior RIPC, both the left and right posterior fusiform
demonstrated greater activation during picture relative to word
encoding. In addition, a stimulus × novelty interaction was
observed in both posterior fusiform regions [left,
F(1,8) = 17.99; right,
F(1,8) = 16.22], which reflected a
greater novelty response for pictures than for words in both
hemispheres. When including hemisphere as a factor in the analysis, a
trend for a hemisphere × stimulus × novelty interaction was
observed [F(1,8) = 5.67;
p < 0.05 uncorrected]. Comparing the difference in
the percent signal change between novel and repeated pictures and words
indicated that although the word novelty response was similar in left
and right posterior fusiform regions
[F(1,8) = 1.01; NS], there was a
greater picture novelty response in the right relative to the left
posterior fusiform cortex [F(1,8) = 19.05].
In contrast to posterior fusiform regions, a left anterior fusiform
region demonstrated a pattern similar to that observed in the posterior
LIPC (Figs. 1, 2, region g). Specifically, this region revealed a main effect of stimulus type
[F(1,8) = 11.67] such that
activation in this region was greater during word relative to picture
encoding. Moreover, there was an effect of novelty [F(1,8) = 30.16], and the
stimulus × novelty interaction was not reliable
[F(1,8) = 1.21; NS], indicating that
novelty effects were observed for both pictures and words.
Word specific encoding pattern: prefrontal-lateral
temporal cortices
A third pattern of activation was observed in the
anterior LIPC and left lateral temporal cortex (Figs. 1, 2,
regions a, f). Both regions
revealed a main effect of stimulus type [anterior LIPC,
F(1,8) = 18.68; lateral
temporal cortex, F(1,8) = 22.45], with activation being greater during word relative to
picture encoding. Moreover, there was a greater response during novel relative to repeated stimuli [anterior LIPC,
F(1,8) = 56.89; lateral temporal
cortex, F(1,8) = 7.11;
p < 0.03 uncorrected]. Significant stimulus × novelty interactions [anterior LIPC,
F(1,8) = 13.96; lateral temporal
cortex, F(1,8) = 12.30] revealed
novelty effects selective for words [anterior LIPC,
F(1,8) = 32.77; lateral temporal, F(1,8) = 13.92] with reliable novelty
effects not being observed for pictures [anterior LIPC,
F < 1; lateral temporal,
F(1,8) = 1.51; NS]. As Figure 2
illustrates, activation in these regions was not above baseline for the
picture trials revealing that these regions selectively responded
during word encoding.
Content sensitive encoding activity: medial temporal lobe
Figure 3 illustrates medial temporal
lobe regions that demonstrated novelty responses. Both picture and word
novelty responses were observed bilaterally in the posterior
hippocampal region and parahippocampal and fusiform gyri. Voxels
demonstrating a word novelty response overlapped with those revealing a
picture novelty response. ROI analyses of bilateral
parahippocampal/fusiform regions demonstrated a significant novelty
response in both regions [left,
F(1,8) = 27.30; right,
F(1,8) = 22.81]. The main effect of
stimulus type was significant in both hemispheres [left,
F(1,8) = 92.27; right,
F(1,8) = 64.18], with both regions
demonstrating a greater response during picture encoding. The left ROI
failed to reveal a reliable stimulus × novelty interaction
[F(1,8) = 3.01; NS], whereas there
was a trend for an interaction in the right ROI
[F(1,8) = 10.46; p < 0.02 uncorrected]. These effects reflect the presence of a picture
novelty effect in both hemispheres [left,
F(1,8) = 29.28; right,
F(1,8) = 38.66] and a word novelty effect only in the left hemisphere [left,
F(1,8) = 8.75; right, F(1,8) = 2.71; NS]. When hemisphere
was included as a factor in the analysis, there was a trend for a
region × stimulus interaction [F(1,8) = 4.74; p < 0.07 uncorrected]. Although picture encoding did not differentially
activate the two hemispheres (F < 1), word encoding
resulted in more activation in the left than in the right parahippocampal/ fusiform cortex
[F(1,8) = 14.42].
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Figure 3.
Parahippocampal/fusiform regions engaged in novel
stimulus encoding. Columns A-C represent novel
stimulus, novel picture, and novel word comparisons, respectively. To
compare the percent signal change responses to novel pictures and novel
words in similar regions in both hemispheres, we used the coordinates
from the left parahippocampal/ fusiform ROI in the novel stimulus
condition to grow a region in the right hemisphere. a
(21, 40, 9; BA 35/36/37) and b (21, 40,
9; BA 35/36/37) reflect the percent signal change time courses from
these ROIs. Picture and word encoding activated overlapping regions of
the posterior MTL. Novel pictures, solid white line with
white squares; repeated pictures, dashed white
line with white squares; novel words,
solid yellow line with yellow squares;
repeated words, dashed yellow line with yellow
squares.
