HIPPOCAMPUS 17:1081–1092 (2007)
Perirhinal and Hippocampal Contributions to Visual Recognition
Memory can be Distinguished From Those of Occipito-Temporal
Structures Based on Conscious Awareness of Prior Occurrence
S.L. Danckert,1 J.S. Gati,2 R.S. Menon,2 and S. Köhler1*
ABSTRACT:
The ability of humans to distinguish consciously between
new and previously encountered objects can be probed with visual recognition memory tasks that require explicit old–new discriminations. Medial
temporal-lobe (MTL) lesions impair performance on such tasks. Within the
MTL, both perirhinal cortex and the hippocampus have been implicated.
Cognitive processes can also be affected by past object encounters in the absence of conscious recognition, as in repetition priming tasks. Past functional
neuroimaging findings in healthy individuals suggest that even in tasks that
require conscious recognition decisions for visual stimuli, posterior cortical
structures in the ventral visual pathway distinguish between old and new
objects at a nonconscious level. Conclusive evidence that differentiates the
neural underpinnings of conscious from nonconscious processes in recognition memory, however, is still missing. In particular, functional magnetic resonance imaging (fMRI) findings for the MTL have been inconsistent towards
this end. In the present fMRI study, we tested whether perirhinal and hippocampal contributions to recognition memory can be distinguished from
those of occipito-temporal structures in the ventral visual pathway based on
the participants’ reported conscious awareness of prior occurrence. Images
of objects with a large degree of feature overlap served as stimuli; they were
selected to ensure an involvement of perirhinal cortex in the present recognition task, based on evidence from past lesion-based research. We found that
both perirhinal cortex and occipito-temporal cortex showed a differential
old–new response that reflected a repetition-related decrease in activity
(i.e., new > old). Whereas in perirhinal cortex this decrease was observed
with respect to whether subjects reported objects to be old or new, irrespective of the true item status, in occipito-temporal cortex it occurred in relation to whether objects were truly old or new, irrespective of the participants’ conscious reports. Hippocampal responses differed in their exact pattern from those of perirhinal cortex, but were also related to the conscious
recognition reports. These results indicate that both perirhinal and hippocampal contributions can be distinguished from those of occipito-temporal
structures in the ventral visual pathway based on the participants’ reported
conscious awareness of prior occurrence. V 2007 Wiley-Liss, Inc.
C
KEY WORDS:
fMRI; medial temporal lobe; ventral visual pathway;
feature ambiguity; recollection; familiarity
INTRODUCTION
The ability of humans to distinguish between new and previously
encountered objects is crucial for adapting to their environment. This abil1
Department of Psychology, University of Western Ontario, London,
Ontario, Canada; 2 Centre for Functional and Metabolic Mapping, John
P. Robarts Research Institute, London, Ontario, Canada
Grant sponsor: Canadian Institutes of Health Research (CIHR).
*Correspondence to: Stefan Köhler, Ph.D., Department of Psychology,
University of Western Ontario, London, ON, Canada N6A 5C2.
E-mail: [email protected]
Accepted for publication 19 June 2007
DOI 10.1002/hipo.20347
Published online 14 August 2007 in Wiley InterScience (www.interscience.
wiley.com).
C 2007
V
WILEY-LISS, INC.
ity can be probed with recognition memory tasks that
require participants to consciously discriminate between
new and old stimuli. The performance on such tasks is
impaired in amnesic patients with medial temporal lobe
(MTL) damage, suggesting a critical role for the MTL
in conscious recognition memory (Moscovitch, 1995;
Aggleton and Shaw, 1996; Milner et al., 1998). Within
the MTL, both perirhinal cortex and the hippocampus
have been implicated, but their exact functional roles
remain a matter of controversy (Squire et al., 2004;
Murray et al., 2005; Eichenbaum et al., 2007).
Studies in amnesic patients have also shown that
perceptual processes can be affected by past encounters
with a particular stimulus even without successful conscious recognition (Moscovitch et al., 1993; Schacter
et al., 2004). Amnesic patients typically demonstrate
intact perceptual priming effects, i.e., facilitated stimulus identification for old as compared to new objects
(e.g., Schacter et al., 1993; Verfaellie et al., 1996).
Functional magnetic resonance imaging (fMRI)
research in healthy individuals has consistently
revealed differential neural activity in the ventral visual
pathway as a neural correlate of visual perceptual priming. For objects, such activity has characteristically
been found in those occipito-temporal and lateral
occipital regions that support object identification
based on shape information (van Turennout et al.,
2000; James et al., 2002; Vuilleumier et al., 2002;
Sayres and Grill-Spector, 2006). This evidence has
been interpreted in light of the notion that the same
brain structures that perform the perceptual identification of objects maintain a record of previously
encountered items as a by-product of the performed
analyses; this record is thought to be inaccessible to
conscious awareness (Tulving and Schacter, 1990).
Research based on event-related potentials and
fMRI suggests that, even in tasks that require conscious recognition decisions, some of the processes
supported by posterior cortical structures distinguish
between old and new stimuli at a nonconscious level
(Rugg et al., 1998; Slotnick and Schacter, 2004; Weis
et al., 2004). Conclusive evidence that differentiates
the neural processes that make nonconscious contributions from those that give rise to conscious awareness,
however, is still missing. While some fMRI studies
have provided clear support for an involvement of the
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DANCKERT ET AL.
hippocampus in conscious recognition processes (e.g., Eldridge
et al., 2000), other fMRI evidence hints that its contributions
to recognition memory may also pertain to nonconscious processes (Daselaar et al., 2006). Furthermore, while there is neuroimaging evidence that links perirhinal responses to consciously
perceived memory strength (Gonsalves et al., 2005), it has not
been systematically examined whether this signal can be double-dissociated from that of occipito-temporal or lateral occipital structures in the ventral visual pathway, which make ostensibly nonconscious contributions. This issue is important given
that the observed differential old–new responses in both regions
have been likened to repetition suppression as measured with
single-cell recordings in nonhuman primates (Wiggs and Martin, 1998; Brozinsky et al., 2005; Gonsalves et al., 2005; GrillSpector et al., 2006).