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Subsequent memory analyses
Having identified regions demonstrating novelty effects, we then
turned our attention to determining which regions predicted subsequent
memory performance as indexed by the postscan recognition memory test.
That is, we sought to determine whether the magnitude of activation
during encoding differed for items later remembered relative to those
later forgotten. The voxel-based subsequent memory comparison
(high-confidence remembered > forgotten trials) for pictures
revealed several brain regions that were more active during the
encoding of subsequently remembered than during the encoding of
subsequently forgotten trials, including the right hippocampus, right
parahippocampal and fusiform gyri, left parahippocampal and fusiform
gyri extending into the hippocampus, bilateral posterior cingulate
gyrus, and right intraparietal sulcus. Although the voxel-based
statistical threshold used in this study was p = 0.001, lowering our statistical threshold to p = 0.05 revealed
activation in the posterior RIPC, which is consistent with previous
findings (Brewer et al., 1998). Stereotaxic localizations of the
picture MTL subsequent memory responses were similar to previously
reported subsequent memory responses for pictures (Brewer et al., 1998) and for words (Wagner et al., 1998b). The voxels demonstrating a
picture subsequent memory response in the right hippocampus, left
parahippocampal/fusiform region extending into the hippocampus, and
right parahippocampal/fusiform region overlapped with MTL voxels
revealing picture and word novelty responses (see Figs. 3, 4). The
voxel-based subsequent memory analysis for the words did not reveal any
prefrontal or medial temporal regions that met our significance
criteria. This null result likely reflects a lack of power in this
comparison because due to the fact that there were relatively few
forgotten word trials (participants forgot 20.3% of the words compared
with 39.4% of the pictures).
Regions that demonstrated subsequent memory responses also revealed
novelty responses
To explore further possible subsequent memory effects for words in
view of Wagner et al.'s (1998b) findings of word subsequent memory
effects (see also Alkire et al., 1998; Henson et al., 1999; Petersson
et al., 1999; Wagner et al., 1999), as well as to investigate the
relationship between subsequent memory effects and novelty effects, ROI
analyses were conducted on MTL regions demonstrating a voxel-based
picture subsequent memory effect. These analyses revealed that MTL
regions that demonstrated picture subsequent memory effects also
revealed picture and word novelty responses and trends for word
subsequent memory effects (Fig. 4). The
right hippocampus (Fig. 4, region a) demonstrated
a main effect of subsequent memory
[F(1,8) = 11.85], with the absence
of a stimulus × subsequent memory interaction (F < 1). An ANOVA examining memory effects for words alone revealed a
trend for a subsequent memory response [F(1,8) = 4.67; p < 0.07 uncorrected], which suggests that both picture and word
subsequent memory effects were present in this region. Considering the
effects of novelty in this region, we observed a main effect of novelty
[F(1,8) = 14.59] and a trend toward
a reliable stimulus × novelty interaction
[F(1,8) = 4.89; p < 0.06 uncorrected], suggesting that there was a greater novelty response for pictures [F(1,8) = 53.50] than for words [F(1,8) = 17.59].
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Figure 4.
Medial temporal regions that were more active
during the encoding of pictures that were subsequently remembered than
during the encoding of pictures that were subsequently forgotten.
a, 28, 30, 6; hippocampus. b,
28, 37, 9; BA35/36/37. c, 31, 40, 6; BA
35/36/37. Graphs a-c, Subsequent memory percent signal
change time courses. Graphs
a1-c1, Novelty percent signal change
time courses for the same ROIs depicted in a-c,
respectively. Medial temporal regions that demonstrated picture
subsequent memory effects also revealed picture and word novelty
responses and trends for word subsequent memory effects. Graphs
a-c, Remembered pictures, solid white line with
white squares; forgotten pictures, dashed white
line with white squares; remembered words,
solid yellow line with yellow squares;
forgotten words, dashed yellow line with yellow
squares. Graphs a1-c1,
Novel pictures, solid white line with white
squares; repeated pictures, dashed white line
with white squares; novel words, solid yellow
line with yellow squares; repeated words,
dashed yellow line with yellow
squares.