The evidence just summarized raises the question as to
whether the differential old–new fMRI signal in perirhinal cortex differs from that in occipito-temporal and lateral occipital
regions during recognition at the level of how ‘‘old’’ and ‘‘new’’
are defined. It remains to be determined within a single study,
taking all four response outcomes into account (i.e., Hits,
Misses, Correct Rejections, and False Alarms), whether the signal in perirhinal cortex can indeed be linked specifically to the
reported recognition experience of an item as being perceived
to be ‘‘old’’ or ‘‘new", whereas that in occipito-temporal and
lateral occipital regions reflects the true item status, irrespective
of the subjects’ conscious recognition reports. In the present
fMRI study we addressed this issue, as well as reexamined the
role of the hippocampus in conscious versus nonconscious recognition processes. For this purpose, we administered a recognition memory task that required old–new recognition decisions for images of objects with a large degree of overlap in
shape components. These stimuli were selected in order to
increase the likelihood to observe a differential fMRI signal in
perirhinal cortex, as research from several lesion studies in
human and nonhuman primates suggests that the integrity of
this structure is critical for their discrimination (Bussey et al.,
2002, 2003; Barense et al., 2005).
METHODS
Participants
Sixteen student volunteers participated in the study. The
data from two of these participants were excluded from our
final analyses because of their excessively low (i.e., at chance
level) recognition accuracy. The remaining 14 participants
(eight females) were 27.43 6 1.5 yr of age (Mean 6 SEM).
They were all right-handed and had normal or corrected-tonormal vision. Participants gave written informed consent
before participating in the study. The study was approved by
the Ethics Board for Health Sciences Research at the University
of Western Ontario. Participants received compensation for
their participation.
Hippocampus DOI 10.1002/hipo
Stimuli
Stimuli were digitized images of 3D rendered novel objects
that had no preexisting meaning to participants. The objects
were created using Rhinoceros modeling software (v.2; Robert
McNeel and Associates, Seattle, USA.). All objects were created
using unique combinations of a set of six parts, which were
arranged such that all objects had an axis of elongation and
were asymmetrical. Each object was comprised of one main
part and three to five smaller parts, resulting in a high degree
of overlap in shape across stimuli. Samples of these objects are
illustrated in Figure 1. The objects were presented to participants in grey on a black background and were 550 3 400 pixels in size.
Before commencement of the fMRI study, behavioral piloting was performed in 20 participants with an original set of
200 stimuli that were combined with an old/new recognition
memory task comparable to that used in the fMRI study. The
goal of this piloting was to finalize stimulus selection such that
the majority of subjects would achieve above-chance levels of
performance over the final set of stimuli, while maintaining a
sufficiently large number of errors that would allow for valid
fMRI comparisons. We performed an item analysis of the behavioral pilot data and removed those items from the original
set that participants failed to recognize consistently during
piloting. Removal of these items led to the final set of 186
items for the fMRI study, consisting of two subsets of 93 stimuli. The two subsets were counterbalanced across participants
in the fMRI study, such that each set served as targets (i.e., old
items to be presented at study) in half of the participants.
Procedure
Stimuli were projected via an LCD projector onto a transparent screen at a fixed distance that allowed for easy object
identification (at a visual angle of 158). Subjects viewed the
projected stimuli through an overhead mirror and were asked
to provide any behavioral responses manually, using an MRcompatible keypad. The behavioral paradigm was a recognition
memory task embedded in a typical study-test session. During
the study phase before scanning, participants viewed a set of 93
target stimuli three times while lying in the scanner. Objects
were presented for 2,500 ms each. Trials were separated by a
fixation period of 500 ms. Participants were instructed to
inspect and memorize each object carefully for a subsequent
memory test. Stimuli were presented in a pseudorandom order
such that no more than four consecutive items had similar
main characteristics (i.e., same main part or same number of
parts). Three additional practice stimuli were shown at the beginning of the study session, which were discarded from all
analyses in order to decrease primacy effects.
Following a 15 min delay period, participants performed an
old/new recognition memory test while undergoing fMRI scanning. Participants were familiarized with the test format on
practice trials immediately preceding the scanning session. During scanning, all objects from the study session, interspersed
fMRI OF RECOGNITION MEMORY FOR VISUAL OBJECTS
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back’’ task that required them to press a button whenever they
detected an item that was identical to the previous one.
Scanning Parameters and Data Analysis
FIGURE 1.
Experimental stimuli. Examples of 3D abstract
objects displayed as pictures in the recognition paradigm. Objects
were comprised of one larger central shape and three to five
smaller shape components, which were all chosen from a group of
six different shape types. Thus, the resulting 186 objects had a
large degree of feature overlap.
with an equal number of novel objects, were presented, making
for a total of 186 trials. Participants were asked to press one of
two response buttons to indicate whether the object was one
they had seen during the study session (old) or one that had
not been studied before (new). Again, the objects were presented in pseudorandom order such that no more than four
consecutive items included the same main parts or the same
number of parts or where of the same trial type (old or new).
Each object was presented for 2,500 ms and subjects were
required to provide their response while the stimulus was visible on the screen. Following the presentation of each object,
there was an intertrial interval of 10 s. This period was
included to optimize extraction of the fMRI BOLD signals
from neighboring recognition trials with minimal assumptions
about linearity (Bandettini and Cox, 2000). During the intertrial interval, participants listened to a series of four prerecorded single-digit numbers while a fixation cross was presented
on the screen. They were asked to respond by button press for
each number whether it was odd or even. This type of task has
been shown to be particularly valuable for the estimation of
baseline activity in MTL structures in past fMRI research
(Stark and Squire, 2001). The entire testing session was divided
into seven fMRI runs, each corresponding to 26 or 27 recognition trials.
Following the recognition memory test, two additional fMRI
runs were administered that served as ‘‘functional localizer’’ for
the identification of the lateral occipital cortex. This localizer
was adapted from previously published research (Kourtzi and
Kanwisher, 2000). It included 16 blocks per run, each 16 s in
length. In each block, 20 images of either intact or scrambled
objects were presented. In half of the blocks these objects were
familiar (i.e., nameable). In the other half of blocks they were
novel (i.e., nonsense) objects. Participants performed a ‘‘1-
All imaging was performed on a 4 Tesla whole body MRI
system (Varian, Palo Alto, California; Siemens, Erlangen, Germany). In an effort to optimize functional image quality and
BOLD signal contrast in anterior MTL regions, images were
acquired with a segmented T2* weighted spiral out acquisition
sequence (Greicius et al., 2003). Functional volumes were
aligned with the ACPC line with 19 contiguous 4-mm thick
slices per volume (volume acquisition time 5 2,500 ms, TE 5
15 ms, flip angle 5 408, FOV 5 220 mm, 64 3 64 matrix
size, four segments per plane; navigator-corrected). This slice
orientation was chosen so as to cover occipital and temporal
cortices entirely. Next, a constrained, three-dimensional phase
shimming procedure (RASTAMAP) was used to optimize the
magnetic field homogeneity over the prescribed functional
planes (Klassen and Menon, 2004). During each experimental
session, a T1-weighted anatomic reference volume was acquired
along the same orientation as the functional images using a 3D
spiral MDEFT sequence (256 3 256 3 128 matrix size,
1.5 mm reconstructed slice thickness, TI 5 1,300 ms, TR 5
50 ms, TE 5 3.0 ms). Each behavioral recognition trial and its
corresponding intertrial interval involved the collection of five
volumes.
Image preprocessing and statistical analyses of fMRI data
were performed using Brain Voyager 2000 software (v. 4.8; R.
Goebel, Brain Innovation, Maastricht, Netherlands). Functional
images were inspected to ensure that no motion artifacts were
present, and corrected for signal drift within runs using a highpass filter. Functional data were resampled into isotropic voxels
(3 3 3 3 3 mm3), coregistered with the anatomical images,
transformed into standardized space (Talairach and Tournoux,
1988), and superimposed on the anatomical images, which
were resampled into isotropic voxels of 1 3 1 3 1 mm3. Following transformation, images underwent smoothing with a
3D Gaussian Kernel and a full-width at half maximum value
of 6 mm. Statistical analyses were performed using the General
Linear Model (GLM). We first computed estimates for the critical event-related predictors for each subject and then entered
these estimates into a second-level analysis to assess their significance in a random-effects model (i.e., based on error variance
across subjects). The time-course of the hemodynamic response
was modeled with a gamma function in these analyses, and all
data were corrected for temporal auto-correlation.
The four critical event-related predictors in the GLM were
created based on participants’ responses (‘‘old’’ or ‘‘new’’) to old
and new items. They were examined in the context of an
ANOVA, involving a 2 3 2 factorial design, in which the two
factors were defined based on the participants’ reported conscious recognition experience (‘‘old’’ or ‘‘new’’) and based on
the actual item status (old or new). The mapping of the
response classification derived from signal detection theory
(Hit, Miss, False Alarm [FA] and Correct Rejection [CR]) onto
Hippocampus DOI 10.1002/hipo
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DANCKERT ET AL.
for a given contrast at P < 0.001, but no other effects in the
subsequent ROI analysis even at P < 0.05, would provide support for the notion that it responds selectively to the contrast
based on which it was identified. Given that the ROIs for the
follow-up ANOVAs were selected based on a novelty response
in one of the relevant contrasts to begin with, the resulting P
values must, however, be considered to be more descriptive
than exact (i.e., the analyses can be considered to be biased).
RESULTS
Behavioral Results
FIGURE 2.
MTL regions showing activity patterns related to
reported conscious recognition experience. fMRI activation maps
correspond to ANOVA-based group comparisons superimposed on
coronal and sagittal structural MR images of a representative subject. Graphs show the corresponding pattern of activity related to
each of the four behavioral response outcomes displayed in regression (b) weights and derived from the GLM analyses. Error bars
represent SEM. Both activation maps were thresholded at P <
0.005 for purposes of illustration. Top: Right perirhinal cortex
region demonstrating the main effect of conscious report. Bottom:
Left hippocampal region demonstrating the interaction of conscious report and item status.
this 2 3 2 matrix is displayed in the labeling of Figure 2 and
in Table 1. Statistical analyses also included the examination of
the interaction between the two factors in our design. Results
from the ANOVA were expressed as t-maps, thresholded at
P < 0.001 (uncorrected), and examined for activation in temporal and occipital cortices. Activation was considered significant
when at least six contiguous voxels reached threshold. Given
that both factors in our design were restricted to two levels,
subsequent pair-wise comparisons between conditions were performed only in activated regions in which a significant interaction was found.