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The left parahippocampal/fusiform and right parahippocampal/ fusiform
regions (Fig. 4, regions b, c)
observed in the voxel-based picture subsequent memory analysis also
revealed main effects of subsequent memory in ROI analyses [left,
F(1,8) = 30.82; right, F(1,8) = 11.42]. The stimulus × subsequent memory interactions were not reliable for either region
[left, F(1,8) = 1.40; NS; right,
F(1,8) = 1.24; NS]. ANOVAs examining
subsequent memory effects for words alone revealed a trend for a word
subsequent memory effect in the left parahippocampus/fusiform
[F(1,8) = 6.49; p < 0.04 uncorrected] but no word subsequent memory effect in the right
parahippocampus/fusiform [F(1,8) = 2.59; NS]. The hemisphere × stimulus × memory interaction
was not significant (F < 1). Considering the effects
of novelty in these regions, analyses revealed main effects of novelty
in both areas [left, F(1,8) = 34.69;
right, F(1,8) = 50.80], a trend for a
reliable stimulus × novelty interaction in the left
parahippocampus/fusiform [F(1,8) = 9.80; p < 0.02 uncorrected], and a significant
stimulus × novelty interaction in the right
parahippocampus/fusiform [F(1,8) = 17.54]. These results suggest that novelty effects were greater for
pictures [left, F(1,8) = 82.67;
right, F(1,8) = 83.53] than for words
[left, F(1,8) = 21.76; right,
F(1,8) = 10.35] in these regions.
Regions that demonstrated novelty responses also revealed
subsequent memory responses
Finally, to examine further the relationship between regions
demonstrating novelty effects and those demonstrating subsequent memory
effects, we examined the presence of subsequent memory effects in the
prefrontal and temporal ROIs observed to demonstrate novelty responses.
In general, those regions demonstrating novelty responses were also
observed to demonstrate subsequent memory effects. Specifically, the
posterior LIPC and posterior RIPC revealed trends for subsequent memory
effects [LIPC, F(1,8) = 8.23;
p < 0.03 uncorrected; RIPC,
F(1,8) = 4.69; p < 0.07 uncorrected]. Both left and right posterior fusiform regions
[left, F(1,8) = 11.65; right,
F(1,8) = 12.78] and the left anterior
fusiform [F(1,8) = 13.04]
demonstrated reliable subsequent memory effects, as did bilateral
parahippocampal/fusiform regions [left,
F(1,8) = 35.59; right,
F(1,8) = 27.21]. None of these
regions revealed significant stimulus × subsequent memory
interactions. It should be noted that the absence of stimulus × subsequent memory interactions should be interpreted cautiously because
the ability to detect content-sensitive subsequent memory responses
likely was limited by the modest number of forgotten word trials. The
left anterior LIPC revealed a trend for a subsequent memory effect
[F(1,8) = 5.69; p < 0.05 uncorrected] and a trend for a stimulus × subsequent memory
interaction [F(1,8) = 4.67;
p < 0.07 uncorrected]. This latter effect reflected
the presence of a subsequent memory effect in this region for words
[F(1,8) = 10.33] but not for
pictures (F < 1). Finally, in contrast to all the
other regions that had significant novelty effects in which we explored
subsequent memory responses, the left lateral temporal lobe did not
reveal a reliable main effect of subsequent memory
[F(1,8) = 1.44; NS]. At present, it
is unclear whether the absence of a subsequent memory effect in this
region reflects a lack of sensitivity/power or meaningful functional
differences between the processes mediated by this region and those
subserved by other prefrontal and temporal regions.
| |
DISCUSSION |
The present results forward our understanding of prefrontal and
temporal contributions to encoding by (1) clearly demonstrating the
presence of at least three patterns of encoding-related activation in
prefrontal and temporal regions that depend in part on event content
and (2) revealing that the same prefrontal, medial temporal, and
lateral temporal regions that are sensitive to stimulus novelty also
predict subsequent explicit memory, suggesting that these regions
actively contribute to encoding.