Additional region-of-interest- (ROI) based analyses were performed on all regions in medial temporal, occipito-temporal,
and occipital cortices that showed a significant effect in the first
set of analyses. ROIs were created by selecting all contiguously
activated voxels within a volume of 6 3 6 3 6 mm3 centered
around the peak. These additional analyses served to probe the
functionally identified regions for potential subthreshold
responses associated with the other effects in the ANOVA.
Results from these tests were considered significant at a level of
P < 0.05 (uncorrected). We reasoned that, even with the most
lenient approach to thresholding, any effect that did not reach
this criterion would not be considered reliable. Following this
rationale, the identification of a region that showed an effect
Hippocampus DOI 10.1002/hipo
To separate activity related to the reported conscious awareness of novelty or prior occurrence from that related to nonconscious processes, performance levels are required that are
characterized by a substantial number of errors in recognition
decisions for both old and new items, while still being at an
above-chance level. In light of this goal, individual participants’
data were only included in the final analyses of the present
study if they achieved above-chance accuracy levels. To test
against chance, a one-sample t-test was computed for each subject with an error estimate obtained from the variance across
the seven runs (pooled across trials within each run). In other
words, for every subject we obtained an accuracy value for each
run, computed the mean of these values across runs, and tested
it against chance (population mean). The data from 2 of the
16 participants were excluded from our final analyses based on
a nonsignificant result for this test (t (6) < 2.14 corresponding
to P > 0.05). Performance levels on the recognition memory
test in the remaining sample are shown in Table 1. Accuracy,
calculated as Hits minus FAs, was found to be significantly
above chance level (i.e., 0) in a group-based t-test for this sample (t (13) 5 8.70, P < 0.001). Expressed in terms of absolute
numbers of responses, participants provided on average 54.79
Hits (SEM 5 3.34), 35.29 Misses (3.25), 32.14 FAs (2.59),
and 57.14 CRs (2.76). An ANOVA was also performed on the
mean median response times of participants. Only the interaction was statistically significant (t (13) 5 2.192, P < 0.05; Table 2), showing that participants responded more quickly when
they made correct than incorrect responses specifically when
the items were old.
TABLE 1.
Mean Percentage and SEM of Participants’ ‘‘Old’’ and ‘‘New’’
Responses to New and Old Objects
Participants’ responses
Item status
Old
New
Old
New
60.95% (63.55) Hit
35.95% (62.83) FA
39.05% (63.55) Miss
64.05% (62.83) CR
fMRI OF RECOGNITION MEMORY FOR VISUAL OBJECTS
TABLE 2.
Mean Median Reaction Times and SEM Across Participants for
Correct and Incorrect Responses to New and Old Objects
Participants’ responses
Item status
Old
New
Old
New
1464.32 ms (648.53)
1572.62 ms (662.01)
1529.61 ms (660.32)
1548.04 ms (653.47)
fMRI Results: Rationale for Analyses
To determine which brain regions show responses during
recognition that are related to the reported conscious experience of the items’ prior occurrence and which ones are not, we
analyzed the fMRI data with a 2 3 2 voxel-based ANOVA
including the factors ‘‘reported conscious recognition’’ and
‘‘actual item status". We reasoned that regions hypothesized to
make contributions pertaining to the conscious awareness of an
item as ‘‘old’’ or ‘‘new’’ should show either a significant main
effect for reported conscious recognition or a significant interaction between this factor and that of actual item status. In
other words, we assumed that any region in which the fMRI
response is modulated by the outcome of the recognition report
is involved in processes that support the conscious awareness of
prior occurrence or novelty. By contrast, we reasoned that
regions hypothesized to make nonconscious contributions
should show a significant main effect for actual item status in
the absence of a main effect for reported conscious recognition
and in the absence of any interaction. Table 3 lists all regions
that showed an effect in our ANOVA at P < 0.001 within the
scanned volume captured with our slice selection. Given the
nature of our hypotheses, however, we specifically focus on
medial temporal, occipito-temporal, and lateral occipital cortices in our more detailed description of results.
fMRI Results: Effects in the MTL
We first examined whether there were regions in the MTL
(defined collectively as hippocampus proper, entorhinal cortex,
perirhinal cortex, and parahippocampal cortex; see Amaral,
1999) that showed a significant main effect of conscious
reported recognition or a significant interaction at P < 0.001
(uncorrected) in a voxel-based ANOVA. When examining activity related to the main effect of reported conscious recognition, we found a region in an anterior portion of the right collateral sulcus, corresponding to perirhinal cortex (Insausti et al.,
1998; Pruessner et al., 2002), which showed greater levels of
activation for items reported to be new than those reported to
be old (Table 3). Further, probing of this perirhinal region
with ROI-based statistical tests revealed neither a significant
main effect of actual item status nor a significant interaction
(Table 4). The region is shown in Figure 2 together with its
response profile. Figure 3 displays the same region superim-
1085
posed on the T2*-weighted averaged scanning volume of a representative participant; the figure illustrates that our imaging
protocol allowed us to obtain a reliable signal in the vicinity of
the activated part of perirhinal cortex (which can be prone to
substantial imaging artifacts). As there can be substantial variability in the shape and size of perirhinal cortex across individuals, even following transformation into standardized space, we
also display this perirhinal region superimposed on the T1weighted MRI image that was obtained after averaging the
structural scans of all participants (Fig. 3). Based on the neuroanatomical landmarks provided in the volumetric protocol
developed by Pruessner et al. (2002), the superimposition supports our interpretation of this anterior MTL activation as
being localized in perirhinal cortex.
TABLE 3.
Coordinates and Peak Activity of all Regions Identified
in the Main Analyses
Talairach coordinates
Region
X
Y
Main effect of reported conscious recognition
New > Old
R perirhinal cortex
16
10
Old > New
L prefrontal cortex
221
33
L Caudate
212
16
L ventral occipital cortex
24
278
R ventral occipital cortex
33
281
Main effect of actual item status
New > Old
L prefrontal cortex
217
24
L orbitofrontal cortex
23
22
R lateral parietal cortex
55
214
R occipito-temporal cortex
46
251
R ventral occipital cortex
6
279
Old > New
NA
Interaction
Correct > Incorrect
R prefrontal cortex
55
24
L insular cortex
228
20
R caudate nucleus
17
19
L globus pallidus
212
2
R opercular cortex
53
1
L caudate nucleus
211
27
R caudate nucleus
10
28
L hippocampus
218
219
L cerebellum
236
225
R cerebellum
50
247
L cerebellum
26
251
R ventral occipital cortex
28
280
L cerebellum
221
281
R cerebellum
28
281
Incorrect > correct
NA
Z
t-value
227
6.19
10
9
213
217
25.37
24.97
26.18
25.71
36
22
26
29
215
4.36
5.83
7.37
4.62
6.06
25
25
1
21
5
14
21
27
230
222
212
223
226
223
4.70
4.51
6.19
4.58
4.97
5.88
4.67
5.25
6.63
4.72
5.82
5.02
4.71
5.02
Hippocampus DOI 10.1002/hipo
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DANCKERT ET AL.
TABLE 4.
Results From ROI-Based Follow-up Analyses in Medial Temporal and Occipito-Temporal Regions Identified in Table 3
Reported experience
Item
Interaction
Region
t-value
P value
t-value
P value
t-value
P value
R perirhinal cortex
L hippocampus
R occipito-temporal cortex
3.93
0.60
21.86
<0.001
ns
ns
20.06
0.35
3.00
ns
ns
<0.005
1.68
3.35
0.43
ns
<0.001
ns
ns for P > 0.05; df 5 13.
When examining activity related to the interaction term in
the ANOVA we identified another MTL region, namely a portion of the left hippocampus (Table 3 and Fig. 2). ROI-based
statistical follow-up tests for this region revealed no main
effects (Table 4). To characterize the observed interaction in
this hippocampal region further, we also conducted ROI-based
pair-wise comparisons between conditions. These comparisons
indicated that the hippocampal region displayed higher levels
of activation for CRs than for FAs (t (13) 5 3. 057, P <
0.005), as well as for Hits than for Misses (t (13) 5 2.732,
P < 0.01). In other words, activation in this left hippocampal
region was greater for correct recognition decisions than for
incorrect ones. Notably, the voxel-based ANOVA revealed no
other effects in the MTL, including the contrasts that focused
on increases for old as compared to new items or responses.
These results demonstrate that both perirhinal cortex and the
hippocampus make contributions to the reported conscious recognition experience in our task. In addition, they suggest that
the exact functional role each structure plays is distinct as the
exact pattern of responses across conditions differed between
them. A final ROI-based three-factorial ANOVA, in which the
original two-factorial design was extended to include MTL
region as an additional factor with two levels, confirmed this
dissociation in the perirhinal versus hippocampal response as a
significant three-way interaction (F (1,13) 5 16.74, P <
0.001).
fMRI Results: Effects in Occipito-Temporal and
Lateral Occipital Regions
Given that past research has identified the occipito-temporal
and lateral occipital cortex as core regions to support visual
object identification based on shape information (Grill-Spector
et al., 2001; Grill-Spector and Malach, 2004; for reviews), we
were specifically interested whether any ventral visual-pathway
regions at the level of lateral occipital cortex or anterior to it
showed any experimental effects. Indeed, our voxel-based analyses identified a right occipito-temporal region that was situated
just anterior to lateral occipital cortex (as identified with our
functional localizer averaged across participants and thresholded
at P < 0.001, uncorrected). This region showed an effect of
actual item status, with greater levels of activation for new than
for old items (Table 3 and Fig. 4). When further probed with
Hippocampus DOI 10.1002/hipo
ROI-based statistical follow-up tests, it showed neither a main
effect of reported conscious recognition nor a significant interaction, even when the threshold was lowered to P < 0.05 (Table 4). In lateral occipital cortex itself (as assessed with an ROI
derived from the functional localizer), activation was observed
only when the threshold for the item-status contrast was lowered to P < 0.05. That the effect of item status was strongest
in a region close but not identical to lateral occipital cortex is
likely a consequence of the difference in stimuli used for the
localizer as compared to the experimental recognition memory
task. While the latter were 3D rendered depictions of nonmeaningful objects, the stimuli for the localizer were all 2D line
drawings, some of which were meaningful while others were
not.
fMRI Results: Effects in Early Occipital Regions
Although not directly pertinent to our hypotheses, we also
explored whether there were effects in early occipital regions
(i.e., regions situated posterior to lateral occipital cortex as
identified with our functional localizer) in our voxel-based
ANOVA. We found three ventral occipital regions that showed
an effect. One right ventral occipital region displayed a main
effect of actual item status, with greater levels of activity for
new than for old items (Table 3). Two additional ventral occipital regions, one in the left and one in the right hemisphere,
displayed a main effect of reported conscious recognition, with
greater activation for old than for new responses (Table 3). Further probing of these early ventral occipital areas with ROIbased analyses revealed no clear-cut selectivity with respect to
conscious or nonconscious processes. The two regions that
were identified based on their main effect of reported conscious
recognition also showed a weaker effect for item status (right
t(13) 5 2.571, P < 0.01; left t(13) 5 2.211, P < 0.05). Furthermore, the early occipital region that was identified based
on the main effect of actual item status also showed a weaker
effect for reported conscious recognition (t(13) 5 3.235, P <
0.005). At the same time, none of these regions showed a significant interaction (P > 0.05, for both). A three-factorial
ROI-based ANOVA, with region as the third factor, revealed
that there was indeed no significant difference in response profiles across these early ventral occipital regions (all interactions
with region P > 0.05).