Posterior RIPC and bilateral posterior fusiform
Consistent with previous reports (Kelley et al., 1998; Wagner et
al., 1998a), the posterior RIPC (BA 6/44) responded preferentially to
picture encoding (Table 1). This observation builds on the proposal
that the inferior prefrontal cortex maintains items in working memory
(Petrides, 1994; Owen et al., 1996) and converges with the hypothesis
that the RIPC mediates control processes supporting access to and
maintenance of visuospatial and visuo-object representations (Awh and Jonides, 1998; Wagner, 1999). Importantly, the present study
extends these results by demonstrating a qualitatively similar encoding
pattern in posterior fusiform regions (BA 37) (Table 1). Other
neuroimaging studies have revealed posterior fusiform activation during
the processing of visual stimuli, such as scenes (Stern et al., 1996;
Gabrieli et al., 1997), faces (Haxby et al., 1994; Kanwisher et al.,
1997), objects (Martin et al., 1996; Chao et al., 1999; Ishai et al.,
1999), and words (Bookheimer et al., 1995; Chao et al., 1999), with
activation magnitude varying with stimulus novelty (Stern et al., 1996;
Buckner et al., 1998). In humans, damage to lingual and fusiform gyri
results in visual agnosia and prosapagnosia (Meadows, 1974; Damasio et
al., 1990), underscoring the importance of this region for object
recognition. Functionally and anatomically, the lingual and fusiform
gyri in humans may be analogous to the inferotemporal cortex in
monkeys, which plays an important role in object discrimination,
recognition, and memory processes (Iwai and Mishkin, 1969; Mishkin et
al., 1983; Desimone, 1996). The present observation of subsequent
memory effects in posterior RIPC and posterior fusiform regions
suggests that the operations mediated by these regions impact the
efficacy of encoding visuo-object representations.
Posterior LIPC and left anterior fusiform
A different encoding pattern was observed in the posterior
LIPC (BA 6/44) and left anterior fusiform (Table 1), with these regions
preferentially responding to word encoding (Kelley et al., 1998; Wagner
et al., 1998a). These results converge with neuroimaging evidence,
suggesting that the posterior LIPC supports access to and maintenance
of phonological codes (Paulesu et al., 1993; Awh et al., 1996; Fiez,
1997; Fiez and Petersen, 1998; Poldrack et al., 1999), and extend these
previous findings by revealing a qualitatively similar pattern in the
left anterior fusiform cortex. A similar fusiform/inferior temporal
region has been hypothesized to play a role in lexical/phonological
retrieval (Price and Friston, 1997; Brunswick et al., 1999; Mummery et
al., 1999), having been observed to be engaged during (1) word, object,
letter, and color naming (Bookheimer et al., 1995; Price and Friston,
1997), (2) reading tasks not requiring overt naming (Price et al.,
1996; Buchel et al., 1998), and (3) naming of tactile and auditory
stimuli (Buchel et al., 1998; Foundas et al., 1998). Moreover, lesions to the left BA 37 can yield anomia without semantic comprehension deficits (Raymer et al., 1997; Foundas et al., 1998). The present results suggest that the posterior LIPC and left anterior fusiform regions mediate phonological/lexical processes involved in word reading
and picture naming. The present subsequent memory effects indicate that
these processes may impact the efficacy of encoding of phonological representations.
Neuroanatomical studies in nonhuman primates have demonstrated strong
connections between the ventrolateral prefrontal cortex and
inferotemporal regions (Barbas, 1988; Felleman and Van Essen, 1991),
and electrophysiological and cortical cooling studies suggest that the
prefrontal cortex modulates inferotemporal processes (Fuster et al.,
1985; Tomita et al., 1999). The present observations that fusiform
activation is related to event content and subsequent explicit memory
raise the possibility that fusiform activation partially derives from
top-down modulation from the posterior RIPC and LIPC, and that it
contributes to the encoding of object and phonological/lexical features
into episodic memory. However, additional evidence regarding the
temporal dynamics and interactions across frontal-temporal regions is
necessary to further explore prefrontal-fusiform functional interactions.
Anterior LIPC and left lateral temporal lobe
A third qualitatively different encoding pattern was observed in
the anterior LIPC and left lateral temporal cortex. The anterior LIPC
has been observed to predict subsequent memory for words (Wagner et
al., 1998b). This result was extended by demonstrating that both the
anterior LIPC (BA 45/47) and left lateral temporal cortex (BA 21/22)
were associated with word specific encoding responses, with the
anterior LIPC also revealing a trend for word specific subsequent
memory effects (Table 1). Primate anatomical studies have demonstrated
that the ventrolateral prefrontal cortex is connected with the lateral
temporal cortex (Petrides and Pandya, 1988; Felleman and Van Essen,
1991). Although the posterior LIPC appears to be more active during
phonologically biased tasks, the anterior LIPC appears to be more
active during semantically biased processing (Fiez, 1997; Poldrack et
al., 1999) and thus is hypothesized to contribute to the accessing of
and working with long-term semantic knowledge (Kapur et al.,
1994; Demb et al., 1995; Fiez, 1997; Wagner, 1999). Within the
lateral temporal lobe, BA 21/22 has been shown to be active during
tasks that require the semantic processing of words (Fiez et al., 1996;
Vandenberghe et al., 1996; Price et al., 1997) and inanimate object
information (Martin et al., 1996; Mummery et al., 1998; Chao et al.,
1999). Patients with damage in this region have semantic processing
deficits including semantic dementia (Hart and Gordon, 1990; Hodges et al., 1992). Interactions between the anterior LIPC and lateral temporal
cortex may support the encoding of abstract semantic attributes into
memory, although at present it is unclear why the lateral temporal
cortex did not predict subsequent memory.