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between region and reported conscious recognition (F (1,13) 5
21.548, P < 0.001), as well as an interaction between region
and actual item status (F (1,13) 5 9.554, P < 0.01). These
two significant interactions show that the responses of perirhinal cortex and occipito-temporal cortex can be double-dissociated in terms of their conscious-report versus item-based
effects, respectively. A similar ANOVA in which we compared
the activity for the hippocampus with that of the occipito-temporal region also revealed a dissociation as reflected in a threeway interaction (F (1,13) 5 11.437, P < 0.01). Together, these
results demonstrate that the pattern of responses in both MTL
regions can clearly be distinguished from that in right occipitotemporal cortex based on a consideration of the participants’
reported conscious recognition awareness.
FIGURE 3.
Further displays of the observed perirhinal-cortex
activity. The fMRI activation map is identical to the one shown in
Figure 2 and corresponds to the main effect of conscious report in
this region. Top: Superimposition of this map onto the T2*weighted averaged image of another representative subject. Bottom:
Superimposition of this map onto the T1-weighted averaged structural image of all participants.
DISCUSSION
Perirhinal Versus Hippocampal Contributions
fMRI Results: Direct Comparison of Responses
in MTL and Occipito-Temporal Regions
Considered together, the response pattern in perirhinal as
well as in ventral occipito-temporal cortex can be described as a
repetition-related decrease in activity. Whereas in perirhinal
cortex this decrease occurred with respect to what subjects
reported to be old or new, in occipito-temporal cortex it
occurred based on whether objects were truly old or new. In a
final set of analyses, we confirmed that the MTL and occipitotemporal responses that were identified in our voxel-based
ANOVA could indeed be dissociated statistically. A three-factorial ANOVA, which served us to compare the perirhinal and
the occipito-temporal region, revealed both an interaction
FIGURE 4.
Right occipito-temporal region showing activity
pattern unrelated to reported conscious recognition experience. This
region (orange) showed a main effect of actual item status (thresholded at P < 0.005 for illustration purposes) and was situated ante-
All differential activity observed in the MTL in the present
fMRI study was found to be related to the participants’
reported conscious recognition experience. This evidence is in
good agreement with the consistently observed impairments in
conscious recognition that are associated with MTL damage in
neurological patients (Aggleton and Shaw, 1996; Buffalo et al.,
1998; Yonelinas et al., 2002; Manns et al., 2003). Our finding
for perirhinal cortex is of particular importance. Evidence from
lesion studies in nonhuman primates indicates that perirhinal
cortex is necessary for accurate performance on delayed nonmatching to sample tasks for objects, i.e., the experimental paradigm most frequently used to examine recognition memory in
nonhuman primates (Zola-Morgan et al., 1989; Meunier et al.,
1993; Baxter and Murray, 2001). Corresponding evidence from
selective lesion studies in humans is missing.
rior to the functional localizer of object-sensitive regions in lateral
occipital cortex (LOC; shown in green). For further details on display format, see Figure 2.
Hippocampus DOI 10.1002/hipo
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DANCKERT ET AL.
We tested recognition memory with visual images of nonmeaningful objects that contained a large degree of overlap in
shape components across items. These stimuli allowed us to establish that the contributions of perirhinal cortex, like those of
the hippocampus, pertain to the conscious awareness of
whether an object has been encountered before. An involvement of perirhinal cortex in our task was expected based on
lesion findings showing that the integrity of this structure is
essential for visual discriminations between stimuli with a large
degree of feature overlap (Bussey et al., 2002, 2003; Barense
et al., 2005). These findings have led to the proposal that perirhinal cortex is recruited in tasks, perceptual or mnemonic,
that require fine-grained object discriminations; perirhinal cortex is thought to represent conjunctions of shape features that
are individually insufficient to allow for unambiguous object
identification (Murray and Bussey, 1999; Bussey et al., 2005).
While consistent with such a proposal, the present findings do
not address whether perirhinal cortex does indeed make contributions to perceptual processing that go beyond its role in
memory (Hampton, 2005; Buckley and Gaffan, 2006; Cate
and Köhler, 2006).
In line with other lesion research, our findings also suggest
that MTL contributions from perirhinal cortex may not always
be sufficient to support successful recognition when finegrained object discriminations are required. Past lesion research
in humans has shown that additional hippocampal-based processes are essential when similar objects must be discriminated
individually, without lures being present for direct comparison
(as in a yes–no recognition task; Holdstock et al., 2002; Mayes
et al., 2002; Norman and O’Reilly, 2003). The present study is
the first to show in healthy human individuals that indeed
both perirhinal cortex and the hippocampus play a role in recognition memory for similar objects under such circumstances.
Our MTL findings also suggest that the specific functional
role of the hippocampus and perirhinal cortex is distinct. Notably, activity in the hippocampus tracked the accuracy of the
reported conscious recognition experience whereas activity in
perirhinal cortex did not. This pattern can be readily understood in the context of dual-process models of recognition
memory if, again, the nature of our stimuli is taken into
account. In the most prominent neuropsychological dual-process model, perirhinal cortex provides a signal that forms the
basis for consciously perceived item-familiarity, i.e., the sense of
having previously encountered an object irrespective of the
availability of specific details about the encoding episode
(Brown and Aggleton, 2001; Yonelinas, 2002). The decrease in
perirhinal activity we observed for reported old as compared to
novel items likely reflects this signal and is consistent with several similar findings in past fMRI (Henson et al., 2003; Brozinsky et al., 2005; Gonsalves et al., 2005; Köhler et al., 2005;
Montaldi et al., 2006) and electrophysiological studies (for
review, Brown and Xiang, 1998). As mentioned earlier, perirhinal signals are thought to be insufficient for recognition, however, when the previously encountered objects are similar to
novel lures and when they need to be judged one at a time
(Norman and O’Reilly, 2003); the high degree of similarity
Hippocampus DOI 10.1002/hipo
requires that additional recollective processes be recruited,
which serve to recover specific details from the encoding episode. According to the dual-process model, such conscious recollective processes are supported by the hippocampus (Eldridge
et al., 2000; Brown and Aggleton, 2001; Yonelinas et al.,
2002), i.e., the only MTL structure whose activity was linked
to successful performance in the present study and whose
response may thus reflect recollection. For new items, the hippocampal response may reflect the presence of additional
encoding processes, which have been shown to take place even
in the context of retrieval tasks (Buckner et al., 2001; Stark
and Okado, 2003) Although fitting and in line with other
recent evidence, this interpretation of our MTL data must be
considered speculative, as we neither probed recollection and
familiarity directly nor examined for evidence of encoding in
the recognition phase of our study. Nevertheless, inasmuch as
our rationale for mapping conscious and nonconscious processes onto the specific imaging contrasts we used is accepted,
our main conclusion that links all MTL functioning to conscious memory processing holds irrespective of whether this
particular interpretation is considered valid.
In another recent fMRI study, the authors came to a conclusion concerning the hippocampus that directly contradicts the
one presented here and therefore requires some discussion (Daselaar et al., 2006). Based on a similar experimental design and
based on similar analyses, Daselaar and colleagues reported that a
posterior MTL region in the vicinity of our hippocampal area
distinguishes between old and new items independent of conscious recognition awareness; their region showed a main effect
of actual item status in the ANOVA rather than the interaction
found here. Even in that study, however, the pattern of activation
was comparable to the present one in that posterior MTL
responses associated with correct recognition for old and new
items were numerically larger than those associated with incorrect
decisions. The higher level of accuracy, in particular the lower
number of false-alarm responses reported by Daselaar et al., may
have limited the power to confirm this pattern as a statistical
interaction and, thus, as evidence to support a role for the hippocampus in conscious processing. This interpretation, while speculative without the presence of further data, would also explain the
outcome of correlational analyses reported in that paper, which
revealed a relationship (across subjects) between the fMRI signal
in the same posterior MTL region and an accuracy measure computed based on the subjects’ conscious report. Such an interpretation of Daselaar et al.’s data would not, however, address why
there was a main effect of item status rather than no effect at all.
Notably, the stimuli (i.e., words) employed in that study did not
show the similarity and feature overlap that was a critical feature
of the current set. It is possible that the hippocampus only shows
a signal related to reported conscious recognition if monitoring
demands specified by prefrontal cortex trigger a detailed examination of relevant perceptual features; such processes are thought
to often be at the core of recollection (Schacter and Slotnick,
2004). If no such monitoring demands are present, the default
mode of hippocampal responding may be more akin to the one
shown by structures in the ventral visual pathway, and may not
fMRI OF RECOGNITION MEMORY FOR VISUAL OBJECTS
‘‘drive’’ the conscious report. Further research is necessary to validate this account of the discrepancy in hippocampal findings
across studies. Resolving the issue will likely require a systematic
investigation of the impact of different retrieval demands, and of
the resulting monitoring processes and shifts in response criteria
during recognition. Neuropsychological evidence has implicated
prefrontal cortex in the deficits of patients who show confabulations and abnormally high false-alarm rates on recognition tests;
it suggests that deficient monitoring process can have a direct
impact on what an individual experiences to be ‘‘old’’ or ‘‘new’’
(Schacter and Slotnick, 2004; Gilboa et al., 2006). In light of
such evidence, an fMRI based examination of hippocampal-prefrontal interactions should prove particularly informative for
obtaining a complete understanding of the relationship between
monitoring processes, response criteria, and reported conscious
recognition experiences (Fletcher and Henson, 2001; Simons and
Spiers, 2003).
Perirhinal Versus Occipito-Temporal and
Occipital Contributions
Unlike perirhinal cortex and the hippocampus, a ventral visual pathway region in right occipito-temporal cortex displayed
a pattern of activity that was unrelated to the conscious recognition reports. This region was situated just anterior to the lateral occipital area, which was identified with a functional localizer (e.g., Grill-Spector et al., 2001; Kourtzi and Kanwisher,
2001). It showed a decreased response to old as compared to
new objects irrespective of whether these objects were considered old or new. Decreases in occipito-temporal and lateral
occipital activity for previously encountered items have also
been reported in numerous fMRI studies of priming, for both
real and nonsense objects (e.g., van Turennout et al., 2000;
James et al., 2002; Vuilleumier et al., 2002). Although in priming studies participants are not required to consciously reflect
upon an item’s prior occurrence, it is well established that participants are sometimes aware that some of the primed items
were previously encountered in the experiment (e.g., Bowers
and Schacter, 1990). Therefore, findings obtained in fMRI
studies of priming in and of themselves do not establish
whether repetition-related activity decreases in the ventral visual
pathway are in fact decoupled from conscious recognition processes (Henson et al., 2003; Ganel et al., 2006). To make such
an inference, reports of conscious recognition awareness must
also be obtained (Schott et al., 2005; Slotnick and Schacter,
2006). Notably, when such reports were yoked to a behavioral
priming task (word-stem completion) in a recent fMRI study,
decreases in occipital and infero-temporal cortex activity were
indeed found even for those primed items that participants
failed to recognize as old (Schott et al., 2005). The current
findings extend this evidence by suggesting that similar
decreases in activity can also be observed under conditions in
which no task other than the recognition report is required,
and when the novel and previously encountered stimuli share a
high degree of perceptual feature overlap.