Medial temporal lobe
Within the MTL, posterior hippocampal and parahippocampal regions
were recruited during both picture and word encoding, with the
magnitude of MTL activity during encoding being observed to predict
subsequent memory (Brewer et al., 1998; Fernandez et al., 1998, 1999;
Grunwald et al., 1998; Wagner et al., 1998b). The finding of posterior
hippocampal/MTL activation complements previous neuroimaging evidence
of posterior MTL involvement in encoding processes. Consistent with
these previous studies, word encoding was associated with greater left
MTL responses, whereas picture encoding activated both hemispheres of
the MTL equivalently (Stern et al., 1996; Dolan and Fletcher, 1997;
Gabrieli et al., 1997; Martin et al., 1997; Kelley et al., 1998). Thus,
the two hemispheres of the MTL differentially contribute to the
encoding of events as a function of their content. Moreover MTL voxels
activated by word encoding overlapped with those activated by picture
encoding, suggesting that the encoding of ostensibly verbal and
nonverbal stimuli rely on similar MTL regions within a given
hemisphere. This similarity may reflect the ability of participants to
access visuo-object codes associated with words and phonological codes associated with pictures.
Novelty and encoding
Prefrontal and MTL regions respond differentially to novel
relative to repeated stimuli (Tulving et al., 1994; Knight, 1996; Stern
et al., 1996; Schacter and Buckner, 1998). Some have posited that this
differential response indicates that these regions mediate the
detection of situationally novel events (Knight, 1996; Tulving et al.,
1996; Dolan and Fletcher, 1997), with one consequence of novelty
detection being the facilitated encoding of these novel experiences
(Knight, 1996; Tulving et al., 1996). However, a link between regions
demonstrating a sensitivity to novelty and subsequent explicit memory
has not been established previously. The present results provide the
first evidence that the same ventrolateral prefrontal and temporal
regions that are sensitive to novelty also predict subsequent explicit
memory, supporting the hypothesis that these regions contribute to
encoding. However, it should also be emphasized that these regions
likely do not simply mediate novelty detection, because they predicted
subsequent memory even when situational novelty was held constant. The
colocalization of novelty and subsequent memory effects indicates that
the operations mediated by ventrolateral prefrontal and temporal
regions, operations that appear to impact the efficacy of encoding, are
engaged to a greater extent during novel events, perhaps yielding
richer and more effective episodic traces for initial relative to
repeated experiences.
Summary
In this study colocalized novelty and subsequent memory responses
were observed in prefrontal, lateral, and medial temporal cortices,
suggesting that these regions are actively engaged in encoding
processes, with novelty perhaps facilitating encoding. Moreover,
qualitatively similar encoding patterns were observed in anatomically
connected regions within the human ventrolateral prefrontal and lateral
temporal cortices. Three distinct prefrontal-temporal circuits likely
differentially contribute to the encoding of visuospatial, phonological/lexical, and semantic stimulus attributes. Prefrontal regions may contribute to encoding by modulating the processing of
these stimulus representations in lateral temporal cortices, with
medial temporal regions mediating associations between stimulus representations and other episodic features to form long-term, flexible
memory traces. Future research that integrates high spatial and
temporal resolution approaches, including fMRI and MEG, will provide additional insight into the temporal organization and top-down/bottom-up interactions that occur along the frontal-temporal axis during encoding.
| |
FOOTNOTES |
Received Feb. 10, 2000; revised May 19, 2000; accepted May 31, 2000.
This work was supported by the National Science Foundation (B.A.K.),
the Alzheimer's Association (C.E.S.), and the National Institute on
Aging (Grant AG 05778; A.D.W.). We would like to thank Terry Campbell,
Seth Sherman, Eena Khalil, and Doug Greve for their assistance with
this study.
Correspondence should be addressed to Brenda A. Kirchhoff, Department
of Psychology, Boston University, 64 Cummington Street, Boston, MA
02215. E-mail address: brendak{at}bu.edu.
| |
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D. Badre and A. D. Wagner
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L. Davachi and A. D. Wagner
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B. A. Strange, L. J. Otten, O. Josephs, M. D. Rugg, and R. J. Dolan
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TOP
ABSTRACT
INTRODUCTION