1089
Concerning the functional role of activity decreases in ventral visual pathway structures, it has been suggested that the familiarity component of recognition memory may rely on the
same processes of ‘‘perceptual fluency’’ that lead to behavioral
facilitation in perceptual priming tasks (e.g., Mandler, 1980;
Jacoby and Dallas, 1981). That the occipito-temporal effect we
observed here was decoupled from the participants’ conscious
reports of prior occurrence, however, does not support such an
account. Furthermore, that the perirhinal response decrease
could be double-dissociated from the occipito-temporal
decrease in terms of their relationship to conscious reports and
actual item status also argues against the idea that a familiarity
signal in perirhinal cortex is computed based on repetitionrelated signal decreases in upstream ventral visual pathway
regions (see also Wagner et al., 1997; Conroy et al., 2005).
Research conducted to elucidate the physiological mechanism
underlying repetition-related fMRI-activity decreases in the ventral visual pathway has likened it to the effect of repetition suppression in single-cell recordings (Wiggs and Martin, 1998).
Recent fMRI-based research suggests that such decreases may
reflect sharpening effects related to fine-tuning and feature selection in the cortical response to specific objects at the level of
neuronal populations (Zago et al., 2005; Grill-Spector et al.,
2006). The present results indicate that any such sharpening
effects in occipito-temporal cortex must be considered as functionally distinct from similar effects in perirhinal cortex.
Although the activity decreases in both of these structures can
be understood as a ‘‘record’’ of previously encountered stimuli
that emerges as the by-product of perceptual analyses performed
in the ventral visual pathway (Tulving and Schacter, 1990), our
results suggest that only the occipito-temporal records are
decoupled from conscious awareness of prior occurrence. It will
be important to explore in future research whether this dissociation between perirhinal and occipito-temporal responses also
holds under conditions in which judgements of perceptual fluency rather than recognition are required.
While our study was specifically concerned with occipitotemporal and lateral occipital regions in the ventral visual pathway that are known to support the identification of objects
based on their unique shape, we also explored activity in earlier
(i.e., upstream) ventral visual pathway structures. These analyses
revealed that not all occipital regions showed a response that
was decoupled from reported conscious recognition awareness.
In fact, several early occipital regions showed effects of both
actual item status and of conscious recognition report. Notably,
the latter effect in these regions did not reflect a repetitionrelated decrease in activity (as found in perirhinal cortex), but
an increase for old as compared to new responses. It may
reflect feed-back influences from later occipital and temporal
cortical regions through re-entrant connections, which are
known to play a role in many different aspects of vision (e.g.,
Di Lollo et al., 2000; Lamme and Roelfsema, 2000). In a
recent related fMRI study, Slotnick and Schacter (2004) also
found that some old-new responses in ventral visual pathway
regions are decoupled from the conscious awareness of prior
stimulus occurrence whereas other are not. Although the
Hippocampus DOI 10.1002/hipo
1090
DANCKERT ET AL.
regions they reported do not appear to be fully overlapping
with those reported here, likely due to some differences in
stimulus materials, the findings from both studies converge to
suggest a nonuniform role of occipital cortex in visual recognition memory.
CAVEATS AND CONCLUSIONS
The present findings critically rest on the assumption that
participants’ subjective reports provide a valid means to assess
their conscious recognition experience; the dichotomous reports
served to mark operationally what information passes the
threshold for conscious awareness of prior occurrence. Another
crucial assumption we made is that any brain region whose
response is related to the outcome of these reports contributes
to conscious memory processing. To what extent the report of
an individual is an appropriate reflection of her phenomenological awareness is a thorny issue that has plagued the empirical
study of consciousness beyond the domain of memory since its
inception. How such reports should be mapped onto specific
experimental contrasts to identify the neural correlates of conscious awareness is an issue that poses similar conceptual challenges in the realm of functional neuroimaging. Yet, many
researchers would agree that the understanding of the cognitive
neuroscience of consciousness has advanced even without
obtaining a consensus on these issues first (e.g., Köhler and
Moscovitch, 1997; Weiskrantz, 1997; Schacter et al., 1998;
Dehaene and Naccache, 2001; Rees et al., 2002; Maia and
Cleeremans, 2005). To the extent that the assumptions summarized above are accepted, the current study adds to this
understanding by pointing to an intricate interplay between
conscious and nonconscious memory processes in the MTL
and the ventral visual pathway when humans determine
whether an object has been encountered before or is novel.
Our findings indicate that the functional contributions of the
hippocampus and of perirhinal cortex can be distinguished
from those of occipito-temporal regions when their relationship
to the individual’s reported conscious recognition experience is
taken into account.
Acknowledgments
We are grateful to Jordan Poppenk who assisted in data collection and analyses. Zoe Kourtzi generously provided the stimuli for the functional localizer for lateral occipital areas. We
thank Roberto Cabeza for his input to an insightful discussion
of the findings reported by Daselaar et al. (2006) in relation to
the current study.
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